Next Article in Journal
Genome-Wide Development of Polymorphic SNP Markers and Evaluation of Genetic Diversity of Litchi (Litchi chinensis Sonn.)
Next Article in Special Issue
A Regulatory Mechanism on Pathways: Modulating Roles of MYC2 and BBX21 in the Flavonoid Network
Previous Article in Journal
The Development of Floral Scent Research: A Comprehensive Bibliometric Analysis (1987–2022)
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Abiotic Stress in Rice: Visiting the Physiological Response and Its Tolerance Mechanisms

Bhaskar Sarma
Hamdy Kashtoh
Tensangmu Lama Tamang
Pranaba Nanda Bhattacharyya
Yugal Kishore Mohanta
4,5,* and
Kwang-Hyun Baek
Department of Botany, Dhemaji College, Dhemaji 787057, Assam, India
Department of Biotechnology, Yeungnam University, Gyeongsan 38541, Gyeongbuk, Republic of Korea
Department of Botany, Nanda Nath Saikia College, Titabar 785630, Assam, India
Nano-Biotechnology and Translational Knowledge Laboratory, Department of Applied Biology, School of Biological Sciences, University of Science and Technology Meghalaya, Techno City, 9th Mile, Ri-Bhoi, Baridua 793101, Meghalaya, India
Centre for Herbal Pharmacology and Environmental Sustainability, Chettinad Hospital and Research Institute, Chettinad Academy of Research and Education, Kelambakkam 603103, Tamil Nadu, India
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Plants 2023, 12(23), 3948;
Submission received: 25 September 2023 / Revised: 6 November 2023 / Accepted: 22 November 2023 / Published: 23 November 2023


Rice (Oryza sativa L.) is one of the most significant staple foods worldwide. Carbohydrates, proteins, vitamins, and minerals are just a few of the many nutrients found in domesticated rice. Ensuring high and constant rice production is vital to facilitating human food supplies, as over three billion people around the globe rely on rice as their primary source of dietary intake. However, the world’s rice production and grain quality have drastically declined in recent years due to the challenges posed by global climate change and abiotic stress-related aspects, especially drought, heat, cold, salt, submergence, and heavy metal toxicity. Rice’s reduced photosynthetic efficiency results from insufficient stomatal conductance and natural damage to thylakoids and chloroplasts brought on by abiotic stressor-induced chlorosis and leaf wilting. Abiotic stress in rice farming can also cause complications with redox homeostasis, membrane peroxidation, lower seed germination, a drop in fresh and dry weight, necrosis, and tissue damage. Frequent stomatal movements, leaf rolling, generation of reactive oxygen radicals (RORs), antioxidant enzymes, induction of stress-responsive enzymes and protein-repair mechanisms, production of osmolytes, development of ion transporters, detoxifications, etc., are recorded as potent morphological, biochemical and physiological responses of rice plants under adverse abiotic stress. To develop cultivars that can withstand multiple abiotic challenges, it is necessary to understand the molecular and physiological mechanisms that contribute to the deterioration of rice quality under multiple abiotic stresses. The present review highlights the strategic defense mechanisms rice plants adopt to combat abiotic stressors that substantially affect the fundamental morphological, biochemical, and physiological mechanisms.

1. Introduction

Rice (Oryza sativa L.), a species of Poaceae, is a ubiquitous staple food worldwide, offering vital nutrients, including carbohydrates, thiamin, folate, calcium, iron, pantothenic acid, and energy [1,2]. Due to the global significance of this economically essential crop in supporting growing human populations and meeting extensive nutritional needs, improving grain production and quality standards is becoming increasingly important [3,4]. Although yields have plateaued in the cultivation of most cereals, including rice, in recent decades, climate change is a significant challenge that greatly influences breeders’ decisions regarding productivity and quality issues [5]. In the coming decades, persistent negative impacts of climatic change and global warming can cause shifts in the severity, duration, and frequency of abiotic stress in rice farming, jeopardizing agricultural sustainability and global food security [6]. By 2050, it is anticipated that global warming and changes in the climate will lower irrigated rice production by 7%, while the yields of rainfed rice will likely decline by 6% and, more conservatively, up to 2.5%, respectively [7]. Various strategies have been adopted in climate-resilient agriculture to promote long-term sustainability. The Green Revolution brought a substantial increment in rice productivity across the globe through the usage of promising and high-yielding rice varieties and the implementation of modern farming techniques like drip irrigation, biofertilizers, biopesticides, and usage of recommended doses of plant protection formulations (PPFs) [8].
Rice farming is under continuous exposure to a broad category of biotic (pathogen invasion and insect infestations) and abiotic (extreme temperatures, drought, cold, heavy metal toxicity, and salinity) stress-related factors leading to serious agricultural issues like poor grain production and quality deterioration [9]. Figure 1 depicts different abiotic stress-related factors that negatively impact rice farming considerably.
Heat stress and drought are major abiotic stressors that interfere with rice’s physiological, molecular, biochemical, and morphological responses, resulting in massive crop losses and compromises in quality [10]. It has become apparent that frequent exposure to high temperatures during rice cultivation appears to have detrimental effects in various tropical and subtropical countries, including India, China, Bangladesh, Pakistan, Thailand, and several African countries. This includes substantial declines in yield and quality, which can be attributed to the sudden occurrence of pollen sterility and loss of fertility [11]. According to Oladosu et al., frequent exposure to drought is detrimental to brown and milled rice, as it can drastically reduce the quality of grain production to a great extent [12]. On the other hand, a rise in temperature leads to a rise in humidity, making spikelets sterile [13]. The flower buds cannot mobilize essential nutrients like carbohydrates and derived products when subjected to extreme heat stress.
Chilling stress is another influential environmental stress that significantly impacts the rice plants’ normal growth and development, including the percentage of seeds that successfully germinate, the vigor of seedlings, the formation of tillers, the reproductive capacity of plants, and the maturity of grains [14]. Similarly, under salinity stress, invasive apoplastic ion transport drives Na+ uptake into rice shoots [15]. Likewise, the submersion of plants can have detrimental effects on various physiological processes, including oxygen and carbon dioxide exchange, light availability, and nutrient absorption. These adverse conditions can hinder the process of photosynthesis, exhaust energy reserves, and eventually lead to growth impairment or the mortality of plants [16]. According to Suwanmontri et al., rice farming under rainfed lowland ecosystems is severely affected by intense and rapid exposure to abiotic stressors, leading to significant damage both in terms of quality and quantity [17]. Furthermore, plants exposed to high amounts of heavy metals experience a decrease or complete halt in metabolic activities and exhibit morphological abnormalities, ultimately leading to a reduction in crop yield [18].
To adapt to these abrupt changes in environments, plants have established intricate response mechanisms for detecting environmental signals and displaying appropriate physiological, morphological, and biochemical adaptations. Abiotic stressors can trigger the up- or downregulation of various genes, activating or inhibiting multiple signaling pathways and enhancing the plant’s tolerance to different environmental challenges [19]. Therefore, a complex interaction of signaling cascades is required at the molecular level to recognize external stimuli and the subsequent awakening of defense mechanisms [16]. In recent years, significant advancements have been made in our understanding of how plants respond to abiotic stresses. This progress can be attributed to contributions made in plant physiology, genetics, biotechnology, and molecular biology. By building upon the existing knowledge of stress tolerance mechanisms in rice cultivars, it is possible to develop novel gene pools that exhibit enhanced resistance to abiotic stresses [20]. In light of the preceding, this review aims to assess the biochemical, physiological, and morphological responses of rice to different abiotic stimuli and identify the process parameters used to generate rice varieties that are tolerant to abiotic stress.

2. Morphophysiological and Biochemical Impacts and Tolerance Mechanisms in Response to Different Abiotic Stressors

2.1. Drought Stress

The environment has witnessed several persistent repercussions from global climate change, like alterations to the growing season, patterns of rainfall, severe droughts, and soaring temperatures. A significant impact of these changes is the serious threat posed to global rice production by drought stress [21]. Statistics show that 42 million hectares of rice in Asia are occasionally or frequently vulnerable to drought, significantly reducing yield [22,23,24]. According to Lafitte et al., rice suffers economic losses of 48–94% during the reproductive stage due to water stress and another 60% during the grain-filling stage [25]. Reduced cell development, elongation, expansion, and the disruption of plant antioxidant activity triggered by the buildup of reactive oxygen species (ROS) are all ways that drought stress affects rice yield [26].

2.1.1. Morphophysiological and Biochemical Responses to Drought Stress

Plants have different strategies to deal with drought, which include escape, avoidance, and tolerance. Escape involves adapting to a shorter life cycle or growing seasonally to reproduce before the environment becomes dry [27]. Avoidance focuses on maintaining a high water potential in plants by reducing water loss through stomatal control and having a well-developed root system for water uptake [28]. Tolerance, on the other hand, involves limiting the number and size of leaves in response to water scarcity, but this strategy can result in reduced yield [29]. Rice production is particularly impacted by three typical types of droughts: early water stress, which delays the transplantation of seedlings; mild intermittent stress with cumulative impacts; and late stress, which affects late-maturing varieties [30]. The root–canopy ratio, plant height, and dry weight decrease upon water scarcity exposure. Especially at the flowering stage of rice, the rate of photosynthesis, stomatal conductance, rate of transpiration, water potential of leaves, and the air–leaf temperature gap all experience a substantial decline [23]. During the reproductive stage, rice is highly susceptible to water stress, significantly reducing grain production with a drastic decrease in the number of whole grains and spikelets per panicle [31]. The major plant part that detects changes in soil conditions are the roots, which also play a pivotal role in how plants react to water stress. When studying rice root systems under drought stress, a significant positive association was observed between root diameter, depth, and overall plant health and vitality. In drought, plants lengthen their roots to use the water in the soil more efficiently [32]. In response to the drought, rice’s root length increases, enabling the plants to access deeper water reserves in the soil. Additionally, there is a notable reduction in the diameter of nodal roots, leading to the development of relatively finer roots that aid in resource conservation [33]. Many upland japonica rice cultivars can withstand drought because of their vast and deep root systems. In contrast, the indica subspecies of rice often experience a reduction in their growth period [34]. Rice is less adapted to water-scarce circumstances than other cereal crops. Upland rice cultivars’ deep root systems are considered good at sustaining yields under drought conditions. In contrast, lowland rain-fed rice crops are susceptible to fluctuating soil water levels, and specific genotypes have adapted to these circumstances by promoting root growth even before and throughout drought [35]. According to Banoc et al., rice plants with well-established root systems exhibit greater water stress resilience and can maintain productivity even under such conditions [36]. Root growth takes precedence over shoot growth when there is a water shortage. Notably, there is a significant disparity in the rate of sap leakage from the root network between rice genotypes that are tolerant to drought and those that are susceptible to it [37].
The rolling of leaves is an adaptive mechanism against water deficiency. This adaptation benefits plants in times of water scarcity and low soil moisture, as it effectively reduces transpiration rates and helps maintain a favorable water balance within plant tissues [38]. As the intensity of the drought stress increases, rice leaves often exhibit varying degrees of leaf rolling. Broader-leafed indica rice cultivars perform better in drought conditions than shorter, narrower-leafed varieties regarding biomass, stomatal conductance, and transpiration efficiency [39]. Furthermore, to sustain turgor conditions, plant cells subjected to drought attempt to regulate their osmotic potential by accumulating specific osmolytes. One of the most well-known osmolytes, proline, functions as a mediator in osmotic control to protect the cell against ROS while maintaining the integrity of the plasma membrane. Accumulation of proline is linked to increased resistance to stress [40].
Photosynthesis, a crucial metabolic process that regulates the growth and yield of crops, is influenced by drought and water stress. When water is scarce, the relative water content in plants is reduced. In response, plants employ water-saving strategies such as closing stomata, which reduces the intake of CO2, transpiration rate, and gaseous exchange and impedes electron transport, leading to the accumulation of ROS [41,42,43]. Drought stress limits the efficient operation of photosystems I and II (PSI and PSII), disrupts the function of rubisco, and hinders the electron transport chain and ATP synthesis [26,44]. In drought conditions, the efficiency of photosynthetic pigments such as carotenoids, phycobilin, and chlorophyll is diminished. This leads to insufficient absorption of light, inadequate light harvesting, and ineffective photoprotection, eventually leading to limited photosynthesis and a decrease in the production of photosynthates [45,46]. Moreover, carotenoid also has a role in plant signaling during stress; thereby, a reduction in their content can detrimentally affect signal perception during drought stress [47]. Multiple studies have documented the effects of drought stress on the structural integrity of chloroplasts, chlorophyll production, and photosynthesis. When subjected to drought stress, chloroplasts change shape, transitioning from oval to nearly round. Additionally, they move from the cell wall toward the center of the cell, and the thylakoids within the chloroplasts become disorganized [48]. Another study observed irregularly shaped chloroplasts with swollen thylakoids in response to drought stress [49]. The severity and duration of the stress and the specific plant species or genotype determine the extent to which chloroplast integrity is affected [50]. Drought stress leads to the accumulation of ROS, predominantly in chloroplasts and to some extent in mitochondria, resulting in oxidative stress [51]. Furthermore, ROS produced in the chloroplasts of water-stressed plants can negatively regulate the expression of genes related to photosynthesis and chlorophyll production via retrograde signaling [52,53].
Direct or indirect oxidative stress in water scarcity conditions causes cell membrane lipid peroxidation in plants, which in turn stimulates a cascade of physiological and biochemical changes with the potential to disrupt metabolism and negatively impact crop yield and quality [54]. During drought stress, the plant’s ROS overproduction causes an abnormal decrease in photosynthetic electron chains [55]. Various ROS, such as hydroxyl radical (HO·), hydrogen peroxide (H2O2), and superoxide anion (O2), are generated by multiple cell organelles. These ROS trigger oxidative damage to cellular components, DNA fragmentation, the suppression of enzyme activity, and lead to lipid and protein peroxidation. They also initiate programmed cell death pathways, ultimately leading to cell death. Antioxidants are vital plant nutrients that scavenge ROS. Therefore, enhancing the expression of antioxidants boosts the rice plants’ ability to withstand drought. Non-enzymatic antioxidants such as ascorbate (AsA), tocopherol, and glutathione (GSH), are different from catalase (CAT), glutathione reductase (GR), ascorbate peroxidase (APX), superoxide dismutase (SOD), and monodehydroascorbate reductase (MDHAR), which are enzymatic antioxidants. The metabolic processes of SOD, CAT, peroxidase (POD), and soluble sugars were elevated in drought-tolerant rice cultivars, whereas malondialdehyde (MDA) level was reduced [56]. At the time of the filling phase, the drought would swiftly increase the activities of POD and CAT while slightly decreasing SOD activity, reducing AsA and GSH contents, and maintaining low levels of H2O2 and MDA. It is commonly accepted that drought causes increased POD and CAT activities of leaves [33]. The removal of H2O2 is significantly aided by the use of ascorbic acid, which is an essential antioxidant. During the ascorbic acid-glutathione cycle, APX employs two of the ascorbic acid molecules to catalyze the breakdown of H2O2 into water. This reaction was followed by the synthesis of monodehydroascorbate. As rice’s drought stress increases, the AsA content of functional leaves drops [57]. Enhancing the content of naturally occurring antioxidants (both enzymatic and non-enzymatic) could be a tactic to lessen or stop oxidative damage and boost plant resilience to drought. During drought, redox-sensitive flavonoids and phenolic acids are synthesized to counteract ROS and bind transition metal ions required for the Fenton reaction [58]. Redox-sensitive phenolic acids (protocatechuic acid, gentisic acid, syringic acid, gallic acid, caffeic acid, salicylic acid (SA), and p-coumaric acid) and flavonoids (rutin, catechin, kaempferol, quercetin, naringin, apigenin, and myricetin) provide drought-tolerant rice cultivars with the capacity to sustain redox homeostasis [59]. Polyamines, which are small molecules with a positive charge, affect rice’s adaptation to stress from drought. Some polyamines identified in plants include putrescine, spermidine, and spermine [60]. They can interact with several signaling networks and control homeostasis, osmotic potential, and membrane stability. When rice plants are subjected to drought stress, there is an elevation in polyamine levels, which is associated with enhanced photosynthetic activity, decreased water loss, and improved ability to detoxify and adapt to osmotic stress [61]. Carotenoids are crucial members of the antioxidant defense system because they prevent the synthesis of singlet oxygen, stabilize triplet chlorophyll in tissues under stress, and shield plants from oxidative damage. As a result, rice’s carotenoid content rises to counteract oxidative stress [62].

2.1.2. Molecular Response to Drought Stress

Rice plants have developed complex mechanisms to survive different abiotic stresses. These mechanisms allow them to adapt or avoid stress by responding optimally. Abiotic stressors are often interconnected and cause damage to plant cells, resulting in oxidative stress [63]. When plants encounter stress, membrane receptors detect the initial signals and transmit them to initiate transcription. This process is controlled by hormones, transcription factors (TFs), and transcription factor-binding proteins (TFBPs). These factors work together to activate stress-responsive mechanisms, repair damaged proteins and membranes, and restore homeostasis [64] (Figure 2). Inadequate response at any stage of the signaling and gene activation process can lead to permanent alterations in cellular equilibrium, breakdown of functional and structural proteins and membranes, and ultimately, cell death [65].
To combat water scarcity, drought stress in rice activates both abscisic acid (ABA)-dependent and ABA-independent signaling pathways [66]. It works via extensive and intricate signaling pathways to regulate drought stress. This involves adjusting the physiological, biochemical, and molecular attributes of the rice to improve the root’s ability to acquire more water and the stomata’s ability to lose less water. This adaptation helps the plants cope with water scarcity stress. Plants respond to drought stress by narrowing their stomata to reduce water loss, improve water utilization efficiency, and enhance their chances of survival [67,68]. ABA governs the movement of stomata to lessen the transpiration rate under drought stress [69,70,71]. ABA receptor, OsPYL/RCAR5, has been demonstrated to exert a positive regulatory effect on the expression of genes that are responsive to abiotic stress, and overexpressing the OsPYL/RCAR5 gene additionally enhanced transgenic rice’s ability to withstand drought [72]. Research has demonstrated that rice DREB transcription factors are essential controllers of ABA-independent drought responses. Rice cultivars that overexpress OsDREB1F exhibited improved drought tolerance, indicating that this gene mediates the ABA-dependent pathway [73]. When rice undergoes drought stress, the root system improves cuticle resilience and boosts the number, density, and depth of root hairs [74]. One key component in achieving that is DRO1, a combined quantitative trait locus (QTL) linked to root depth, which is upregulated in response to drought stress, promotes deeper growth of roots, and enhances tolerance against drought [75]. It also regulates the elongation of cells of the root tip, asymmetric growth, and bending of the root tip. When transformed with DRO1, rice cultivars with shallow roots become drought tolerant by establishing a deeper root system [75]. Drought resistance also depends on genes related to osmotic adjustment, equilibrium of stomatal activity, water-use effectiveness, phytohormones, and root and shoot biomass. Various genes, like OsPYL/RCAR5 and EcNAC67, cause delayed leaf rolling and increased root and shoot mass under drought stress [72,76]. Drought resistance in rice is improved by EcNAC67 overexpression. When exposed to water stress, in comparison to non-transgenic ASD16, transgenic plants displayed delayed leaf rolling signs. Additionally, they revived quickly after re-watering, retained a 20% higher relative water content in the leaves, and experienced a less pronounced decline in plant height and yield [76]. Research studies revealed that the DSM1 gene, a Raf-like MAPKKK, might modulate ROS scavenging to mediate drought responses in rice [77]. Table 1 presents a summary of key genes associated with drought resistance in rice.
It has been noted that seed priming is an effective strategy to reinforce the antioxidative defense system and enhance plant stress responses. One study observed a notable increase in antioxidant activity, total phenolic content, and expression of RD1 and RD2, rice drought-responsive genes belonging to the AP2/ERF family in two different rice genotypes, Nagina-22 (known for its drought tolerance), and Pusa Sugandh-5 (known for its drought sensitivity). This upregulation was observed when the seeds of these genotypes were primed with different plant hormonal or chemical elicitors, such as methyl jasmonate, SA, and paclobutrazol, under drought stress [98]. Rice that has been colonized by Trichoderma harzianum isolates is drought tolerant, grows faster, and experiences a delay in the effects of drought [99]. Colonization boosts rice’s ability to acquire and store water and root growth. In colonized plants, there is a lesser increase in the concentration of stress-induced metabolites.

2.2. Heat Stress

Global food security is now seriously threatened by heat stress brought on by a fast-changing climate. When the temperature rises above a specific point and continues for a while, it is said to be under heat stress, which can permanently harm plant growth and development [100]. Without effective adaptability, CO2 fertilization, and genetic development, it is predicted that every one-degree rise in the global mean temperature will result in lower worldwide yields of wheat, rice, maize, and soybeans [101]. Rice can grow normally at temperatures between 27 and 32 °C. Above 32 °C, all phases of growth and development of plants are negatively affected. The flowering stage, however, required a temperature of 33 °C. Heat damage occurs when rice is exposed to air temperatures above 35 °C [102].

2.2.1. Morphophysiological and Biochemical Responses to Heat Stress

Rice has three types of heat stress resistance: defense, avoidance, and tolerance. Heat defense is the mechanism of controlling morphological development and transpiration of leaves to lower the temperature of the panicles and avoid deterioration from scorching temperatures [103]. Heat avoidance includes adjusting spikelet flowering time by shortening the flowering period and early blooming, which is a desirable characteristic for developing heat-resistant rice cultivars [104]. Heat tolerance is the ability to continue generally living in hot temperatures. In response to heat stress, rice adjusts its physiochemical processes, which comprises growth retardation, leaf rolling, the senescence of leaves, and changes to fundamental physiological functions such as photosynthesis, respiration, the permeability of membranes, and ROS, that minimize the pollen sterility [105].
In addition to the hormone synthesis that influences the growth and development of shoots, the roots play essential roles in water intake and nutrients [106]. Although root systems are crucial in helping plants adapt to high temperatures, their thermotolerance mechanism has been less explored. Most of the research has focused on studying the aerial parts of plants [107,108]. Root growth is more susceptible to high temperatures than shoot growth, due to its lower optimal temperature [109]. Typically, when soil temperatures are elevated, a decrease in root growth and physiological activity occurs before the cessation of shoot growth [110]. A study showed that the rice plant roots failed to elongate and divide at a temperature of 43 °C [111]. Heat stress can affect rice plants during most of their vegetative growth stages. When temperatures are consistently high, the potential for seed germination decreases, resulting in a lower germination rate and weaker seedling growth [112]. When exposed to heat stress (42–45 °C), the seedlings experience increased water loss, wilting and yellowing of leaves, hindered growth of roots and seedlings, and in severe cases, death of the seedlings [102,113]. Similarly, rice seeds failed to germinate upon continuous exposure to a constant temperature of 43 °C [114]. In addition, another study found that rice plants died in the initial vegetative phase when exposed to a constant air temperature of 40 °C and high levels of CO2 (700 ppm) [115]. Furthermore, when a sequence of distinct heat stress treatments was applied to rice seeds, young seeds, in particular, were the most vulnerable in the initial two days following flowering [116].
Rice plants are more vulnerable to heat stress during the reproductive stage than the vegetative stage, including initiation of panicle, development of male and female gametophytes, anthesis, pollination, and fertilization [117,118]. Under heat stress (40 °C day/35 °C night) for 15 days, rice output per plant was 86% lower overall, and the panicle number was roughly 35% lower [119]. In japonica rice, compared to indica rice, heat stress significantly impacts the number of tillers and panicles [120]. When the rice plant enters the flowering stage, it becomes highly vulnerable to elevated temperatures. The second-most vulnerable stage appears around nine days before blossoming. Significant rises in temperatures during anthesis cause a high proportion of spikelets to be sterile. During the grain-filling stage, heat stress has been observed to impact the quality of rice negatively. This is evident through a decrease in palatability, an unfavorable grain appearance, and an increase in grain chalkiness [121,122,123,124]. The presence of chalky kernels is considered the most prominent indication of heat stress during this particular phase of rice development. During the panicle-initiation stage, heat-stressed plants experience a decrease in non-structural carbohydrates, underdeveloped vascular bundles, and smaller glumes, ultimately reducing grain weight [125]. The total grains and rice production percentage declines as nighttime temperatures rise. White immature kernels are formed when rice plants endure exposure to high temperatures at the ripening stage, disrupting the carbohydrate sink–source balance. The increased rhizosphere temperature causes the total dry weight of super rice to decrease by 16.26% [126].
A reduction in the stomatal aperture size, the xylem in the leaves, and an increase in the trichome density on both surfaces are additional examples of common adaptive responses to heat stress [127]. Photosynthesis is a crucial biochemical function in plants that is most susceptible to heat. The main sites of injury at high temperatures in chloroplast are light-dependent reactions in the thylakoid membrane and carbon fixation reactions in the stroma [128]. High temperature has a strong affinity for the thylakoid membrane. Significant changes in chloroplasts include changed thylakoid structural arrangement, loss of grana stacking, and grana swelling during heat stress. Heat shock decreases the number of photosynthetic pigments. At extreme temperatures, the enzymatic activities of invertase, ADP-glucose pyrophosphorylase, and sucrose phosphate synthase are diminished, leading to a substantial decrease or complete cessation of the function of PSII [129,130].
Heat stress-induced imbalance in metabolic activities, including photosynthesis and respiration, results in a rise in ROS or a fall in the cell’s efficiency to scavenge oxygen radicals. When exposed to high temperatures, rice anthers produce much more ROS, decreasing floret fertility and pollen viability [131]. MDA, a reliable indication of free radical damage to cell membranes, is produced when membrane lipids under heat stress undergo peroxidation. Increased lipid peroxidation demonstrated that oxidative stress frequently developed in rice leaves following exposure to high temperatures [132]. Various enzymes and metabolites take part in the antioxidant defense framework. The antioxidant enzymes, such as SOD, APX, CAT, GR, glutathione peroxidase (GPX), and peroxiredoxins, assist in shielding the cells from an accumulation of ROS. Furthermore, Phenolic chemicals can remove ROS, neutralize singlet and triplet oxygen, or break down peroxides. Moreover, the GSH molecule has a crucial function in protecting the photosynthetic system [133].

2.2.2. Molecular Response to Heat Stress

Heat stress signals are sensed through numerous heat shock transcription factors (HSTFs) and proteins. Various genes related to Ca2+ homeostasis, ROS, lipid metabolism, and phytohormones are activated to trigger the response against heat stress [134]. In rice, a large number of high-temperature-related genes, including stress-related transcription factors (TFs), HSTFs, and heat shock proteins (HSPs), have been cloned. These genes are involved in heat stress-related temperature sensing and response [135] (Table 2). OsHSP26.7, for instance, encodes an HSP that shields chloroplasts from oxidative damage brought on by extreme heat and ultraviolet radiation [136]. Similarly, under the HSP101 promoter, OsWRKY11 encodes a TF with a WRKY domain that can dramatically increase rice’s tolerance towards heat and drought [137]. Furthermore, a NAC TF called SNAC3 mediates ROS metabolism, and OsMYB55 TF in rice significantly improves tolerance to high-temperature and increases grain yield [138,139]. The HYR gene is a crucial regulator that can directly activate photosynthesis and can control downstream genes involved in carbon metabolism as well as morphology and physiology during drought and heat stress, maintaining the yield of rice [140]. The cytoskeleton plays a vital role in the ability of organisms to tolerate and adapt to stressful conditions. In the case of rice, a specific intermediate filament called OsIF has been identified as being particularly important in mitigating the implications of heat and salinity stress on the photosynthetic apparatus and overall crop yield [119]. Additionally, several enzymes, including glutamate decarboxylase and glutamine synthase, are some of the additional key factors that produce stress-related amino acids that aid rice in tolerating extreme heat [139,141]. A mitochondrial lipase known as EG1 can activate the expression of floral organ genes during high temperatures, thereby preserving the consistency of floral organ growth [142]. Table 2 presents a summary of key genes associated with heat stress tolerance in rice.
As a key defense against heat stress, plants accumulate soluble carbohydrates like glucose and fructose as well as non-soluble sugars like starch [156]. Under acute heat stress, the expression of OsSUT1, a sucrose transporter, is elevated, which results in increased sugar buildup and reduced photosynthesis [157]. Tolerance to high temperatures in plants is greatly influenced by the accumulation of certain metabolites. Under intense heat, the MYB55 TF in rice controls the expression of downstream glutamate dehydrogenases GAD3 and glutamine synthase OsGS1.2, thus promoting the buildup of stress-related amino acids like gamma-aminobutyric acid (GABA) and L-glutamic acid [139]. The analysis of the temporal transcriptome of germinating seeds subjected to heat stress at 35 °C reveals that the early response to heat stress is mediated by the Inositol-requiring enzyme 1 (IRE1)-mediated endoplasmic reticulum (ER) stress response and the jasmonic acid (JA) pathways. As JA promotes the spliced form of OsbZIP50, a gene marker linked to the IRE1-specific pathway, it is hypothesized that the rise in JA concentration levels during heat stress may happen before the ER stress response [116]. Numerous genes associated with high-temperature responses have been documented, leading to a better understanding of the signaling pathways in which they participate. Nevertheless, the precise molecular processes and regulatory systems underlying sensing of high-temperature signaling and transmission to downstream components remain inadequately recognized, thus necessitating further investigation as the critical area of prospective studies.
Ethylene, a crucial plant hormone, significantly regulates biotic or abiotic stress signaling. In the case of heat stress in rice seedlings, ethylene-mediated signaling has been found to mitigate oxidative damage, preserve chlorophyll levels, and enhance thermotolerance [158]. Specifically, under heat stress conditions, ethylene-mediated signaling controls the mRNA transcripts of certain heat stress transcription factors (HSFs) and genes related to ethylene signaling [125]. Phytohormones are also crucial in controlling how rice yield qualities react to heat stress. Specifically, cytokinin and abscisic acid (ABA) regulate the number of spikelets per panicle under high-temperature conditions. Additionally, gibberellin and indole-3-acetic acid may be associated with spikelet fertility, while indole-3-acetic acid, ABA, gibberellin, and cytokinin regulate grain weight [100].
When exposed to heat stress, foliar sprays of boric acid (25, 50, or 100 mg L−1) or sodium borate (50 mg L−1) substantially boosted net photosynthetic rates in comparison to untreated plants [159]. The use of foliar borate compounds on seedlings experiencing heat stress led to a decrease in oxidative damage, as indicated by the reduction in the levels of leaf MDA and proline synthesis and an enhancement in the photochemical efficiency of PSII.

2.3. Cold or Low-Temperature Stress

Rice is sensitive to cold, especially during the germination process, which causes significant economic losses. The dynamics of the crop’s growth are negatively impacted by cold stress in temperate and high-altitude rice-growing regions in the tropics and subtropics [160]. Cold stress has detrimental consequences on rice, such as decreased seedling growth, poor germination, constrained leaf expansion, chlorosis, and wilting. Necrosis, or tissue death, is the final impact of these factors [161].

2.3.1. Morphophysiological and Biochemical Responses to Cold or Low-Temperature Stress

In circumstances of cold stress, the growth of rice shoots and roots is hindered in terms of length, fresh and dry weight, and protein content [162]. A research study found that when exposed to cold stress, the root growth and developmental characteristics of various genotypes of rice decreased, ranging from 2% to 87% [163]. Furthermore, when rice is subjected to cold stress during the vegetative stage, the leaves begin to yellow, the plant grows shorter, and the number of tillers decreases [164]. Rice’s ability to germinate, as well as its coleoptile and radicle growth, is significantly reduced by low temperatures. Inhibition of seed germination and growth retardation or death of the seedlings cause a decline in crop yield [165]. The reproductive phase of rice, specifically in the post-meiotic stages of anthers, has a pronounced impact on pollen production due to cold stress [166]. In addition, cold temperatures during the immature microspore stage of rice anthers lead to heightened protein degradation. Other effects of cold stress comprise damage to the photosynthetic apparatus, including modifications to the number of chloroplasts, ultrastructure, light-harvesting chlorophyll antenna complexes, modified grana arrangement, and lamellar structures [164,167]. Thus, there is a shortage of plant energy resources since cold temperatures generally slow photosynthetic processes. This is due to the reduced activity of several enzymes involved in tetrapyrrole metabolism and the down-regulation of gene expression, which affects chlorophyll production [164]. The circadian clock is crucial for rice’s reaction to chilling stress. Night chilling stress affects leaf chlorophyll metabolism and PSII more severely than its daytime equivalent [168]. Additionally, nitrogen intake has often been found to be restricted by chilling stress in rice [169]. Numerous studies have shown that stress caused by low water temperature reduces nitrogen absorption [170,171]. This could be attributed to the decreased activity of enzymes and transporters in the roots under such conditions.
Plants have developed advanced mechanisms to prevent damage caused by cold temperatures. One such mechanism is cold acclimation, where plants exposed to mild cold temperatures for a short period become more resistant to following freezing stress [172,173]. During cold acclimation, various physiological, biochemical, and molecular transformations take place. These include the activation of antioxidant systems, the production and buildup of cryoprotectants, and the implementation of mechanisms that safeguard and stabilize cell membranes [174]. To keep the cell membrane stable, the content of unsaturated phospholipids in the membrane increases. Additionally, cells store osmotic molecules rich in sucrose and proline, as well as antifreeze proteins, which help to retain water molecules [175]. Plants synthesize various proteins such as late embryogenesis abundant (LEA), anti-freezing proteins (AFP), and cold shock proteins (CSP) to increase their tolerance to cold stress [176,177]. Lower molecular-weight solutes, soluble sugars, and proline act as osmoprotectants to shield plants from cold-induced damage. Similarly, the accumulation of protective proteins like LEA, AFPs, and CSPs during cold acclimation is crucial for enhancing cold tolerance in plants [178]. The acclimation mechanism is crucial for improving the ability of plants to withstand cold temperatures. Even plants that are sensitive to cold, like rice, can adapt to chilling conditions [179,180]. Freezing-resistant plants also adapt through cold acclimation, where they are exposed to temperatures slightly above freezing. Under these conditions, aquaporins play a key role in regulating the water uptake mechanism and the permeability of cell membranes [181,182,183,184]. Various studies have shown that aquaporins are functionally important in controlling the hydraulic conductivity of roots (Lpr) [180,185,186]. It has also been demonstrated that the decrease in water uptake in rice under cold stress is associated with a decrease in aquaporin expression [187].
Furthermore, the presence of low temperatures can result in the buildup of ROS and H2O2. This accumulation can subsequently lead to leakage of electrolytes, lipid peroxidation, and damage to the cell membrane [188]. This can be observed through the rise in levels of MDA. The breakdown of polyunsaturated lipids to MDA is one possible way ROS can damage cells and tissues [188,189]. Plants contain a variety of antioxidant systems to prevent catastrophic breakdown of protein and lipid components when under stress. Antioxidants like CAT, POD, 2,2-diphenyl-1-picrylhydrazyl, and SOD can compete against ROS generation in rice under cold stress due to their high stability and pace of rising [164]. A study on rice cultivars under cold stress found that cultivars with a faster growth rate had greater H2O2 levels in the shoots but lower levels in the roots. However, this was reversed in the case of rice cultivars with a low growth rate. Moreover, the roots had higher MDA concentrations and electrolyte leakage due to cell damage than the shoots under cold stress. Cold stress boosts SOD and CAT activities in the rice roots [162]. These biochemical characteristics can be used as a selection marker for breeding and adjusting rice crops with enhanced cold tolerance.
Glutamic acid (Glu) is essential in the amino acid metabolism of plants and is involved in vital metabolic processes during abiotic stress [190]. These functions include the production of proline and gamma-aminobutyric acid (GABA), which are essential for plants’ defense systems [191]. Under cold stress, GABA, proline, and soluble carbohydrates like glucose and sucrose buildup in rice and work as osmoprotectants to prevent damage from dehydration and freezing [192,193]. The findings suggest that GABA and proline could improve plants’ ability to withstand cold temperatures.

2.3.2. Molecular Response to Cold or Low-Temperature Stress

Rice plants must maintain the stability of their cell membranes, their levels of chlorophyll and fluorescence, the initiation of ROS defense mechanisms, and the accumulation of osmolytes to withstand cold stress [194]. During cold stress, COLD1 and CIPK sense cold-related stress signals, and several genes relating to osmoprotectants and phytohormones are modulated. To facilitate cold sensing and extracellular Ca2+ influx at low temperatures, COLD1 has been demonstrated to interact with the rice G protein α subunit 1 (RGA1) [195]. Rice CBL-interacting protein kinase 7 (OsCIPK7), in addition to COLD1, is believed to recognize cold stress cues by controlling the configuration of its kinase domain and the influx of Ca2+ [196].
At low temperatures, endogenous ABA levels rise, and expression of ABA-responsive genes is activated, strengthening plant tolerance to cold stress. Overexpression of the OsPYL9 (an ABA receptor), which positively modulates ABA signaling, can dramatically increase rice’s ability to withstand low temperatures [197]. In addition to the fundamental component PYL-PP2C-SnRK2-ABF, the ABA signaling pathway also involves nitric oxide (NO), ROS, Ca2+, phospholipid molecules, and other kinases, like MAPK [198]. The mitogen-activated protein kinase OsMAPK3 elevates trehalose content and strengthens rice adaptation against cold stress [199]. Table 3 presents a summary of key genes associated with cold stress tolerance. Although there has been a significant advancement in cold stress tolerance, little is known about single-cell responses in rice plants.
Abiotic stressors can be effectively reduced using nanoparticles. Zinc oxide nanoparticles (ZnO NPs) applied topically considerably reduce the chilling stress experienced by rice seedlings, resulting in increased plant height and root length and enhanced dry biomass. With the decreased concentration of H2O2 and MDA, in addition to higher activities of the key antioxidative enzymes like SOD, CAT, and POD, ZnO NPs further restore chlorophyll accumulation and markedly mitigate chilling-induced oxidative stress [221]. Plant melatonin, an organic molecule, has also been demonstrated to be crucial for plant stress adaptation. Melatonin pretreatments boost the non-enzymatic antioxidant content and upregulate the antioxidant enzyme activity in rice. The application of exogenous melatonin reduces rice seedling development inhibition, formation of ROS, MDA, inhibitions of photosynthesis and PSII activities, and cell death brought on by cold stress in rice [222]. Similarly, Teixeira et al. found that rice seed priming with carrot extract greatly speeds up germination and raises the final germination percentage while reducing the damage caused by cold [223].

2.4. Submergence Stress

Submergence is a major concern for rice cultivation in lowlands subjected to rainfall and flood-prone regions globally. It is expected to become more common as climate change increases flood threats, particularly in regions impacted by monsoon rains in Asia [224]. Rice plants possess a partially aquatic characteristic, enabling them to thrive in waterlogged or submerged environments for extended periods [225]. Nevertheless, prolonged submersion exposes rice plants to various stresses, such as reduced access to light, decreased gaseous exchange, physical damage, and increased vulnerability to pests. In addition, submergence typically lowers the photosynthesis process, depleting carbohydrate stores and eventually causing the death of the plant [226]. Rice usually comes to be affected by two different types of flooding. The initial type is flash flooding, which arises when the crop is flooded for 1–2 weeks due to a sudden rise in water levels. Another kind of flooding is stagnant flooding, in which the water level rises above 100 cm and stays there for several weeks [227].

2.4.1. Morphophysiological and Biochemical Responses to Submergence Stress

Rice is extremely sensitive to submersion during the germination and early seedling growth stages. When rice seeds are entirely submerged in water, they suffer from hypoxia or anoxia, resulting in poor germination and seedling mortality [228]. The rice plant undergoes numerous morphological and physiological changes as a result of submergence. Rice withstands submersion by growing longer leaf sheaths and blades during the seedling stage and internodes during the vegetative growth stage [229]. Even submergence-tolerant types attempt to expose their leaf tips above the water’s surface if the flooding lasts longer than two to three weeks to ensure their survival [230,231]. When fully submerged, the leaves and stems of the rice plant grow moderately longer to reach the water’s surface. However, there are negative effects from this elongation process that are necessary for post-submergence plant growth [232]. Turbid water reduces the amount of light that may pass through floodwater, which lowers photosynthesis and, as a result, the submerged plant uses its reserve carbohydrate to sustain its metabolism [233]. However, if the depth of flooding is significant and the duration of flooding is prolonged, the plant’s limited ability to perform photosynthesis causes its energy reserves to deplete rapidly, ultimately leading to the plant’s death [234]. The amount of carbohydrates found in plant sections determines a variety’s capacity to withstand submersion [235]. Submergence-tolerant rice cultivators benefit from limited shoot elongation because they preserve carbohydrate reserves, which aid in resuming development after de-submergence. For recovery from submergence shock, carbohydrate availability following flooding is crucial [236]. During periods of flooding, plants are entirely or partially immersed in water. However, when the floodwater recedes, the plants are suddenly exposed to oxygen again. This reoxygenation process can harm plants after being submerged. MDA, O2−, and H2O2 were found to increase in rice plants’ leaves after being submerged for seven days as a sign of oxidative damage [237]. Rice leaves began to dry out when exposed to air oxygen again after being submerged for 7 to 10 days [238]. Due to conserving glucose metabolism during submersion, tolerant rice cultivars on de-submergence exhibit an ascent in fresh biomass. On the other hand, the non-tolerant cultivars’ reserves undergo hydrolysis and are incapable of regeneration. These findings suggest that resistance to several stresses, including submersion, re-oxygenation, and dehydration, is necessary for a plant to survive a flood [239]. Due to frequent oxygen deprivation and low light intensity, submerged plants develop ROS, which, if unchecked, can adversely harm the cellular structure and end in plant death. [240]. The antioxidant defense mechanism is crucial to detoxify ROS and lessen their harmful effects. SOD, APX, and GPX are the substances that are crucial in ROS detoxification [241].
To thrive in submerged environments, rice cultivars employ two growth control techniques: quiescence and escape strategies, both of which rely on ethylene-responsive transcription factors (ERFs). In the quiescence strategy, shoot prolongation is postponed for quite some time (10–14 days) during flash flooding to save carbohydrates [242]. Utilizing conserved carbohydrates, cultivars that can withstand submersion can resume their growth after de-submergence. The escape strategy is adopted by deepwater rice genotypes and involves rapid internode extension to climb above the water level [243]. To implement these strategies, rice has evolved specific anatomical and morphological characteristics. These include the development of adventitious roots, aerenchyma formation, radial oxygen loss (ROL) barrier, and the ability to create a thin film of gas on its leaves. Furthermore, rice plants generate ventilated tissues and ethylene to aid in gas exchange and regulate the programmed death of specific cells in the cortex and epidermis [244,245]. In addition, the growth of adventitious roots regulates the death of epidermal cells utilizing the mechanical energy they produce [246]. When submerged, rice plants rapidly accumulate gibberellic acid (GA), which leads to the elongation of internodes [247]. To protect their roots from oxygen loss, rice plants form an ROL barrier. This barrier extends from the base to the tip of the roots and is located outside the aerenchyma [248]. Various Asian rice cultivars have developed additional characteristics to adapt to prolonged submergence. These traits include aerobic germination and dormancy of leaf elongation during flash floods, and internode elongation during periodic flooding. Certain rice cultivars can withstand being submerged for around 15 days by limiting elongation growth, carbohydrate consumption, and chlorophyll degradation [249,250].
One of the significant regulators of rice’s submergence reactions is ethylene. Owing to physical confinement and active production during stress, this gaseous phytohormone quickly builds up in tissues of submerged plants, inducing various acclimation reactions, such as shoot elongation, development of adventitious root, and glucose metabolism. Deepwater rice encourages internode growth during submersion to project the photosynthetic parts of the plant above the air–water contact [242]. High production rates of ethylene and sensitivity to the hormone mediate this flight response. Lowland rice that can withstand submersion, in contrast, limits the number of carbohydrates it consumes, which encourages underwater elongation and is used for cell division and elongation. Limited ethylene production and sensitivity are the causes of this tolerance [251]. Aerenchyma, which allows for relatively unimpeded movement of O2 from well-aerated shoots to buried roots, is another way lowland rice adapts to soil waterlogging [252]. Inducing a barrier to radial O2 loss (ROL) that reduces O2 loss to the surroundings can further boost longitudinal O2 diffusion along the root apex. Under flooded conditions, these characteristics are used by both lowland and upland different rice species [253].
Unlike flood-sensitive rice types, flood-tolerant rice cultivars utilize energy stores more effectively and maintain higher non-structural carbohydrate (NSC) concentrations in stems and leaves. Additionally, they use anaerobic respiration as a different energy-producing method. Submergence-tolerant rice cultivars decrease shoot prolongation to preserve energy for survival and recuperation following de-submergence. Complete submersion-tolerant rice genotypes maintain their chlorophyll and embrace a strategy of modest growth, shown by reduced elongation when submerged. Because of this, plants can save enough glucose reserves to maintain metabolism while submerged and after the floodwaters have receded [250].

2.4.2. Molecular Response to Submergence Stress

Rice plants implement passive approaches for adapting and avoiding recurring floods. SUB1A is a crucial modulator of submergence tolerance, which activates transcriptional modulation of other ERF response factors and SLR1 [250]. In deepwater rice, the ERF OsEIL1 is stabilized by ethylene accumulation. OsEIL1 binds to the SD1 promoter to boost gene expression. SD1 participates in GA synthesis and affects internode elongation [254]. The GA then increases the expression of the Accelerator of Internode Elongation 1 (ACE1), while DEC1, a protein that prevents internode elongation, sees a decrease in expression [255]. In addition, OsEIL1 also activates the expression of other downstream genes as a result of submergence stress by binding to the promoter sites of SNORKEL1 (SK1) and SNORKEL2 (SK2) [247,256]. Table 4 presents a summary of key genes associated with submergence stress tolerance in rice.
A study found that SK1 and SK2 respond during flood stress by encoding response factors associated with ethylene signaling [264]. During submergence, ethylene levels in rice rise, and the expression of SK1 and SK2 elevate, ultimately promoting internode elongation via GA [265,266,267,268]. Functional assessment of ERF-type TFs indicated that they play a role in regulating several physiological and morphological responses to submersion. SUBMERGENCE-1 (Sub1) and SK are TF genes that belong to the ERF class [247,249]. Three clusters of related genes, SUB1A, SUB1B, and SUB1C, expressing ERF-like TFs, are found in the Sub1 region of submergence-tolerant cultivars, with SUB1A being the most investigated. Systematic genetic analyses showed that SUB1A introgression with SUB1B and SUB1C imparts a strong endurance against submergence and does not alter rice grain quality or production [234,249,250,269]. Additionally, SUB1A prevents the development of proteins that loosen and expand cell walls in response to flooding stress, preserving high levels of chlorophyll a and b [270]. Furthermore, SUB1A also promotes resistance to oxidative stress by controlling genes that encode ROS-detoxifying enzymes [237].
In soil, silicon (Si) is the second most prevalent element. According to Debona et al., silicon significantly increases plant resilience to various biotic and abiotic stressors [271]. Si treatment improves rice root morphological features and chloroplast ultrastructure to counteract the inhibitory effect of submergence stress by boosting Si absorption, accumulation, and plant biomass. Si also lessens oxidase damage by increasing POD and CAT activity and decreasing MDA concentration, which helps rice recover from submersion stress-related damage [272,273].

2.5. Salinity Stress

Salinization is becoming an ever-worsening problem resulting from poor agricultural practices and environmental changes. Salinity is characterized by excessive levels of various salts in the soil, including sodium chloride, magnesium sulfates, magnesium bicarbonates, calcium sulfates, and calcium bicarbonates. When it is young, the rice crop is considered a salt-sensitive cereal, and as it matures, salinity limits the yield’s efficiency [274,275]. Salt stress is particularly detrimental to rice during its early vegetative and reproductive phases. Water, along with toxic ions from the soil, enter the vascular section of the root system via two pathways: apoplastic and symplastic. Through the apoplastic pathway, salt stress causes shoots to accumulate more Na+, primarily in mature leaves. A Na+/K+ symporter called the high-affinity potassium transporter (HKT) controls the movement of Na+ and K+ within plant cell membranes [276,277]. The potassium uptake is hampered by sodium ions overloading the root’s surface. Na+ interferes negatively with K+ uptake because it shares the same molecular characteristics as K+. When plants come under salt stress, a considerable quantity of Na+ enters the plant, elevating the intracellular Na+ levels. This has detrimental impacts since Na+ competes with K+ to activate enzymes and synthesize proteins [278].

2.5.1. Morphophysiological and Biochemical Responses to Salinity Stress

Rice plants exhibit various morphological, physiological, or biochemical changes and symptoms when exposed to high salinity. In extreme cases, they may even perish. Direct accumulated salts interfere with metabolic functions and all key morpho-physiological and yield-related traits, comprising photosynthesis, plant height, root length, tiller number, length of panicle, spikelet count per panicle, filling of grains, and plant biomass. As a result, yield is significantly reduced [279,280,281]. In a salt-sensitive plant, exposure to salinity stress results in pericycle shrinkage and physical damage. Salt stress exposure at the early seedling stage raises the mortality rate of rice leaves [282]. The productiveness of the rice crop under salt stress is greatly impacted by panicle sterility [283].
Salinity generally induces two types of stress in plants: osmotic and ionic stress. Osmotic stress arises when the salt concentration around the plant’s roots exceeds the threshold tolerance level. On the other hand, ionic stress develops when there is a large Na+ inflow into the plant, which raises the salt concentration in older leaves to a toxic level. This leads to higher Na+ concentrations in the vacuole and cytoplasm, disrupting metabolic processes and causing cell death [284]. In the beginning, osmotic stress caused by soil salinity restricts plant growth, and later, ionic stress follows. A significant amount of salt in the soil contributes to the first phase, characterized by reduced plant water intake and the subsequent induction of several cellular metabolic processes [285]. Enlargement of cells, cell wall protein synthesis, net photosynthesis, photosynthetically active radiation, stomatal conductance, relative water content, transpiration rate, and pigment degradation are all inhibited during the initial phase whereas the accumulation of compatible solutes and ABA increased [286]. According to research by Cha-umi et al., salt stress caused a significant drop in carotenoid and chlorophyll in rice leaves [287]. During the latter phase, the accumulation of ions (Na+ and Cl) is linked to changes in the ions ratio of Na+/K+ and Na+/Ca2+. The subsequent increase in ions promotes the synthesis of ROS. The extra ROS generation increases cellular oxidative stress, which upsets the equilibrium between generating and eliminating ROS [288].
Like the majority of plants, rice has developed several defense strategies against salinity stress, such as (i) antioxidant generation for ROS detoxification (ii) ion homeostasis and compartmentation, (iii) osmoprotection through osmolyte regulation, and (iv) programmed cell death [289]. Plants have devised an exquisite antioxidant defense mechanism to scavenge and detoxify ROS to shield the cells from oxidative damage. According to studies, the salt-tolerant rice cultivar Pokkali performed better under salinity stress than the Pusa Basmati (salt-sensitive rice cultivar) in terms of ROS scavenging enzymes like CAT and content of antioxidants like AsA and GSH [290]. In rice plants, the basal area of the leaf can scavenge H2O2 by boosting the activity of CAT and maintaining higher constitutive levels of APX and GPX than those in the apical region under salinity. Under salt, the GR in the basal area might inhibit O2 generation. The apical area can, however, scavenge O2 by boosting SOD activity, whereas, under salinity, the activity of H2O2 scavenging enzymes, including APX and CAT reduced [291]. To prevent the rice from oxidative stress brought on by salt, both enzymatic and non-enzymatic ROS scavenging machinery must work together. A transcriptional cascade in rice roots, which is regulated by the transcription factor SERF1, is responsible for salt tolerance and is dependent on ROS [292].
To maintain ion homeostasis during salinity stress, plants employ different mechanisms. One of the mechanisms for tolerating salinity stress involves the transport of Na+ and Cl in the roots to prevent their excessive accumulation in the leaves. This process includes removing Na+ from the xylem and releasing ions back into the soil. If Na+ exclusion fails, it can have toxic effects on older leaves, leading to their premature death [293]. The concentration of Na+ in the rice leaves is linked with the salinity stress tolerance level in both japonica and indica rice varieties [294]. Maintaining a low cytosolic Na+/K+ ratio is important for maintaining ionic homeostasis and improving photosynthesis and overall plant growth [295,296]. During salinity stress, the accumulation of Na+ in the leaves and shoots of salt-tolerant varieties of rice is lower compared to salt-sensitive varieties [297,298]. It was also reported that the salt-tolerant cultivar Pokkali can reduce Na+ uptake into the cytosol and maintain lower cytosolic Na+ content by temporarily taking up Na+ into the cytoplasm and quickly extruding it into vacuoles. However, the salt-sensitive rice variety BRRI Dhan29 was unable to perform this function [299].
Due to osmotic stress, most organisms, including bacteria and plants, accumulate specific organic solutes, especially proline and sugars which are referred to as osmoprotectants [300,301]. Trehalose, a non-reducing sugar, stands out for having a unique property that protects biological molecules from dehydration stress. According to Garg et al., the production and accumulation of trehalose in transgenic rice can give the grain some resistance to the negative impacts of salinity and drought [302]. Glycine betaine, a potent solute containing quaternary ammonium, is found in several organisms. Though rice plants generally do not store glycine betaine, it has been shown that they may absorb exogenously and store it in their leaves to aid in sustaining PSII quantum yield when subjected to salt stress [289,303]. If the plant’s several defense strategies against salinity stress fail, it will implement programmed cell death (PCD) as a last-ditch effort to survive [304]. According to Liu et al.’s [305] findings, rice roots under salt stress had a well-regulated progression of cell death. This raised the possibility that the dead cells prevented salt exclusion by blocking the inflow of extra Na+ ions into the interior of roots and shoots. Another possibility is that the plant sheds cells to avoid unregulated cell death and the release of toxins to safeguard and maintain the growth of other cells [306].

2.5.2. Molecular Response to Salinity Stress

Various proteins are involved in activating the tolerance mechanism against salt stress. They play different roles in the accumulation of MDA, antioxidants and osmoprotectants, ROS and Na+ homeostasis, and electrolyte leakage [289]. Certain WRKY TFs restrict the expression of DREB1B and OsNAC1, contributing to salt susceptibility [307].
TFs influence salt tolerance positively or negatively. OsCOIN, OsbZIP71, OsbZIP23, OsDREB2A, and OsMYB2 are some of the salt-responsive TFs that may cause a variety of alterations in rice, such as a buildup of osmoprotectants and antioxidants and an upsurge in the activity of the Na+ and K+ transporters [308]. In rice, overexpression of these salt-responsive TFs promotes a higher survival rate of seedlings, reduces oxidative damage, and improves osmotic regulation [309,310]. On the contrary, OsWRKY13, one of the negative regulatory TFs, prevents the expression of the salt-responsive genes SNAC1 and ERD1, thereby delaying the rice plants’ growth and development [311]. The expression of genes including SNAC1, NCED4, Rab16D, and DREB1B was suppressed by the transcriptional repressor OsWRKY45-2, and as a consequence, overexpression of OsWRKY45-2 drastically lowered the survivability of rice cultivars under salt stress [312]. Liu et al. revealed two newly discovered genes (LOC Os02g49700, LOC Os03g28300) and five known genes (OsMYB6, OsGAMYB, OsHKT1;4, OsCTR3, and OsSUT1) connected with grain production and its associated attributes in rice cultivars exposed to saline stress conditions [313].
According to Rahman et al., maintaining lower shoot Na+ buildup is a standard method for preserving salt tolerance in rice [78]. These methods include sodium exclusion, effective toxic salt sequestration into older leaves and roots, compartmentalization of Na+ into vacuoles, and extrusion from cells. According to Wang et al., OsHKT1;1, OsHAK10, and OsHAK16 were shown to be elevated in the leaves of old rice under salt stress [314]. These genes are integral to Na+ transport from the roots to the shoot. OsHKT1;5 and OsSOS1, which promote Na+ exclusion from xylem vessels of roots, thereby lowering accumulation in the shoot, were downregulated, resulting in large quantities of Na+ in older leaves rather than young ones. Rice’s class 1 HKT transporter eliminates extra Na+ from the xylem, shielding the photosynthesis-dependent leaf tissues from the harmful effects of Na+. By mediating K+ absorption and transfer to sustain a high K+/Na+ ratio under salt stress, the K+ transporter genes OsHAK1 and OsHAK5 are stimulated by salt stress in rice [315]. When there is a higher concentration of Na+ in the cytosol, it is transported into the vacuole to prevent it from reaching toxic levels for enzyme reactions. Na+/H+ antiporters control this process. An increase in salt content activates the Na+/H+ antiporter action [316]. Two proton pumps, vacuolar H+-ATPase, and vacuolar H+-translocating pyrophosphatase, control the interchange of Na+/H+ in the vacuole. Modifying the vacuolar transporter levels can enhance rice’s tolerance to salinity [317]. According to a study, elevated CYP94C2b expression and concurrent jasmonate inactivation in rice are associated with salt tolerance [318]. Table 5 summarizes the key genes associated with salt stress tolerance in rice.
Arbuscular mycorrhizal fungus (AMF) symbionts aid the host plant development and ameliorate stress caused by abiotic factors. Under salt stress, the upland pigmented rice cv. Leum Pua (LP) infected with Glomus etunicatum produced total soluble sugars and free proline, which worked as osmolytes to preserve the flag leaf’s photosynthetic capacities, chlorophyll pigments, Chla fluorescence, and stomatal function. Leum Pua rice infected with Glomus etunicatum maintained yield characteristics and showed high anthocyanin content in the pericarp [333].

2.6. Heavy Metal Stress

Heavy metal pollution is a major contributor to harmful effects on plants, ecosystems, soil, and water. It is a significant factor in reducing the quality and yield of crops. Rice grown in paddy soils contaminated with heavy metals like arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg) is a major source of heavy metal intake for humans in many countries. This gradual buildup of heavy metals in rice grains and their subsequent entry into the food chain poses a severe risk to agriculture and public health [334]. Heavy metals have the potency to modify reactions that aid in generating ROS, ˙OH, and H2O2 within living cells. Nevertheless, when highly reactive radicals come into contact with water, they produce ˙OH, which can harm essential biomolecules within cells such as carbohydrates, lipids, amino acids, and DNA [335,336,337]. Therefore, it is necessary to comprehend how heavy metals interact with rice crops at all levels, from the cellular to the entire plant, and to develop effective strategies to reduce these stress reactions [338,339].

2.6.1. Morphological and Physiological Responses to Heavy Metals

Arsenic can exist in various oxidation states in soil, the most prevalent of which are arsenides (As3−), arsenites (As3+), and arsenates (As5+). Depending on the species, arsenic can harm rice, with inorganic species being far more toxic than organic ones. As5+ and As3+ are the most prevalent inorganic species found in the rice plant, whereas monomethylarsonic acid (MMA) and dimethylarsinic acid (DMA) are the most occurring organic species [340]. As3+ is thought to be more mobile and hazardous than As5+ among inorganic entities. It can react with methyl groups in any oxidation state to create organic arsenic species. However, compared to inorganic arsenic species, the presence of organic species in paddy soil is substantially lower. The reduced form (As3+) predominates in anaerobic soil types, such as submerged rice fields, whereas As5+ (oxidized counterpart) predominates in aerobic soil environments, such as highland rice fields [341]. An increase in arsenic absorption will have a detrimental impact on plant development. Poor and lower germination rates of seeds, impaired plant growth, lower photosynthetic rates, sterility-related yield loss, low biomass production, and a physiological condition known as straight head disease are just a few of the symptoms that are brought on by arsenic toxicity in rice plants [342]. Reduced floret/spikelet sterility, decreased grain production, and, in severe cases, the absence of panicles or heads are some signs of this disease. Arsenic toxicity damages the chloroplast and photosynthetic processes by deteriorating the membrane structure. Arsenic affects the metabolism of proteins, lipids, and carbohydrates. More crucially, arsenic can increase the production of ROS that is greater than what can be scavenged, damaging plants through oxidative stress. Exposure of rice seedlings to As5+ promotes the formation of H2O2, whereas As3+ was shown to induce the formation of O2 and H2O2, thereby causing lipid peroxidation [343]. When seedling roots are grown in an As5+ solution, APX activity is increased, reducing H2O2 through the ascorbate-glutathione cycle [344]. Similarly, the enzymatic antioxidants CAT, SOD, guaiacol peroxidase, chloroplastic ascorbate peroxidase, GR, and monodehydroascorbate reductase concentrations were raised for scavenging ROS developed in the presence of As3+ conditions [345].
Cd is a trace element that is not necessary for plants but is widespread in the environment. Different anthropogenic operations such as smelting, mining, usage of synthetic phosphate fertilizers, and disposal of urban wastes lead to a rise in the levels of Cd in the environment that pose serious health risks to humans [346]. Recently, it has been found that Cd pollution in paddy soil poses a danger to rice quality [347]. Rice plants absorb Cd from the soil, eventually building up in the grains after several transit steps. Rice plant absorbs Cd from the ground through its roots, moves it to the shoots via xylem flow, reroutes it at nodes, and remobilizes it from the leaves. According to Huijie et al. [348], citrate, tartaric acid, and histidine were found to participate in root-to-shoot Cd transfer in the xylem actively. Indica cultivars often accumulate more significant amounts of Cd in their shoots and grains than japonica cultivars. Stomatal conductance, transpiration rate, leaf water content, vital minerals, water-soluble proteins, and enzyme- and non-enzyme-based antioxidants are all decreased due to Cd toxicity [349,350]. Cd poisoning reduced rice yield and grain quality by inducing changes in yield components (such as panicle number, spikelets per panicle, and spikelet setting percent). Excessive Cd has a deleterious impact on photosynthesis as it affects the photosynthetic pigments and disrupts electron transport mechanisms, interfering with chloroplast structure and Chl-protein complexes. This disruption causes a disturbance in Chl biosynthesis enzymes, the Calvin cycle, and water balance [351]. Cd prevents the formation of chlorophyll by inhibiting the enzyme δ-aminolevulinic acid dehydratase, which is present in rice seedlings. An increase in Cd concentration in the medium led to a higher accumulation of Cd in the seeds and the thiobarbituric acid reactive substance amount. It also caused a drastic decrease in the germination rate, shoot elongation, biomass, and water content of the rice [352].
Despite not being a direct cause, Cd can cause exorbitant accumulations of ROS when its concentration surpasses the plant tolerance level. This can occur through several mechanisms, comprising the exhaustion of ROS-scavenging enzymatic and non-enzymatic components, metabolic abnormalities during respiration, displacement of redox-active Fe from proteins, photorespiration, and CO2 assimilation [351,353].
Pb is a non-essential element that may disrupt plant metabolism if taken up by the plant. In addition to interfering with roots’ ability to absorb minerals from the soil solution, Pb2+ ions also passively penetrate the roots of rice plants by following water streams that are moving through the soil. Pb is carried into the root epidermal cells from the soil and loaded into the root xylem vessels before being distributed to other plant organs [354]. In rice cultivars, a high Pb concentration (1.2 mM) results in a considerable decrease in plant height, tiller count, panicle count, and spikelet count per panicle [355]. Lead poisoning negatively affects photosynthetic activity by altering chloroplast structure, slowing the production of carotenoid, plastoquinone, and chlorophyll, and breaking up the electron transport chain. Additionally, it causes a CO2 shortage, which causes the stomata to close and Calvin cycle’s enzymatic activity to decrease. According to a study by Khan et al. [356], Pb poisoning does not affect root development but drastically reduces shoot length and biomass of rice in nitrogen or phosphorus-deprived seedlings. ROS are overproduced, and antioxidant enzyme activity fluctuates due to Pb toxicity in plants.
One of the environment’s most hazardous elements is Hg. Hg is a strong phytotoxin to plant cells at high concentrations and can cause injury and physiological disturbances. Hg preferentially accumulates on the roots of several plant species. As a result, the most toxic effects are observed at the roots. Under Hg stress, rice roots bind to proteins of 15–25 kDa, which results in irreparable harm to root development. Under Hg stress, rice roots altered the expression levels of the associated proteins [357]. When rice is grown on Hg-contaminated land, a significant amount of Hg is enriched into the grain, which is terrible for the rice’s consumers [358]. There are three different types of mercury: methylmercury (MeHg), inorganic mercury (Hg2+), and elemental mercury (Hg0) [359]. Hg is most bio-accumulative in the form of methylmercury MeHg. MeHg is the most harmful type of Hg to human and animal health [358]. The generation of MeHg in the rhizosphere soil and its buildup in rice are greatly influenced by moderate soil Hg content (3 mg kg−1). MeHg production in rhizosphere soil increases significantly at the blooming or filling stage, but rice leaves’ antioxidant systems show little impact [273]. The bulk of an individual rice grain’s Hg2+ by mass is found in the hull and bran. Conversely, white rice contains a large proportion of the more dangerous form of MeHg. Proteins contain MeHg, which is primarily coupled to cysteine in bran. This MeHg-cysteine relationship acts as a mobile nutrient during seed ripening and is actively transferred to the endosperm [360]. ROS, MDA content, and lipoxygenase activity are all considerably enhanced with increasing Hg levels in rice roots, which disturbs numerous cellular processes and hinders growth and development in rice plants [359].

2.6.2. Biochemical Responses to Heavy Metals

An increased quantity of heavy metals like As, Hg, Pb, and Cd triggers ROS generation, leading to oxidative stress. This stress damages the plasma membrane and disrupts rice plants’ metabolism and physiological response. To combat oxidative stress, rice plants develop various defense strategies, such as activating the antioxidant defense system, ion homeostasis, osmolyte accumulation, osmoregulation, and excess production of signaling molecules [361,362]. In addition, in response to stress caused by heavy metals and metalloids, rice plants produce phytochelatins (PC), which are thiol-rich peptides [363]. For instance, rice leaves containing As-PC complexes reduce the amount of As3+ that may be transferred to the grain [364]. Similarly, under Cd stress, rice roots and leaves showed increased SOD, POD, CAT, GPX, and APX activity. Under Cd toxicity, rice also has higher levels of non-protein thiols like PCs and GSH to scavenge harmful free radicals [353]. In another experiment, rice showed an increase in the activity of CAT and POD under Pb poisoning. There was also an increase in the accumulation of proline and the content of sucrose with the rise in Pb concentration [355]
Recently, glutamate (Glu) has been found to participate in a signaling role in responses developed by plants toward abiotic stress [365]. In a study, glutamate supplementation was found to dramatically improve Cd-induced oxidative stress in rice with decreased levels of MDA, H2O2, O2, proline, γ-aminobutyric acid, arginine, and higher activities of CAT, POD, and glutathione S-transferase. Roots of Cd-treated plants showed decreased expression of Cd-induced metal transporter genes OsNramp1, OsNramp5, OsIRT1, OsIRT2, OsHMA2, and OsHMA3 when supplemented with Glu [366]. According to Ahsan et al., 21 proteins were demonstrated to be engaged in defense and detoxification, antioxidant, protein biosynthesis, and germination activities in rice under Cd toxicity [367]. Hg stress raises the free Phe and Trp content and upregulated numerous genes related to aromatic amino acids. Chen et al. found that applying Phe and Trp to rice roots exogenously increases their tolerance to Hg and significantly decreases the concentration of ROS that Hg induces [368]. Additionally, research has shown that the formation of iron plaque on the roots of rice may serve as a protective barrier, reducing the absorption of Cd and As into the roots of the rice plant [369,370].

2.6.3. Molecular Responses to Heavy Metals

Heavy metal stress-related signal transduction is triggered by the recognition of stress signals by receptors/ion channels and then carried on by non-protein messengers such as calcium, hydrogen ions, and cyclic nucleotides (Figure 3).
The stress signals are relayed by several kinases and phosphatases, which in turn cause the expression of multiple TFs and the generation of metal-detoxifying peptides [371,372,373]. Heavy metals initiate various distinctive signaling pathways in plants, which include ROS signaling, calcium-dependent signaling, MAPK signaling, and hormone signaling that promote the expression of TFs and stress-responsive genes [344,372]. Calmodulins (CaM), calmodulin-like proteins, calcineurin B-like proteins, and CDPK are some of the calcium signaling sensors that monitor, process, and transmit changes in cytosolic Ca2+ content for the stress response. Individual sensors respond differently depending on the Ca2+ content [374,375]. Likewise, the MAPK signaling cascade also phosphorylates several TFs, including NAC, MYC, MYB, bZIP, DREB, and ABRE, which alters the expression of metal stress response genes [376,377]. For instance, Cd activates rice’s myelin basic protein (MBP) kinase and OsMAPK2 genes [378]. Additionally, numerous research studies have displayed that the activation of MAPKs by heavy metals in rice is caused by ROS production, accumulation, and modification [372,379]. Furthermore, several phytohormone signaling pathways, especially ethylene, auxin, and JA, are affected by ROS. According to Singh and Shah, JA treatment enhanced rice’s ability to withstand Cd stress via improving antioxidant response [380]. When As3+ was applied to rice seedlings, comparative transcriptome analysis revealed modification in signal transduction, defensive responses, and hormonal signaling pathways, including ABA metabolism [381]. The results above strongly imply that changes in phytohormone levels alter how plants react to metal stress. Hence, it is crucial to comprehend the complex pathways through which metal stress is signaled in plants and the interconnections between them. This understanding is essential to unravelling the networks that plants employ to respond to stress. Numerous molecular research studies have examined how rice plants react to elevated levels of heavy metals. These research studies aim to enhance the ability of current rice cultivars to withstand heavy metal toxicity and offer valuable insights for incorporating these specific genes/traits into future breeding initiatives. Table 6 summarizes key genes associated with heavy metal tolerance in rice.

3. Conclusions

Abiotic stress is a significant factor restricting rice crop yield in many places of the world. Under the current climate change scenario, abiotic factors such as drought, heat, cold, submersion, salinity, and heavy metals are responsible for the sharp decline in rice yields. These abiotic stressors have a detrimental impact on various stages of plant growth and development, including germination, seedling establishment, lengths of root and shoot, plant height, blooming time, and ripening time. These stressors during both the vegetative and reproductive stages hinder the development of the plant’s panicles and the filling of grains, decreasing overall grain production and posing a risk to global food security. The combined application of genomics and QTL-based techniques has aided in identifying genes and loci that contribute to adaptation to abiotic stress in rice. These recently discovered molecular candidates have the potential to enhance rice physiological growth, reproductive development, and crop yields in challenging environments. However, in the future, research employing high-throughput phenotype determination and next-generation sequencing technology will help identify innovative potential genes responsible for regulating grain development under varied stress situations, paving the way for the breeding of climate-ready crops. In this review, we have discussed the developments in the current understanding of the defense mechanisms that rice employs to counteract various environmental stresses. Despite our vast knowledge in this area, there are still gaps in our understanding. Bridging these gaps will allow researchers to design plants that respond better to environmental stimuli such as drought, heat, cold, submersion, salinity, heavy metals, etc.

Author Contributions

Conceptualization, B.S., H.K., T.L.T. and Y.K.M.; validation, P.N.B.; resources, B.S., H.K., T.L.T. and Y.K.M.; data curation, B.S., H.K. and T.L.T.; writing—original draft preparation, B.S., H.K., T.L.T. and Y.K.M.; writing—review and editing, P.N.B., Y.K.M. and K.-H.B.; supervision, Y.K.M. and K.-H.B.; All authors have read and agreed to the published version of the manuscript.


This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (NRF-2021R1F1A1060297).

Conflicts of Interest

The authors declare no conflict of interest.


  1. Yadav, G.S.; Lal, R.; Meena, R.S.; Babu, S.; Das, A.; Bhowmik, S.N.; Datta, M.; Layak, J.; Saha, P. Conservation tillage and nutrient management effects on productivity and soil carbon sequestration under double cropping of rice in north eastern region of India. Ecol. Indic. 2019, 105, 303–315. [Google Scholar] [CrossRef]
  2. Mahanta, K.; Bhattacharyya, P.N.; Sharma, A.K.; Rajkhowa, D.; Lesueur, D.; Verma, H.; Parit, R.; Deka, J.; Medhi, B.K.; Kohli, A. Residue and soil dissipation kinetics of chloroacetanilide herbicides on rice (Oryzae sativa L.) and assessing the impact on soil microbial parameters and enzyme activity. Environ. Monit. Assess. 2023, 195, 910. [Google Scholar] [CrossRef] [PubMed]
  3. Hanafiah, N.M.; Mispan, M.S.; Lim, P.E.; Baisakh, N.; Cheng, A. The 21st century agriculture: When rice research draws attention to climate variability and how weedy rice and underutilized grains come in handy. Plants 2020, 9, 365. [Google Scholar] [CrossRef] [PubMed]
  4. Mohapatra, P.K.; Sahu, B.B. Diversity of Panicle Architecture and Traits Influencing Grain Filling. In Panicle Architecture of Rice and Its Relationship with Grain Filling; Springer International Publishing: Cham, Switzerland, 2022; pp. 107–128. ISBN 978-3-030-67897-5. [Google Scholar]
  5. Pickson, R.B.; He, G.; Boateng, E. Impacts of climate change on rice production: Evidence from 30 Chinese provinces. Environ. Dev. Sustain. 2022, 24, 3907–3925. [Google Scholar] [CrossRef]
  6. Dar, M.H.; Bano, D.A.; Waza, S.A.; Zaidi, N.W.; Majid, A.; Shikari, A.B.; Ahangar, M.A.; Hossain, M.; Kumar, A.; Singh, U.S. Abiotic Stress Tolerance-Progress and Pathways of Sustainable Rice Production. Sustainability 2021, 13, 2078. [Google Scholar] [CrossRef]
  7. Saud, S.; Wang, D.; Fahad, S.; Alharby, H.F.; Bamagoos, A.A.; Mjrashi, A.; Alabdallah, N.M.; AlZahrani, S.S.; AbdElgawad, H.; Adnan, M.; et al. Comprehensive Impacts of Climate Change on Rice Production and Adaptive Strategies in China. Front. Microbiol. 2022, 13, 926059. [Google Scholar] [CrossRef] [PubMed]
  8. Aguilar-Rivera, N.; Michel-Cuello, C.; Cárdenas-González, J.F. Green Revolution and Sustainable Development. In Encyclopedia of Sustainability in Higher Education; Leal Filho, W., Ed.; Springer International Publishing: Cham, Switzerland, 2019; pp. 833–850. ISBN 978-3-030-11352-0. [Google Scholar]
  9. Iqbal, J.; Zia-ul-Qamar; Yousaf, U.; Asgher, A.; Dilshad, R.; Qamar, F.M.; Bibi, S.; Rehman, S.U.; Haroon, M. Sustainable Rice Production Under Biotic and Abiotic Stress Challenges. In Sustainable Agriculture in the Era of the OMICs Revolution; Prakash, C.S., Fiaz, S., Nadeem, M.A., Baloch, F.S., Qayyum, A., Eds.; Springer International Publishing: Cham, Switzerland, 2023; pp. 241–268. ISBN 978-3-031-15568-0. [Google Scholar]
  10. Yang, Y.; Yu, J.; Qian, Q.; Shang, L. Enhancement of Heat and Drought Stress Tolerance in Rice by Genetic Manipulation: A Systematic Review. Rice 2022, 15, 67. [Google Scholar] [CrossRef]
  11. Hussain, S.; Khaliq, A.; Ali, B.; Hussain, H.A. Temperature Extremes: Impact on Rice Growth and Development. In Plant Abiotic Stress Tolerance; Springer: Berlin/Heidelberg, Germany, 2019. [Google Scholar] [CrossRef]
  12. Oladosu, Y.; Rafii, M.Y.; Samuel, C.; Fatai, A.; Magaji, U.; Kareem, I.; Kamarudin, Z.S.; Muhammad, I.; Kolapo, K. Drought Resistance in Rice from Conventional to Molecular Breeding: A Review. Int. J. Mol. Sci. 2019, 20, 3519. [Google Scholar] [CrossRef]
  13. Fahad, S.; Adnan, M.; Hassan, S.; Saud, S.; Hussain, S.; Wu, C.; Wang, D.; Hakeem, K.R.; Alharby, H.F.; Turan, V.; et al. Chapter 10—Rice Responses and Tolerance to High Temperature; Hasanuzzaman, M., Fujita, M., Nahar, K., Biswas, J.K., Eds.; Woodhead Publishing: Sawston, UK, 2019; pp. 201–224. ISBN 978-0-12-814332-2. [Google Scholar]
  14. Bhattacharya, A. Effect of Low Temperature Stress on Photosynthesis and Allied Traits: A Review; Springer: Singapore, 2022; ISBN 978-981-16-9037-2. [Google Scholar]
  15. Horie, T.; Karahara, I.; Katsuhara, M. Salinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plants. Rice 2012, 5, 11. [Google Scholar] [CrossRef]
  16. Mahmood-ur-Rahman; Ijaz, M.; Qamar, S.; Bukhari, S.A.; Malik, K. Chapter 27—Abiotic Stress Signaling in Rice Crop; Hasanuzzaman, M., Fujita, M., Nahar, K., Biswas, J.K., Eds.; Woodhead Publishing: Sawston, UK, 2019; pp. 551–569. ISBN 978-0-12-814332-2. [Google Scholar]
  17. Suwanmontri, P.; Kamoshita, A.; Fukai, S. Recent changes in rice production in rainfed lowland and irrigated ecosystems in Thailand. Plant Prod. Sci. 2020, 24, 15–28. [Google Scholar] [CrossRef]
  18. Arif, N.; Sharma, N.C.; Yadav, V.; Ramawat, N.; Dubey, N.K.; Tripathi, D.K.; Chauhan, D.K.; Sahi, S. Understanding Heavy Metal Stress in a Rice Crop: Toxicity, Tolerance Mechanisms, and Amelioration Strategies. J. Plant Biol. 2019, 62, 239–253. [Google Scholar] [CrossRef]
  19. Melo, F.V.; Oliveira, M.M.; Saibo, N.J.M.; Lourenço, T.F. Modulation of Abiotic Stress Responses in Rice by E3-Ubiquitin Ligases: A Promising Way to Develop Stress-Tolerant Crops. Front. Plant Sci. 2021, 12, 640193. [Google Scholar] [CrossRef]
  20. Das, G.; Patra, J.K.; Baek, K.H. Insight into MAS: A Molecular Tool for Development of Stress Resistant and Quality of Rice through Gene Stacking. Front. Plant Sci. 2017, 8, 985. [Google Scholar] [CrossRef]
  21. Pandey, V.; Shukla, A. Acclimation and Tolerance Strategies of Rice under Drought Stress. Rice Sci. 2015, 22, 147–161. [Google Scholar] [CrossRef]
  22. Miyan, M.A. Droughts in asian least developed countries: Vulnerability and sustainability. Weather Clim. Extrem. 2015, 7, 8–23. [Google Scholar] [CrossRef]
  23. Yang, X.; Wang, B.; Chen, L.; Li, P.; Cao, C. The Different Influences of Drought Stress at the Flowering Stage on Rice Physiological Traits, Grain Yield, and Quality. Sci. Rep. 2019, 9, 3742. [Google Scholar] [CrossRef]
  24. Venuprasad, R.; Lafitte, H.R.; Atlin, G.N. Response to direct selection for grain yield under drought stress in rice. Crop Sci. 2007, 47, 285–293. [Google Scholar] [CrossRef]
  25. Lafitte, H.; Ismail, A.; Bennett, J. Abiotic Stress Tolerance in Rice for Asia: Progress and the Future. In Proceedings of the 4th International Crop Science Congress, Brisbane, Australia, 26 September–1 October 2004. [Google Scholar]
  26. Upadhyaya, H.; Panda, S.K. Chapter 9—Drought Stress Responses and Its Management in Rice; Hasanuzzaman, M., Fujita, M., Nahar, K., Biswas, J.K., Eds.; Woodhead Publishing: Sawston, UK, 2019; ISBN 978-0-12-814332-2. [Google Scholar]
  27. Farooq, M.; Wahid, A.; Kobayashi, N.; Fujita, D.; Basra, S.M.A. Plant Drought Stress: Effects, Mechanisms and Management. In Sustainable Agriculture; Springer: Dordrecht, The Netherlands, 2009; pp. 153–188. [Google Scholar] [CrossRef]
  28. Caine, R.S.; Yin, X.; Sloan, J.; Harrison, E.L.; Mohammed, U.; Fulton, T.; Biswal, A.K.; Dionora, J.; Chater, C.C.; Coe, R.A.; et al. Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol. 2019, 221, 371–384. [Google Scholar] [CrossRef] [PubMed]
  29. Zampieri, E.; Pesenti, M.; Nocito, F.F.; Sacchi, G.A.; Valè, G. Rice Responses to Water Limiting Conditions: Improving Stress Management by Exploiting Genetics and Physiological Processes. Agriculture 2023, 13, 464. [Google Scholar] [CrossRef]
  30. Fukai, S.; Cooper, M. Development of drought-resistant cultivars using physiomorphological traits in rice. Field Crop. Res. 1995, 40, 67–86. [Google Scholar] [CrossRef]
  31. Moonmoon, S.; Islam, M. Effect of Drought Stress at Different Growth Stages on Yield and Yield Components of Six Rice (Oryza sativa L.) Genotypes. Fundam. Appl. Agric. 2017, 2, 285–289. [Google Scholar] [CrossRef]
  32. Ranjan, A.; Sinha, R.; Singla-Pareek, S.L.; Pareek, A.; Singh, A.K. Shaping the root system architecture in plants for adaptation to drought stress. Physiol. Plant. 2022, 174, e13651. [Google Scholar] [CrossRef] [PubMed]
  33. Kim, Y.; Chung, Y.S.; Lee, E.; Tripathi, P.; Heo, S.; Kim, K.-H.K.-H. Root Response to Drought Stress in Rice (Oryza Sativa L.). Int. J. Mol. Sci 2020, 21, 1513. [Google Scholar] [CrossRef] [PubMed]
  34. Champoux, M.C.; Wang, G.; Sarkarung, S.; Mackill, D.J.; O’Toole, J.C.; Huang, N.; McCouch, S.R. Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. Theor. Appl. Genet. 1995, 90, 969–981. [Google Scholar] [CrossRef] [PubMed]
  35. Bañoc, D.M.; Yamauchi, A.; Kamoshita, A.; Wade, L.J.; Pardales, J.R. Dry Matter Production and Root System Development of Rice Cultivars under Fluctuating Soil Moisture. Plant Prod. Sci. 2000, 3, 197–207. [Google Scholar] [CrossRef]
  36. Bañoc, D.M.; Yamauchi, A.; Kamoshita, A.; Wade, L.J.; Pardales, J.R. Genotypic Variations in Response of Lateral Root Development to Fluctuating Soil Moisture in Rice. Plant Prod. Sci. 2000, 3, 335–343. [Google Scholar] [CrossRef]
  37. Henry, A.; Cal, A.J.; Batoto, T.C.; Torres, R.O.; Serraj, R. Root attributes affecting water uptake of rice (Oryza sativa) under drought. J. Exp. Bot. 2012, 63, 4751–4763. [Google Scholar] [CrossRef]
  38. Fang, Y.; Xiong, L. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell. Mol. Life Sci. 2015, 72, 673–689. [Google Scholar] [CrossRef]
  39. Farooq, M.; Kobayashi, N.; Ito, O.; Wahid, A.; Serraj, R. Broader leaves result in better performance of indica rice under drought stress. J. Plant Physiol. 2010, 167, 1066–1075. [Google Scholar] [CrossRef]
  40. Kavi Kishor, P.B.; Sangam, S.; Amrutha, R.N.; Sri Laxmi, P.; Naidu, K.R.; Rao, K.R.S.S.; Rao, S.; Reddy, K.J.; Theriappan, P.; Sreenivasulu, N. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr. Sci. 2005, 88, 424–438. [Google Scholar]
  41. Zhu, R.; Wu, F.; Zhou, S.; Hu, T.; Huang, J.; Gao, Y. Cumulative effects of drought–flood abrupt alternation on the photosynthetic characteristics of rice. Environ. Exp. Bot. 2020, 169, 103901. [Google Scholar] [CrossRef]
  42. Mishra, S.S.; Behera, P.K.; Kumar, V.; Lenka, S.K.; Panda, D. Physiological characterization and allelic diversity of selected drought tolerant traditional rice (Oryza sativa L.) landraces of Koraput, India. Physiol. Mol. Biol. Plants 2018, 24, 1035–1046. [Google Scholar] [CrossRef] [PubMed]
  43. Farooq, M.; Kobayashi, N.; Wahid, A.; Ito, O.; Basra, S.M.A. Strategies for Producing More Rice with Less Water. In Advances in Agronomy; Elsevier: San Diego, CA, USA, 2009; Volume 101, p. e1. [Google Scholar] [CrossRef]
  44. Panda, D.; Mishra, S.S.; Behera, P.K. Drought Tolerance in Rice: Focus on Recent Mechanisms and Approaches. Rice Sci. 2021, 28, 119–132. [Google Scholar] [CrossRef]
  45. Fahad, S.; Bajwa, A.A.; Nazir, U.; Anjum, S.A.; Farooq, A.; Zohaib, A.; Sadia, S.; Nasim, W.; Adkins, S.; Saud, S.; et al. Crop Production under Drought and Heat Stress: Plant Responses and Management Options. Front. Plant Sci. 2017, 8, 1147. [Google Scholar] [CrossRef]
  46. Gupta, A.; Rico-Medina, A.; Caño-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269. [Google Scholar] [CrossRef] [PubMed]
  47. Ashraf, M.; Harris, P.J.C. Photosynthesis under stressful environments: An overview. Photosynthetica 2013, 51, 163–190. [Google Scholar] [CrossRef]
  48. Zhang, F.-J.; Zhang, K.-K.; Du, C.-Z.; Li, J.; Xing, Y.-X.; Yang, L.-T.; Li, Y.-R. Effect of Drought Stress on Anatomical Structure and Chloroplast Ultrastructure in Leaves of Sugarcane. Sugar Tech 2015, 17, 41–48. [Google Scholar] [CrossRef]
  49. Ayyaz, A.; Fang, R.; Ma, J.; Hannan, F.; Huang, Q.; Athar, H.-R.; Sun, Y.; Javed, M.; Ali, S.; Zhou, W.; et al. Calcium nanoparticles (Ca-NPs) improve drought stress tolerance in Brassica napus by modulating the photosystem II, nutrient acquisition and antioxidant performance. NanoImpact 2022, 28, 100423. [Google Scholar] [CrossRef]
  50. Zahra, N.; Hafeez, M.B.; Kausar, A.; Al Zeidi, M.; Asekova, S.; Siddique, K.H.M.M.; Farooq, M.; Al Zeidi, M.; Asekova, S.; Siddique, K.H.M.M.; et al. Plant photosynthetic responses under drought stress: Effects and management. J. Agron. Crop Sci. 2023, 209, 651–672. [Google Scholar] [CrossRef]
  51. Lum, M.S.; Hanafi, M.M.; Rafii, Y.M.; Akmar, A.S.N. Effect of drought stress on growth, proline and antioxidant enzyme activities of upland rice. J. Anim. Plant Sci. 2014, 24, 1487–1493. [Google Scholar]
  52. Schlicke, H.; Hartwig, A.S.; Firtzlaff, V.; Richter, A.S.; Glässer, C.; Maier, K.; Finkemeier, I.; Grimm, B. Induced Deactivation of Genes Encoding Chlorophyll Biosynthesis Enzymes Disentangles Tetrapyrrole-Mediated Retrograde Signaling. Mol. Plant 2014, 7, 1211–1227. [Google Scholar] [CrossRef] [PubMed]
  53. Busch, A.W.U.; Montgomery, B.L. Interdependence of tetrapyrrole metabolism, the generation of oxidative stress and the mitigative oxidative stress response. Redox Biol. 2015, 4, 260–271. [Google Scholar] [CrossRef] [PubMed]
  54. Hasanuzzaman, M.; Hossain, M.A.; da Silva, J.A.T.; Fujita, M. Plant Response and Tolerance to Abiotic Oxidative Stress: Antioxidant Defense Is a Key Factor. In Crop Stress and its Management: Perspectives and Strategies; Springer: Dordrecht, The Netherlands, 2012; pp. 261–315. [Google Scholar] [CrossRef]
  55. Asada, K. The Water-Water Cycle In Chloroplasts: Scavenging of Active Oxygens and Dissipation of Excess Photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 601–639. [Google Scholar] [CrossRef] [PubMed]
  56. Cruz de Carvalho, M.H. Drought stress and reactive oxygen species. Plant Signal. Behav. 2008, 3, 156–165. [Google Scholar] [CrossRef] [PubMed]
  57. Wang, X.; Liu, H.; Yu, F.; Hu, B.; Jia, Y.; Sha, H.; Zhao, H. Differential Activity of the Antioxidant Defence System and Alterations in the Accumulation of Osmolyte and Reactive Oxygen Species under Drought Stress and Recovery in Rice (Oryza Sativa L.) Tillering. Sci. Rep. 2019, 9, 8543. [Google Scholar] [CrossRef] [PubMed]
  58. Bhattacharjee, S.; Dey, N. Redox metabolic and molecular parameters for screening drought tolerant indigenous aromatic rice cultivars. Physiol. Mol. Biol. Plants 2018, 24, 7–23. [Google Scholar] [CrossRef] [PubMed]
  59. Dey, N.; Bhattacharjee, S. Accumulation of Polyphenolic Compounds and Osmolytes under Dehydration Stress and Their Implication in Redox Regulation in Four Indigenous Aromatic Rice Cultivars. Rice Sci. 2020, 27, 329–344. [Google Scholar] [CrossRef]
  60. Chen, D.; Shao, Q.; Yin, L.; Younis, A.; Zheng, B. Polyamine Function in Plants: Metabolism, Regulation on Development, and Roles in Abiotic Stress Responses. Front. Plant Sci. 2019, 9, 1945. [Google Scholar] [CrossRef]
  61. Capell, T.; Bassie, L.; Christou, P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl. Acad. Sci. USA 2004, 101, 9909–9914. [Google Scholar] [CrossRef]
  62. Kuru, İ.; Işıkalan, Ç.; Akbaş, F. Physiological and Biochemical Responses of Rice (Oryza Sativa L.) Varieties Against Drought Stress. Bangladesh J. Bot. 2021, 50, 335–342. [Google Scholar] [CrossRef]
  63. Fujita, M.; Fujita, Y.; Noutoshi, Y.; Takahashi, F.; Narusaka, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006, 9, 436–442. [Google Scholar] [CrossRef] [PubMed]
  64. Hoang, X.L.T.; Nhi, D.N.H.; Thu, N.B.A.; Thao, N.P.; Tran, L.-S.P. Transcription Factors and Their Roles in Signal Transduction in Plants under Abiotic Stresses. Curr. Genom. 2017, 18, 483–497. [Google Scholar] [CrossRef] [PubMed]
  65. Gao, J.-P.; Chao, D.-Y.; Lin, H.-X. Toward understanding molecular mechanisms of abiotic stress responses in rice. Rice 2008, 1, 36–51. [Google Scholar] [CrossRef]
  66. Maruyama, K.; Todaka, D.; Mizoi, J.; Yoshida, T.; Kidokoro, S.; Matsukura, S.; Takasaki, H.; Sakurai, T.; Yamamoto, Y.Y.; Yoshiwara, K.; et al. Identification of Cis-Acting Promoter Elements in Cold- and Dehydration-Induced Transcriptional Pathways in Arabidopsis, Rice, and Soybean. DNA Res. 2012, 19, 37–49. [Google Scholar] [CrossRef] [PubMed]
  67. Deng, Y.; Kashtoh, H.; Wang, Q.; Zhen, G.; Li, Q.; Tang, L.; Gao, H.; Zhang, C.; Qin, L.; Su, M.; et al. Structure and activity of SLAC1 channels for stomatal signaling in leaves. Proc. Natl. Acad. Sci. USA 2021, 118, e2015151118. [Google Scholar] [CrossRef] [PubMed]
  68. Kashtoh, H.; Baek, K.-H. Structural and Functional Insights into the Role of Guard Cell Ion Channels in Abiotic Stress-Induced Stomatal Closure. Plants 2021, 10, 2774. [Google Scholar] [CrossRef] [PubMed]
  69. Ma, Y.; Szostkiewicz, I.; Korte, A.; Moes, D.; Yang, Y.; Christmann, A.; Grill, E. Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors. Science 2009, 324, 1064–1068. [Google Scholar] [CrossRef]
  70. Park, S.-Y.; Fung, P.; Nishimura, N.; Jensen, D.R.; Fujii, H.; Zhao, Y.; Lumba, S.; Santiago, J.; Rodrigues, A.; Chow, T.F.; et al. Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins. Science 2009, 324, 1068–1071. [Google Scholar] [CrossRef]
  71. Chen, X.; Ding, Y.; Yang, Y.; Song, C.; Wang, B.; Yang, S.; Guo, Y.; Gong, Z. Protein kinases in plant responses to drought, salt, and cold stress. J. Integr. Plant Biol. 2021, 63, 53–78. [Google Scholar] [CrossRef]
  72. Kim, H.; Lee, K.; Hwang, H.; Bhatnagar, N.; Kim, D.-Y.; Yoon, I.S.; Byun, M.-O.; Kim, S.T.; Jung, K.-H.; Kim, B.-G. Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression. J. Exp. Bot. 2014, 65, 453–464. [Google Scholar] [CrossRef]
  73. Matsukura, S.; Mizoi, J.; Yoshida, T.; Todaka, D.; Ito, Y.; Maruyama, K.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol. Genet. Genom. 2010, 283, 185–196. [Google Scholar] [CrossRef] [PubMed]
  74. Blum, A. Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crop. Res. 2009, 112, 119–123. [Google Scholar] [CrossRef]
  75. Uga, Y.; Sugimoto, K.; Ogawa, S.; Rane, J.; Ishitani, M.; Hara, N.; Kitomi, Y.; Inukai, Y.; Ono, K.; Kanno, N.; et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 2013, 45, 1097–1102. [Google Scholar] [CrossRef] [PubMed]
  76. Rahman, H.; Ramanathan, V.; Nallathambi, J.; Duraialagaraja, S.; Muthurajan, R. Over-expression of a NAC 67 transcription factor from finger millet (Eleusine coracana L.) confers tolerance against salinity and drought stress in rice. BMC Biotechnol. 2016, 16, 35. [Google Scholar] [CrossRef] [PubMed]
  77. Ning, J.; Li, X.; Hicks, L.M.; Xiong, L. A raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 2010, 152, 876–890. [Google Scholar] [CrossRef] [PubMed]
  78. Rahman, A.; Nahar, K.; Hasanuzzaman, M.; Fujita, M. Calcium Supplementation Improves Na+/K+ Ratio, Antioxidant Defense and Glyoxalase Systems in Salt-Stressed Rice Seedlings. Front. Plant Sci. 2016, 7, 609. [Google Scholar] [CrossRef] [PubMed]
  79. Jeong, J.S.; Kim, Y.S.; Redillas, M.C.F.R.; Jang, G.; Jung, H.; Bang, S.W.; Choi, Y.D.; Ha, S.H.; Reuzeau, C.; Kim, J.K. OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol. J. 2013, 11, 101–114. [Google Scholar] [CrossRef]
  80. Hu, H.; Dai, M.; Yao, J.; Xiao, B.; Li, X.; Zhang, Q.; Xiong, L. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. USA 2006, 103, 12987–12992. [Google Scholar] [CrossRef]
  81. Xiao, B.; Huang, Y.; Tang, N.; Xiong, L. Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor. Appl. Genet. 2007, 115, 35–46. [Google Scholar] [CrossRef]
  82. Xiang, Y.; Tang, N.; Du, H.; Ye, H.; Xiong, L. Characterization of OsbZIP23 as a Key Player of the Basic Leucine Zipper Transcription Factor Family for Conferring Abscisic Acid Sensitivity and Salinity and Drought Tolerance in Rice. Plant Physiol. 2008, 148, 1938–1952. [Google Scholar] [CrossRef]
  83. Lu, G.; Gao, C.; Zheng, X.; Han, B. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 2009, 229, 605–615. [Google Scholar] [CrossRef] [PubMed]
  84. Oh, S.J.; Kim, Y.S.; Kwon, C.W.; Park, H.K.; Jeong, J.S.; Kim, J.K. Overexpression of the Transcription Factor AP37 in Rice Improves Grain Yield under Drought Conditions. Plant Physiol. 2009, 150, 1368–1379. [Google Scholar] [CrossRef] [PubMed]
  85. Jeong, J.S.; Kim, Y.S.; Baek, K.H.; Jung, H.; Ha, S.H.; Choi, Y.D.Y.D.; Kim, M.; Reuzeau, C.; Kim, J.K. Root-Specific Expression of OsNAC10 Improves Drought Tolerance and Grain Yield in Rice under Field Drought Conditions. Plant Physiol. 2010, 153, 185–197. [Google Scholar] [CrossRef] [PubMed]
  86. Yu, L.; Chen, X.; Wang, Z.; Wang, S.; Wang, Y.; Zhu, Q.; Li, S.; Xiang, C. Arabidopsis Enhanced Drought Tolerance1/HOMEODOMAIN GLABROUS11 Confers Drought Tolerance in Transgenic Rice without Yield Penalty. Plant Physiol. 2013, 162, 1378–1391. [Google Scholar] [CrossRef] [PubMed]
  87. Ravikumar, G.; Manimaran, P.; Voleti, S.R.; Subrahmanyam, D.; Sundaram, R.M.; Bansal, K.C.; Viraktamath, B.C.; Balachandran, S.M. Stress-inducible expression of AtDREB1A transcription factor greatly improves drought stress tolerance in transgenic indica rice. Transgenic Res. 2014, 23, 421–439. [Google Scholar] [CrossRef] [PubMed]
  88. Wei, S.; Hu, W.; Deng, X.; Zhang, Y.; Liu, X.; Zhao, X.; Luo, Q.; Jin, Z.; Li, Y.; Zhou, S.; et al. A Rice Calcium-Dependent Protein Kinase OsCPK9 Positively Regulates Drought Stress Tolerance and Spikelet Fertility. BMC Plant Biol. 2014, 14, 133. [Google Scholar] [CrossRef]
  89. You, J.; Hu, H.; Xiong, L. An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci. 2012, 197, 59–69. [Google Scholar] [CrossRef] [PubMed]
  90. Li, H.-W.; Zang, B.-S.; Deng, X.-W.; Wang, X.-P. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 2011, 234, 1007–1018. [Google Scholar] [CrossRef]
  91. Zhu, B.; Su, J.; Chang, M.; Verma, D.P.S.; Fan, Y.-L.; Wu, R. Overexpression of a Δ1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. Plant Sci. 1998, 139, 41–48. [Google Scholar] [CrossRef]
  92. Chandra Babu, R.; Zhang, J.; Blum, A.; David Ho, T.-H.; Wu, R.; Nguyen, H. HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci. 2004, 166, 855–862. [Google Scholar] [CrossRef]
  93. Zhang, L.; Xiao, S.; Li, W.; Feng, W.; Li, J.; Wu, Z.; Gao, X.; Liu, F.; Shao, M. Overexpression of a Harpin-encoding gene hrf1 in rice enhances drought tolerance. J. Exp. Bot. 2011, 62, 4229–4238. [Google Scholar] [CrossRef] [PubMed]
  94. Zhang, Z.; Li, F.; Li, D.; Zhang, H.; Huang, R. Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 2010, 232, 765–774. [Google Scholar] [CrossRef] [PubMed]
  95. Bae, H.; Kim, S.K.; Cho, S.K.; Kang, B.G.; Kim, W.T. Overexpression of OsRDCP1, a rice RING domain-containing E3 ubiquitin ligase, increased tolerance to drought stress in rice (Oryza sativa L.). Plant Sci. 2011, 180, 775–782. [Google Scholar] [CrossRef]
  96. Gao, T.; Wu, Y.; Zhang, Y.; Liu, L.; Ning, Y.; Wang, D.; Tong, H.; Chen, S.; Chu, C.; Xie, Q. OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol. Biol. 2011, 76, 145–156. [Google Scholar] [CrossRef] [PubMed]
  97. You, J.; Zong, W.; Li, X.; Ning, J.; Hu, H.; Li, X.; Xiao, J.; Xiong, L. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J. Exp. Bot. 2013, 64, 569–583. [Google Scholar] [CrossRef] [PubMed]
  98. Samota, M.K.; Sasi, M.; Awana, M.; Yadav, O.P.; Amitha Mithra, S.V.; Tyagi, A.; Kumar, S.; Singh, A. Elicitor-Induced Biochemical and Molecular Manifestations to Improve Drought Tolerance in Rice (Oryza Sativa L.) through Seed-Priming. Front. Plant Sci. 2017, 8, 934. [Google Scholar] [CrossRef]
  99. Pandey, V.; Ansari, M.W.; Tula, S.; Yadav, S.; Sahoo, R.K.; Shukla, N.; Bains, G.; Badal, S.; Chandra, S.; Gaur, A.K.; et al. Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 2016, 243, 1251–1264. [Google Scholar] [CrossRef]
  100. Wu, C.; Cui, K.; Wang, W.; Li, Q.; Fahad, S.; Hu, Q.; Huang, J.; Nie, L.; Peng, S. Heat-Induced Phytohormone Changes Are Associated with Disrupted Early Reproductive Development and Reduced Yield in Rice. Sci. Rep. 2016, 6, 34978. [Google Scholar] [CrossRef]
  101. Zhao, C.; Liu, B.; Piao, S.; Wang, X.; Lobell, D.B.; Huang, Y.; Huang, M.; Yao, Y.; Bassu, S.; Ciais, P.; et al. Temperature increase reduces global yields of major crops in four independent estimates. Proc. Natl. Acad. Sci. USA 2017, 114, 9326–9331. [Google Scholar] [CrossRef]
  102. Kilasi, N.L.; Singh, J.; Vallejos, C.E.; Ye, C.; Jagadish, S.V.K.; Kusolwa, P.; Rathinasabapathi, B. Heat Stress Tolerance in Rice (Oryza Sativa L.): Identification of Quantitative Trait Loci and Candidate Genes for Seedling Growth Under Heat Stress. Front. Plant Sci. 2018, 9, 1578. [Google Scholar] [CrossRef]
  103. Wang, Y.; Wang, L.; Zhou, J.; Hu, S.; Chen, H.; Xiang, J.; Zhang, Y.Y.Y.; Zeng, Y.; Shi, Q.; Zhu, D.; et al. Research Progress on Heat Stress of Rice at Flowering Stage. Rice Sci. 2019, 26, 1–10. [Google Scholar] [CrossRef]
  104. Ishimaru, T.; Hirabayashi, H.; Kuwagata, T.; Ogawa, T.; Kondo, M. The Early-Morning Flowering Trait of Rice Reduces Spikelet Sterility under Windy and Elevated Temperature Conditions at Anthesis. Plant Prod. Sci. 2012, 15, 19–22. [Google Scholar] [CrossRef]
  105. Fahad, S.; Ihsan, M.Z.; Khaliq, A.; Daur, I.; Saud, S.; Alzamanan, S.; Nasim, W.; Abdullah, M.; Khan, I.A.; Wu, C.; et al. Consequences of high temperature under changing climate optima for rice pollen characteristics-concepts and perspectives. Arch. Agron. Soil Sci. 2018, 64, 1473–1488. [Google Scholar] [CrossRef]
  106. Ranathunge, K.; Steudle, E.; Lafitte, R. Control of water uptake by rice (Oryza sativa L.): Role of the outer part of the root. Planta 2003, 217, 193–205. [Google Scholar] [CrossRef]
  107. Khan, S.; Anwar, S.; Ashraf, M.Y.; Khaliq, B.; Sun, M.; Hussain, S.; Gao, Z.; Noor, H.; Alam, S. Mechanisms and Adaptation Strategies to Improve Heat Tolerance in Rice. A Review. Plants 2019, 8, 508. [Google Scholar] [CrossRef] [PubMed]
  108. Ren, H.; Bao, J.; Gao, Z.; Sun, D.; Zheng, S.; Bai, J. How rice adapts to high temperatures. Front. Plant Sci. 2023, 14, 1137923. [Google Scholar] [CrossRef] [PubMed]
  109. González-García, M.P.; Conesa, C.M.; Lozano-Enguita, A.; Baca-González, V.; Simancas, B.; Navarro-Neila, S.; Sánchez-Bermúdez, M.; Salas-González, I.; Caro, E.; Castrillo, G.; et al. Temperature changes in the root ecosystem affect plant functionality. Plant Commun. 2023, 4, 100514. [Google Scholar] [CrossRef] [PubMed]
  110. Arai-Sanoh, Y.; Ishimaru, T.; Ohsumi, A.; Kondo, M. Effects of Soil Temperature on Growth and Root Function in Rice. Plant Prod. Sci. 2010, 13, 235–242. [Google Scholar] [CrossRef]
  111. Yamakawa, Y.; Kishikawa, H. On the Effect of Temperature upon the Division and Elongation of Cells in the Root of Rice Plant. Jpn. J. Crop Sci. 1957, 26, 94–95. [Google Scholar] [CrossRef]
  112. Liu, J.; Hasanuzzaman, M.; Wen, H.; Zhang, J.; Peng, T.; Sun, H.; Zhao, Q. High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice. Protoplasma 2019, 256, 1217–1227. [Google Scholar] [CrossRef]
  113. Liu, J.; Sun, X.; Xu, F.; Zhang, Y.; Zhang, Q.; Miao, R.; Zhang, J.; Liang, J.; Xu, W. Suppression of OsMDHAR4 Enhances Heat Tolerance by Mediating H2O2-Induced Stomatal Closure in Rice Plants. Rice 2018, 11, 38. [Google Scholar] [CrossRef] [PubMed]
  114. Chaudhary, T.N.; Ghildyal, B.P. Germination Response of Rice Seeds to Constant and Alternating Temperatures. Agron. J. 1969, 61, 328–330. [Google Scholar] [CrossRef]
  115. Baker, J.T. Yield responses of southern US rice cultivars to CO2 and temperature. Agric. For. Meteorol. 2004, 122, 129–137. [Google Scholar] [CrossRef]
  116. Sandhu, J.; Irvin, L.; Liu, K.; Staswick, P.; Zhang, C.; Walia, H. Endoplasmic Reticulum Stress Pathway Mediates the Early Heat Stress Response of Developing Rice Seeds. Plant. Cell Environ. 2021, 44, 2604–2624. [Google Scholar] [CrossRef] [PubMed]
  117. Jagadish, S.V.K.; Murty, M.V.R.; Quick, W.P. Rice Responses to Rising Temperatures--Challenges, Perspectives and Future Directions. Plant. Cell Environ. 2015, 38, 1686–1698. [Google Scholar] [CrossRef] [PubMed]
  118. Arshad, M.S.; Farooq, M.; Asch, F.; Krishna, J.S.V.; Prasad, P.V.V.; Siddique, K.H.M. Thermal stress impacts reproductive development and grain yield in rice. Plant Physiol. Biochem. 2017, 115, 57–72. [Google Scholar] [CrossRef] [PubMed]
  119. Soda, N.; Gupta, B.K.; Anwar, K.; Sharan, A.; Govindjee, S.-P.L.S.; Pareek, A.; Govindjee; Singla-Pareek, S.L.; Pareek, A. Rice Intermediate Filament, OsIF, Stabilizes Photosynthetic Machinery and Yield under Salinity and Heat Stress. Sci. Rep. 2018, 8, 4072. [Google Scholar] [CrossRef] [PubMed]
  120. Wang, H.H.; Wang, H.H.; Shao, H.; Tang, X. Recent Advances in Utilizing Transcription Factors to Improve Plant Abiotic Stress Tolerance by Transgenic Technology. Front. Plant Sci. 2016, 7, 67. [Google Scholar] [CrossRef]
  121. Miyahara, K.; Wada, T.; Sonoda, J.-Y.; Tsukaguchi, T.; Miyazaki, M.; Tsubone, M.; Yamaguchi, O.; Ishibashi, M.; Iwasawa, N.; Umemoto, T.; et al. Detection and validation of QTLs for milky-white grains caused by high temperature during the ripening period in Japonica rice. Breed. Sci. 2017, 67, 333–339. [Google Scholar] [CrossRef]
  122. Kaneko, K.; Sasaki, M.; Kuribayashi, N.; Suzuki, H.; Sasuga, Y.; Shiraya, T.; Inomata, T.; Itoh, K.; Baslam, M.; Mitsui, T. Proteomic and Glycomic Characterization of Rice Chalky Grains Produced Under Moderate and High-Temperature Conditions in Field System. Rice 2016, 9, 26. [Google Scholar] [CrossRef]
  123. Nevame, A.Y.M.; Emon, R.M.; Malek, M.A.; Hasan, M.M.; Alam, M.A.; Muharam, F.M.; Aslani, F.; Rafii, M.Y.; Ismail, M.R. Relationship between High Temperature and Formation of Chalkiness and Their Effects on Quality of Rice. Biomed Res. Int. 2018, 1653721, 1653721. [Google Scholar] [CrossRef] [PubMed]
  124. Wada, T.; Miyahara, K.; Sonoda, J.-Y.; Tsukaguchi, T.; Miyazaki, M.; Tsubone, M.; Ando, T.; Ebana, K.; Yamamoto, T.; Iwasawa, N.; et al. Detection of QTLs for white-back and basal-white grains caused by high temperature during ripening period in japonica rice. Breed. Sci. 2015, 65, 216–225. [Google Scholar] [CrossRef] [PubMed]
  125. Wu, Y.S.; Yang, C.Y. Ethylene-Mediated Signaling Confers Thermotolerance and Regulates Transcript Levels of Heat Shock Factors in Rice Seedlings under Heat Stress. Bot. Stud. 2019, 60, 23. [Google Scholar] [CrossRef] [PubMed]
  126. Li, S.; Jiang, H.; Wang, J.; Wang, Y.; Pan, S.; Tian, H.; Duan, M.; Wang, S.; Tang, X.; Mo, Z. Responses of Plant Growth, Physiological, Gas Exchange Parameters of Super and Non-Super Rice to Rhizosphere Temperature at the Tillering Stage. Sci. Rep. 2019, 9, 10618. [Google Scholar] [CrossRef] [PubMed]
  127. Li, X.-M.; Chao, D.-Y.; Wu, Y.; Huang, X.; Chen, K.; Cui, L.-G.; Su, L.; Ye, W.-W.; Chen, H.; Chen, H.-C.; et al. Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat. Genet. 2015, 47, 827–833. [Google Scholar] [CrossRef] [PubMed]
  128. Allakhverdiev, S.I.; Kreslavski, V.D.; Klimov, V.V.; Los, D.A.; Carpentier, R.; Mohanty, P. Heat stress: An overview of molecular responses in photosynthesis. Photosynth. Res. 2008, 98, 541–550. [Google Scholar] [CrossRef] [PubMed]
  129. Rodriguez, M.; Canales, E.; Borras-Hidalgo, O. Molecular aspects of abiotic stress in plants. Biotecnol. Apl. 2005, 22, 1–10. [Google Scholar]
  130. Djanaguiraman, M.; Annie Sheeba, J.; Durga Devi, D.; Bangarusamy, U. Cotton Leaf Senescence Can Be Delayed by Nitrophenolate Spray through Enhanced Antioxidant Defence System. J. Agron. Crop Sci. 2009, 195, 213–224. [Google Scholar] [CrossRef]
  131. Zhao, Q.; Zhou, L.; Liu, J.; Du, X.; Asad, M.-A.-U.; Huang, F.; Pan, G.; Cheng, F. Relationship of ROS accumulation and superoxide dismutase isozymes in developing anther with floret fertility of rice under heat stress. Plant Physiol. Biochem. PPB 2018, 122, 90–101. [Google Scholar] [CrossRef]
  132. Awasthi, R.; Bhandari, K.; Nayyar, H. Temperature stress and redox homeostasis in agricultural crops. Front. Environ. Sci. 2015, 3, 11. [Google Scholar] [CrossRef]
  133. Soengas, P.; Rodríguez, V.M.; Velasco, P.; Cartea, M.E. Effect of Temperature Stress on Antioxidant Defenses in Brassica Oleracea. ACS Omega 2018, 3, 5237–5243. [Google Scholar] [CrossRef] [PubMed]
  134. Hasanuzzaman, M.; Nahar, K.; Alam, M.; Roychowdhury, R.; Fujita, M. Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants. Int. J. Mol. Sci. 2013, 14, 9643–9684. [Google Scholar] [CrossRef] [PubMed]
  135. Zou, J.; Liu, C.; Chen, X. Proteomics of rice in response to heat stress and advances in genetic engineering for heat tolerance in rice. Plant Cell Rep. 2011, 30, 2155–2165. [Google Scholar] [CrossRef] [PubMed]
  136. Lee, B.-H.; Won, S.-H.; Lee, H.-S.; Miyao, M.; Chung, W.-I.; Kim, I.-J.; Jo, J. Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 2000, 245, 283–290. [Google Scholar] [CrossRef]
  137. Wu, X.; Shiroto, Y.; Kishitani, S.; Ito, Y.; Toriyama, K. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 2009, 28, 21–30. [Google Scholar] [CrossRef] [PubMed]
  138. Fang, Y.; Liao, K.; Du, H.; Xu, Y.; Song, H.; Li, X.; Xiong, L. A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J. Exp. Bot. 2015, 66, 6803–6817. [Google Scholar] [CrossRef] [PubMed]
  139. El-kereamy, A.; Bi, Y.M.; Ranathunge, K.; Beatty, P.H.; Good, A.G.; Rothstein, S.J. The Rice R2R3-MYB Transcription Factor OsMYB55 Is Involved in the Tolerance to High Temperature and Modulates Amino Acid Metabolism. PLoS ONE 2012, 7, 52030. [Google Scholar] [CrossRef]
  140. Ambavaram, M.M.R.; Basu, S.; Krishnan, A.; Ramegowda, V.; Batlang, U.; Rahman, L.; Baisakh, N.; Pereira, A. Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat. Commun. 2014, 5, 5302. [Google Scholar] [CrossRef]
  141. Lim, S.D.; Cho, H.Y.; Park, Y.C.; Ham, D.J.; Lee, J.K.; Jang, C.S. The rice RING finger E3 ligase, OsHCI1, drives nuclear export of multiple substrate proteins and its heterogeneous overexpression enhances acquired thermotolerance. J. Exp. Bot. 2013, 64, 2899–2914. [Google Scholar] [CrossRef]
  142. Zhang, B.; Wu, S.; Zhang, Y.; Xu, T.; Guo, F.; Tang, H.; Li, X.; Wang, P.; Qian, W.; Xue, Y. A High Temperature-Dependent Mitochondrial Lipase EXTRA GLUME1 Promotes Floral Phenotypic Robustness against Temperature Fluctuation in Rice (Oryza sativa L.). PLOS Genet. 2016, 12, e1006152. [Google Scholar] [CrossRef]
  143. Hossain, M.A.; Cho, J.I.; Han, M.; Ahn, C.H.; Jeon, J.S.; An, G.; Park, P.B. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J. Plant Physiol. 2010, 167, 1512–1520. [Google Scholar] [CrossRef]
  144. Liu, J.G.; Qin, Q.-L.; Zhang, Z.; Peng, R.H.; Xiong, A.S.; Chen, J.M.; Yao, Q.H. OsHSF7 Gene in Rice, Oryza Sativa L., Encodes a Transcription Factor That Functions as a High Temperature Receptive and Responsive Factor. BMB Rep. 2009, 42, 16–21. [Google Scholar] [CrossRef]
  145. Lin, M.Y.; Chai, K.H.; Ko, S.S.; Kuang, L.Y.; Lur, H.S.; Charng, Y.Y. A Positive Feedback Loop between Heat Shock Protein101 And Heat Stress-Associated 32-Kd Protein Modulates Long-Term Acquired Thermotolerance Illustrating Diverse Heat Stress Responses in Rice Varieties. Plant Physiol. 2014, 164, 2045–2053. [Google Scholar] [CrossRef] [PubMed]
  146. Liu, J.; Zhang, C.; Wei, C.; Liu, X.; Wang, M.; Yu, F.; Xie, Q.; Tu, J. The RING Finger Ubiquitin E3 Ligase OsHTAS Enhances Heat Tolerance by Promoting H2O2-Induced Stomatal Closure in Rice. Plant Physiol. 2016, 170, 429–443. [Google Scholar] [CrossRef] [PubMed]
  147. Zheng, K.; Zhao, J.; Lin, D.; Chen, J.; Xu, J.; Zhou, H.; Teng, S.; Dong, Y. The Rice TCM5 Gene Encoding a Novel Deg Protease Protein Is Essential for Chloroplast Development under High Temperatures. Rice 2016, 9, 13. [Google Scholar] [CrossRef] [PubMed]
  148. Wang, D.; Qin, B.; Li, X.; Tang, D.; Zhang, Y.; Cheng, Z.; Xue, Y. Nucleolar DEAD-Box RNA Helicase TOGR1 Regulates Thermotolerant Growth as a Pre-rRNA Chaperone in Rice. PLoS Genet. 2016, 12, e1005844. [Google Scholar] [CrossRef] [PubMed]
  149. Xia, S.; Liu, H.; Cui, Y.; Yu, H.; Rao, Y.; Yan, Y.; Zeng, D.; Hu, J.; Zhang, G.; Gao, Z.; et al. UDP-N-Acetylglucosamine Pyrophosphorylase Enhances Rice Survival at High Temperature. New Phytol. 2022, 233, 344–359. [Google Scholar] [CrossRef] [PubMed]
  150. Chen, K.; Guo, T.; Li, X.M.; Zhang, Y.M.; Yang, Y.B.; Ye, W.W.; Dong, N.Q.; Shi, C.L.; Kan, Y.; Xiang, Y.H.; et al. Translational Regulation of Plant Response to High Temperature by a Dual-Function TRNAHis Guanylyltransferase in Rice. Mol. Plant 2019, 12, 1123–1142. [Google Scholar] [CrossRef] [PubMed]
  151. Liu, X.; Lyu, Y.; Yang, W.; Yang, Z.; Lu, S.; Liu, J. A membrane-associated NAC transcription factor OsNTL3 is involved in thermotolerance in rice. Plant Biotechnol. J. 2020, 18, 1317–1329. [Google Scholar] [CrossRef]
  152. Singh, A.; Mittal, D.; Lavania, D.; Agarwal, M.; Mishra, R.C.; Grover, A. OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.). Cell Stress Chaperones 2012, 17, 243–254. [Google Scholar] [CrossRef]
  153. Tang, Y.; Gao, C.-C.; Gao, Y.; Yang, Y.; Shi, B.; Yu, J.-L.; Lyu, C.; Sun, B.-F.; Wang, H.-L.; Xu, Y.; et al. OsNSUN2-Mediated 5-Methylcytosine mRNA Modification Enhances Rice Adaptation to High Temperature. Dev. Cell 2020, 53, 272–286.e7. [Google Scholar] [CrossRef] [PubMed]
  154. Zhang, H.; Zhou, J.-F.; Kan, Y.; Shan, J.-X.; Ye, W.-W.; Dong, N.-Q.; Guo, T.; Xiang, Y.-H.; Yang, Y.-B.; Li, Y.-C.; et al. A genetic module at one locus in rice protects chloroplasts to enhance thermotolerance. Science 2022, 376, 1293–1300. [Google Scholar] [CrossRef] [PubMed]
  155. Qiao, B.; Zhang, Q.; Liu, D.; Wang, H.; Yin, J.; Wang, R.; He, M.; Cui, M.; Shang, Z.; Wang, D.; et al. A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H2O2. J. Exp. Bot. 2015, 66, 5853–5866. [Google Scholar] [CrossRef] [PubMed]
  156. Jeandet, P.; Formela-Luboińska, M.; Labudda, M.; Morkunas, I. The Role of Sugars in Plant Responses to Stress and Their Regulatory Function during Development. Int. J. Mol. Sci. 2022, 23, 5161. [Google Scholar] [CrossRef] [PubMed]
  157. Miyazaki, M.; Araki, M.; Okamura, K.; Ishibashi, Y.; Yuasa, T.; Iwaya-Inoue, M. Assimilate translocation and expression of sucrose transporter, OsSUT1, contribute to high-performance ripening under heat stress in the heat-tolerant rice cultivar Genkitsukushi. J. Plant Physiol. 2013, 170, 1579–1584. [Google Scholar] [CrossRef] [PubMed]
  158. Savada, R.P.; Ozga, J.A.; Jayasinghege, C.P.A.; Waduthanthri, K.D.; Reinecke, D.M. Heat stress differentially modifies ethylene biosynthesis and signaling in pea floral and fruit tissues. Plant Mol. Biol. 2017, 95, 313–331. [Google Scholar] [CrossRef] [PubMed]
  159. Calderón-Páez, S.E.; Cueto-Niño, Y.A.; Sánchez-Reinoso, A.D.; Garces-Varon, G.; Chávez-Arias, C.C.; Restrepo-Díaz, H. Foliar boron compounds applications mitigate heat stress caused by high daytime temperatures in rice (Oryza sativa L.) Boron mitigates heat stress in rice. J. Plant Nutr. 2021, 44, 2514–2527. [Google Scholar] [CrossRef]
  160. Li, J.; Zhang, Z.; Chong, K.; Xu, Y. Chilling tolerance in rice: Past and present. J. Plant Physiol. 2022, 268, 153576. [Google Scholar] [CrossRef]
  161. Bhattacharya, A. Effect of Low-Temperature Stress on Germination, Growth, and Phenology of Plants: A Review. In Physiological Processes in Plants Under Low Temperature Stress; Springer: Singapore, 2022; pp. 1–106. [Google Scholar] [CrossRef]
  162. Hsu, C.H.; Hsu, Y.T. Biochemical Responses of Rice Roots to Cold Stress. Bot. Stud. 2019, 60, 14. [Google Scholar] [CrossRef]
  163. Reddy, K.R.; Seghal, A.; Jumaa, S.; Bheemanahalli, R.; Kakar, N.; Redoña, E.D.; Wijewardana, C.; Alsajri, F.A.; Chastain, D.; Gao, W.; et al. Morpho-Physiological Characterization of Diverse Rice Genotypes for Seedling Stage High- and Low-Temperature Tolerance. Agronomy 2021, 11, 112. [Google Scholar] [CrossRef]
  164. Freitas, G.M.; Thomas, J.; Liyanage, R.; Lay, J.O.; Basu, S.; Ramegowda, V.; Amaral, M.N.; Benitez, L.C.; Bolacel Braga, E.J.; Pereira, A.; et al. Cold tolerance response mechanisms revealed through comparative analysis of gene and protein expression in multiple rice genotypes. PLoS ONE 2019, 14, e0218019. [Google Scholar] [CrossRef]
  165. Baruah, A.R.; Ishigo-Oka, N.; Adachi, M.; Oguma, Y.; Tokizono, Y.; Onishi, K.; Sano, Y. Cold tolerance at the early growth stage in wild and cultivated rice. Euphytica 2009, 165, 459–470. [Google Scholar] [CrossRef]
  166. González-Schain, N.; Roig-Villanova, I.; Kater, M.M. Early Cold Stress Responses in Post-Meiotic Anthers from Tolerant and Sensitive Rice Cultivars. Rice 2019, 12, 94. [Google Scholar] [CrossRef] [PubMed]
  167. Nurhasanah Ritonga, F.; Chen, S. Physiological and Molecular Mechanism Involved in Cold Stress Tolerance in Plants. Plants 2020, 9, 560. [Google Scholar] [CrossRef] [PubMed]
  168. Lu, X.; Song, S.; Xiao, Y.; Fan, F.; Zhou, Y.; Jia, G.; Tang, W.; Peng, J. Circadian Clock-Coordinated Response to Chilling Stress in Rice. Environ. Exp. Bot. 2021, 185, 104398. [Google Scholar] [CrossRef]
  169. Shimono, H.; Fujimura, S.; Nishimura, T.; Hasegawa, T. Nitrogen Uptake by Rice (Oryza sativa L.) Exposed to Low Water Temperatures at Different Growth Stages. J. Agron. Crop Sci. 2012, 198, 145–151. [Google Scholar] [CrossRef]
  170. Feng, H.; Yan, M.; Fan, X.; Li, B.; Shen, Q.; Miller, A.J.; Xu, G. Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J. Exp. Bot. 2011, 62, 2319–2332. [Google Scholar] [CrossRef] [PubMed]
  171. Lu, B.; Yuan, Y.; Zhang, C.; Ou, J.; Zhou, W.; Lin, Q. Modulation of key enzymes involved in ammonium assimilation and carbon metabolism by low temperature in rice (Oryza sativa L.) roots. Plant Sci. 2005, 169, 295–302. [Google Scholar] [CrossRef]
  172. Guy, C.L. Cold Acclimation and Freezing Stress Tolerance: Role of Protein Metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1990, 41, 187–223. [Google Scholar] [CrossRef]
  173. Thomashow, M.F. Plant Cold Acclimation: Freezing Tolerance Genes and Regulatory Mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 571–599. [Google Scholar] [CrossRef]
  174. Janmohammadi, M.; Zolla, L.; Rinalducci, S. Low temperature tolerance in plants: Changes at the protein level. Phytochemistry 2015, 117, 76–89. [Google Scholar] [CrossRef] [PubMed]
  175. Dikilitas, M.; Karakas, S.; Simsek, E.; Yadav, A.N. Microbes from cold deserts and their applications in mitigation of cold stress in plants. In Microbiomes of Extreme Environments; CRC Press: Boca Raton, FL, USA, 2021; pp. 126–152. ISBN 9780429328633. [Google Scholar]
  176. Steponkus, P.L.; Uemura, M.; Joseph, R.A.; Gilmour, S.J.; Thomashow, M.F. Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 1998, 95, 14570–14575. [Google Scholar] [CrossRef] [PubMed]
  177. Kaplan, F.; Kopka, J.; Sung, D.Y.; Zhao, W.; Popp, M.; Porat, R.; Guy, C.L. Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J. 2007, 50, 967–981. [Google Scholar] [CrossRef] [PubMed]
  178. Ruelland, E.; Vaultier, M.-N.N.; Zachowski, A.; Hurry, V. Chapter 2 Cold Signalling and Cold Acclimation in Plants. In Advances in Botanical Research; Elsevier: Amsterdam, The Netherlands, 2009; Volume 49, pp. 35–150. [Google Scholar]
  179. Yu, X.; Peng, Y.H.; Zhang, M.H.; Shao, Y.J.; Su, W.A.; Tang, Z.C. Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res. 2006, 16, 599–608. [Google Scholar] [CrossRef] [PubMed]
  180. Ahamed, A.; Murai-Hatano, M.; Ishikawa-Sakurai, J.; Hayashi, H.; Kawamura, Y.; Uemura, M. Cold Stress-Induced Acclimation in Rice is Mediated by Root-Specific Aquaporins. Plant Cell Physiol. 2012, 53, 1445–1456. [Google Scholar] [CrossRef] [PubMed]
  181. Maurel, C.; Boursiac, Y.; Luu, D.-T.; Santoni, V.; Shahzad, Z.; Verdoucq, L. Aquaporins in Plants. Physiol. Rev. 2015, 95, 1321–1358. [Google Scholar] [CrossRef] [PubMed]
  182. Maurel, C.; Javot, H.; Lauvergeat, V.; Gerbeau, P.; Tournaire, C.; Santoni, V.; Heyes, J. Molecular physiology of aquaporins in plants. In International Review of Cytology; Elsevier: Amsterdam, The Netherlands, 2002; Volume 215, pp. 105–148. [Google Scholar] [CrossRef]
  183. Javot, H.; Lauvergeat, V.; Santoni, V.; Martin-Laurent, F.; Güçlü, J.; Vinh, J.; Heyes, J.; Franck, K.I.; Schäffner, A.R.; Bouchez, D.; et al. Role of a Single Aquaporin Isoform in Root Water Uptake. Plant Cell 2003, 15, 509–522. [Google Scholar] [CrossRef]
  184. Postaire, O.; Tournaire-Roux, C.; Grondin, A.; Boursiac, Y.; Morillon, R.; Schäffner, A.R.; Maurel, C. A PIP1 Aquaporin Contributes to Hydrostatic Pressure-Induced Water Transport in Both the Root and Rosette of Arabidopsis. Plant Physiol. 2010, 152, 1418–1430. [Google Scholar] [CrossRef]
  185. Murai-Hatano, M.; Kuwagata, T.; Sakurai, J.; Nonami, H.; Ahamed, A.; Nagasuga, K.; Matsunami, T.; Fukushi, K.; Maeshima, M.; Okada, M. Effect of Low Root Temperature on Hydraulic Conductivity of Rice Plants and the Possible Role of Aquaporins. Plant Cell Physiol. 2008, 49, 1294–1305. [Google Scholar] [CrossRef]
  186. Aroca, R.; Amodeo, G.; Fernández-Illescas, S.; Herman, E.M.; Chaumont, F.; Chrispeels, M.J. The Role of Aquaporins and Membrane Damage in Chilling and Hydrogen Peroxide Induced Changes in the Hydraulic Conductance of Maize Roots. Plant Physiol. 2005, 137, 341–353. [Google Scholar] [CrossRef]
  187. Sakurai, J.; Ishikawa, F.; Yamaguchi, T.; Uemura, M.; Maeshima, M. Identification of 33 Rice Aquaporin Genes and Analysis of Their Expression and Function. Plant Cell Physiol. 2005, 46, 1568–1577. [Google Scholar] [CrossRef] [PubMed]
  188. Bhattacharjee, S. Heat and chilling induced disruption of redox homeostasis and its regulation by hydrogen peroxide in germinating rice seeds (Oryza sativa L., Cultivar Ratna). Physiol. Mol. Biol. Plants 2013, 19, 199–207. [Google Scholar] [CrossRef] [PubMed]
  189. Hung, K.T.; Cheng, D.G.; Hsu, Y.T.; Kao, C.H. Abscisic acid-induced hydrogen peroxide is required for anthocyanin accumulation in leaves of rice seedlings. J. Plant Physiol. 2008, 165, 1280–1287. [Google Scholar] [CrossRef] [PubMed]
  190. Seifi, H.S.; Van Bockhaven, J.; Angenon, G.; Höfte, M. Glutamate Metabolism in Plant Disease and Defense: Friend or Foe? Mol. Plant-Microbe Interact. 2013, 26, 475–485. [Google Scholar] [CrossRef] [PubMed]
  191. Kavi Kishor, P.B.; Sreenivasulu, N. Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant. Cell Environ. 2014, 37, 300–311. [Google Scholar] [CrossRef] [PubMed]
  192. Raza, A.; Charagh, S.; Abbas, S.; Hassan, M.U.; Saeed, F.; Haider, S.; Sharif, R.; Anand, A.; Corpas, F.J.; Jin, W.; et al. Assessment of proline function in higher plants under extreme temperatures. Plant Biol. 2023, 25, 379–395. [Google Scholar] [CrossRef] [PubMed]
  193. da Cruz, R.P.; Sperotto, R.A.; Cargnelutti, D.; Adamski, J.M.; FreitasTerra, T.; Fett, J.P. Avoiding damage and achieving cold tolerance in rice plants. Food Energy Secur. 2013, 2, 96–119. [Google Scholar] [CrossRef]
  194. Zhang, Q.; Chen, Q.; Wang, S.; Hong, Y.; Wang, Z. Rice and cold stress: Methods for its evaluation and summary of cold tolerance-related quantitative trait loci. Rice 2014, 7, 24. [Google Scholar] [CrossRef]
  195. Ma, Y.; Dai, X.; Xu, Y.; Luo, W.; Zheng, X.; Zeng, D.; Pan, Y.; Lin, X.; Liu, H.; Zhang, D.; et al. COLD1 Confers Chilling Tolerance in Rice. Cell 2015, 160, 1209–1221. [Google Scholar] [CrossRef]
  196. Deng, X.; Hu, W.; Wei, S.; Zhou, S.; Zhang, F.; Han, J.; Chen, L.; Li, Y.; Feng, J.; Fang, B.; et al. TaCIPK29, a CBL-Interacting Protein Kinase Gene from Wheat, Confers Salt Stress Tolerance in Transgenic Tobacco. PLoS ONE 2013, 8, e69881. [Google Scholar] [CrossRef]
  197. Tian, X.; Wang, Z.; Li, X.; Lv, T.; Liu, H.; Wang, L.; Niu, H.; Bu, Q. Characterization and Functional Analysis of Pyrabactin Resistance-Like Abscisic Acid Receptor Family in Rice. Rice 2015, 8, 28. [Google Scholar] [CrossRef] [PubMed]
  198. Zhu, J.-K. Abiotic Stress Signaling and Responses in Plants. Cell 2016, 167, 313–324. [Google Scholar] [CrossRef] [PubMed]
  199. Zhang, Z.; Li, J.; Li, F.; Liu, H.; Yang, W.; Chong, K.; Xu, Y. OsMAPK3 Phosphorylates OsbHLH002/OsICE1 and Inhibits Its Ubiquitination to Activate OsTPP1 and Enhances Rice Chilling Tolerance. Dev. Cell 2017, 43, 731–743.e5. [Google Scholar] [CrossRef] [PubMed]
  200. Zhao, J.; Wang, S.; Qin, J.; Sun, C.; Liu, F. The lipid transfer protein OsLTPL159 is involved in cold tolerance at the early seedling stage in rice. Plant Biotechnol. J. 2020, 18, 756–769. [Google Scholar] [CrossRef] [PubMed]
  201. Sun, J.; Yang, L.; Wang, J.; Liu, H.; Zheng, H.; Xie, D.; Zhang, M.; Feng, M.; Jia, Y.; Zhao, H.; et al. Identification of a Cold-Tolerant Locus in Rice (Oryza Sativa L.) Using Bulked Segregant Analysis with a next-Generation Sequencing Strategy. Rice 2018, 11, 24. [Google Scholar] [CrossRef] [PubMed]
  202. Liu, K.; Wang, L.; Xu, Y.; Chen, N.; Ma, Q.; Li, F.; Chong, K. Overexpression of OsCOIN, a Putative Cold Inducible Zinc Finger Protein, Increased Tolerance to Chilling, Salt and Drought, and Enhanced Proline Level in Rice. Planta 2007, 226, 1007–1016. [Google Scholar] [CrossRef] [PubMed]
  203. Yang, C.; Li, D.; Mao, D.; Liu, X.; Ji, C.; Li, X.; Zhao, X.; Cheng, Z.; Chen, C.; Zhu, L. Overexpression of MicroRNA319 Impacts Leaf Morphogenesis and Leads to Enhanced Cold Tolerance in Rice (Oryza Sativa L.). Plant Cell Environ. 2013, 36, 2207–2218. [Google Scholar] [CrossRef] [PubMed]
  204. Greco, M.; Chiappetta, A.; Bruno, L.; Bitonti, M.B. In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning. J. Exp. Bot. 2012, 63, 695–709. [Google Scholar] [CrossRef]
  205. Ma, Q.; Dai, X.; Xu, Y.; Guo, J.; Liu, Y.; Chen, N.; Xiao, J.; Zhang, D.; Xu, Z.; Zhang, X.; et al. Enhanced Tolerance to Chilling Stress in OsMYB3R-2 Transgenic Rice Is Mediated by Alteration in Cell Cycle and Ectopic Expression of Stress Genes. Plant Physiol. 2009, 150, 244–256. [Google Scholar] [CrossRef]
  206. Hu, H.; You, J.; Fang, Y.; Zhu, X.; Qi, Z.; Xiong, L. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol. Biol. 2008, 67, 169–181. [Google Scholar] [CrossRef]
  207. Wang, Q.; Guan, Y.; Wu, Y.; Chen, H.; Chen, F.; Chu, C. Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol. Biol. 2008, 67, 589–602. [Google Scholar] [CrossRef]
  208. Joo, J.; Lee, Y.H.; Kim, Y.K.; Nahm, B.H.; Song, S.I. Abiotic stress responsive rice ASR1 and ASR3 exhibit different tissue-dependent sugar and hormone-sensitivities. Mol. Cells 2013, 35, 421–435. [Google Scholar] [CrossRef]
  209. Shi, J.; Cao, Y.; Fan, X.; Li, M.; Wang, Y.; Ming, F. A rice microsomal delta-12 fatty acid desaturase can enhance resistance to cold stress in yeast and Oryza sativa. Mol. Breed. 2012, 29, 743–757. [Google Scholar] [CrossRef]
  210. Kim, S.H.; Kim, J.Y.; Kim, S.J.; An, K.S.; An, G.; Kim, S.R. Isolation of Cold Stress-Responsive Genes in the Reproductive Organs, and Characterization of the OsLti6b Gene from Rice (Oryza Sativa L.). Plant Cell Rep. 2007, 26, 1097–1110. [Google Scholar] [CrossRef] [PubMed]
  211. Tao, Z.; Kou, Y.; Liu, H.; Li, X.; Xiao, J.; Wang, S. OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J. Exp. Bot. 2011, 62, 4863–4874. [Google Scholar] [CrossRef] [PubMed]
  212. Chen, N.; Xu, Y.; Wang, X.; Du, C.; Du, J.; Yuan, M.; Xu, Z.; Chong, K. OsRAN2, essential for mitosis, enhances cold tolerance in rice by promoting export of intranuclear tubulin and maintaining cell division under cold stress. Plant Cell Environ. 2011, 34, 52–64. [Google Scholar] [CrossRef] [PubMed]
  213. Wang, C.; Wei, Q.; Zhang, K.; Wang, L.; Liu, F.; Zhao, L.; Tan, Y.; Di, C.; Yan, H.; Yu, J.; et al. Down-Regulation of OsSPX1 Causes High Sensitivity to Cold and Oxidative Stresses in Rice Seedlings. PLoS ONE 2013, 8, 81849. [Google Scholar] [CrossRef] [PubMed]
  214. Park, H.Y.; Kang, I.S.; Han, J.S.; Lee, C.H.; An, G.; Moon, Y.H. OsDEG10 encoding a small RNA-binding protein is involved in abiotic stress signaling. Biochem. Biophys. Res. Commun. 2009, 380, 597–602. [Google Scholar] [CrossRef] [PubMed]
  215. Yamori, W.; Sakata, N.; Suzuki, Y.; Shikanai, T.; Makino, A. Cyclic Electron Flow around Photosystem i via Chloroplast NAD(P)H Dehydrogenase (NDH) Complex Performs a Significant Physiological Role during Photosynthesis and Plant Growth at Low Temperature in Rice. Plant J. 2011, 68, 966–976. [Google Scholar] [CrossRef] [PubMed]
  216. Li, G.-W.G.-W.; Zhang, M.-H.M.-H.; Cai, W.-M.W.-M.; Sun, W.-N.W.-N.; Su, W.-A.W.-A. Characterization of OsPIP2: 7, a Water Channel Protein in Rice. Plant Cell Physiol. 2008, 49, 1851–1858. [Google Scholar] [CrossRef]
  217. Gothandam, K.M.; Nalini, E.; Karthikeyan, S.; Shin, J.S. OsPRP3, a flower specific Proline-rich protein of rice, determines extracellular matrix structure of floral organs and its overexpression confers cold-tolerance. Plant Mol. Biol. 2010, 72, 125–135. [Google Scholar] [CrossRef]
  218. Kim, S.-J.; Lee, S.-C.; Hong, S.K.; An, K.; An, G.; Kim, S.-R. Ectopic expression of a cold-responsive OsAsr1 cDNA gives enhanced cold tolerance in transgenic rice plants. Mol. Cells 2009, 27, 449–458. [Google Scholar] [CrossRef] [PubMed]
  219. Su, C.-F.; Wang, Y.-C.; Hsieh, T.-H.; Lu, C.-A.; Tseng, T.-H.; Yu, S.-M. A Novel MYBS3-Dependent Pathway Confers Cold Tolerance in Rice. Plant Physiol. 2010, 153, 145–158. [Google Scholar] [CrossRef] [PubMed]
  220. Zhang, J.; Li, J.; Wang, X.; Chen, J. OVP1, a Vacuolar H+-translocating inorganic pyrophosphatase (V-PPase), overexpression improved rice cold tolerance. Plant Physiol. Biochem. 2011, 49, 33–38. [Google Scholar] [CrossRef] [PubMed]
  221. Song, Y.; Jiang, M.; Zhang, H.; Li, R. Zinc Oxide Nanoparticles Alleviate Chilling Stress in Rice (Oryza Sativa L.) by Regulating Antioxidative System and Chilling Response Transcription Factors. Molecules 2021, 26, 2196. [Google Scholar] [CrossRef] [PubMed]
  222. Han, Q.H.; Huang, B.; Ding, C.B.; Zhang, Z.W.; Chen, Y.E.; Hu, C.; Zhou, L.J.; Huang, Y.; Liao, J.Q.; Yuan, S.; et al. Effects of Melatonin on Anti-Oxidative Systems and Photosystem II in Cold-Stressed Rice Seedlings. Front. Plant Sci. 2017, 8, 785. [Google Scholar] [CrossRef] [PubMed]
  223. Teixeira, S.B.; Pires, S.N.; Ávila, G.E.; Silva, B.E.P.; Schmitz, V.N.; Deuner, C.; Silva Armesto, R.; Silva Moura, D.; Deuner, S.; da Silva Armesto, R.; et al. Application of Vigor Indexes to Evaluate the Cold Tolerance in Rice Seeds Germination Conditioned in Plant Extract. Sci. Rep. 2021, 11, 11038. [Google Scholar] [CrossRef]
  224. Bui, L.T.; Ella, E.S.; Dionisio-Sese, M.L.; Ismail, A.M. Morpho-Physiological Changes in Roots of Rice Seedling upon Submergence. Rice Sci. 2019, 26, 167–177. [Google Scholar] [CrossRef]
  225. Kumar, A.; Nayak, A.K.; Hanjagi, P.S.; Kumari, K.S.V.; Mohanty, S.; Tripathi, R.; Panneerselvam, P. Submergence stress in rice: Adaptive mechanisms, coping strategies and future research needs. Environ. Exp. Bot. 2021, 186, 104448. [Google Scholar] [CrossRef]
  226. Nishiuchi, S.; Yamauchi, T.; Takahashi, H.; Kotula, L.; Nakazono, M. Mechanisms for coping with submergence and waterlogging in rice. Rice 2012, 5, 2. [Google Scholar] [CrossRef]
  227. Kato, Y.; Collard, B.C.Y.; Septiningsih, E.M.; Ismail, A.M. Increasing flooding tolerance in rice: Combining tolerance of submergence and of stagnant flooding. Ann. Bot. 2019, 124, 1199–1209. [Google Scholar] [CrossRef] [PubMed]
  228. Ismail, A.M.; Ella, E.S.; Vergara, G.V.; Mackill, D.J. Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann. Bot. 2009, 103, 197–209. [Google Scholar] [CrossRef] [PubMed]
  229. Jackson, M.B. Physiological and Molecular Basis of Susceptibility and Tolerance of Rice Plants to Complete Submergence. Ann. Bot. 2003, 91, 227–241. [Google Scholar] [CrossRef] [PubMed]
  230. Sarkar, R.K.; Bhattacharjee, B. Rice Genotypes with SUB1 QTL Differ in Submergence Tolerance, Elongation Ability during Submergence and Re-generation Growth at Re-emergence. Rice 2011, 5, 7. [Google Scholar] [CrossRef]
  231. Colmer, T.D.; Armstrong, W.; Greenway, H.; Ismail, A.M.; Kirk, G.J.D.; Atwell, B.J. Physiological Mechanisms of Flooding Tolerance in Rice: Transient Complete Submergence and Prolonged Standing Water. In Progress in Botany; Springer: Berlin/Heidelberg, Germany, 2014; Volume 75, pp. 255–307. [Google Scholar] [CrossRef]
  232. Singh, H.P.; Singh, B.B.; Ram, P.C. Submergence tolerance of rainfed lowland rice: Search for physiological marker traits. J. Plant Physiol. 2001, 158, 883–889. [Google Scholar] [CrossRef]
  233. Setter, T.L.; Ingram, K.T.; Tuong, T.P. Environmental characterization requirements for strategic research in rice grown under adverse conditions of drought, flooding and salinity. Int. Rice Res. Inst. 1995, 3–18. [Google Scholar]
  234. Bailey-Serres, J.; Fukao, T.; Ronald, P.; Ismail, A.; Heuer, S.; Mackill, D. Submergence Tolerant Rice: SUB1’s Journey from Landrace to Modern Cultivar. Rice 2010, 3, 138–147. [Google Scholar] [CrossRef]
  235. Sarkar, R.K.; Panda, D. Distinction and characterisation of submergence tolerant and sensitive rice cultivars, probed by the fluorescence OJIP rise kinetics. Funct. Plant Biol. 2009, 36, 222. [Google Scholar] [CrossRef]
  236. Emes, M.J.; Wilkins, C.P.; Smith, P.A.; Kupkanchanakul, K.; Hawker, K.; Charlton, W.A.; Cutter, E.G. Starch utilization by deepwater rices during submergence. Int. Deep. Rice Work. 1988, 26–30. [Google Scholar]
  237. Fukao, T.; Yeung, E.; Bailey-Serres, J. The Submergence Tolerance Regulator SUB1A Mediates Crosstalk between Submergence and Drought Tolerance in Rice. Plant Cell 2011, 23, 412–427. [Google Scholar] [CrossRef]
  238. Setter, T.L.; Bhekasut, P.; Greenway, H. Desiccation of leaves after de-submergence is one cause for intolerance to complete submergence of the rice cultivar IR 42. Funct. Plant Biol. 2010, 37, 1096. [Google Scholar] [CrossRef]
  239. Upadhyay, R.; Panda, S.; Dutta, B. Growth, Chlorophyll and Electric Conductivity responses of rice cultivars to different levels of Submergence and Post-submergence Stress. J. Phytol. 2009, 1, 425–432. [Google Scholar]
  240. Upadhyay, R.K. Oxidative Injury and Its Detoxification in Rice Plants after Submergence Stress. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 2018, 88, 15–21. [Google Scholar] [CrossRef]
  241. Ribeiro, C.W.; Korbes, A.P.; Garighan, J.A.; Jardim-Messeder, D.; Carvalho, F.E.L.L.; Sousa, R.H.V.V.; Caverzan, A.; Teixeira, F.K.; Silveira, J.A.G.G.; Margis-Pinheiro, M. Rice Peroxisomal Ascorbate Peroxidase Knockdown Affects ROS Signaling and Triggers Early Leaf Senescence. Plant Sci. 2017, 263, 55–65. [Google Scholar] [CrossRef] [PubMed]
  242. Bailey-Serres, J.; Voesenek, L. Flooding Stress: Acclimations and Genetic Diversity. Annu. Rev. Plant Biol. 2008, 59, 313–339. [Google Scholar] [CrossRef] [PubMed]
  243. Colmer, T.D.; Voesenek, L.A.C.J. Flooding tolerance: Suites of plant traits in variable environments. Funct. Plant Biol. 2009, 36, 665. [Google Scholar] [CrossRef] [PubMed]
  244. Drew, M.C.; He, C.-J.; Morgan, P.W. Programmed cell death and aerenchyma formation in roots. Trends Plant Sci. 2000, 5, 123–127. [Google Scholar] [CrossRef]
  245. Shiono, K.; Takahashi, H.; Colmer, T.D.; Nakazono, M. Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Sci. 2008, 175, 52–58. [Google Scholar] [CrossRef]
  246. Steffens, B.; Sauter, M. Epidermal Cell Death in Rice Is Confined to Cells with a Distinct Molecular Identity and Is Mediated by Ethylene and H2O2 through an Autoamplified Signal Pathway. Plant Cell 2009, 21, 184–196. [Google Scholar] [CrossRef]
  247. Hattori, Y.; Hattori, Y.; Nagai, K.; Nagai, K.; Furukawa, S.; Furukawa, S.; Song, X.-J.X.-J.; Song, X.-J.X.-J.; Kawano, R.; Kawano, R.; et al. The Ethylene Response Factors SNORKEL1 and SNORKEL2 Allow Rice to Adapt to Deep Water. Nature 2009, 460, 1026. [Google Scholar] [CrossRef]
  248. Colmer, T.D.; Pedersen, O. Oxygen dynamics in submerged rice (Oryza sativa). New Phytol. 2008, 178, 326–334. [Google Scholar] [CrossRef]
  249. Xu, K.; Xu, X.; Fukao, T.; Canlas, P.; Maghirang-Rodriguez, R.; Heuer, S.; Ismail, A.M.; Bailey-Serres, J.; Ronald, P.C.; Mackill, D.J. Sub1A Is an Ethylene-Response-Factor-like Gene That Confers Submergence Tolerance to Rice. Nature 2006, 442, 705–708. [Google Scholar] [CrossRef] [PubMed]
  250. Fukao, T.; Xu, K.; Ronald, P.; Bailey-Serres, J. A Variable Cluster of Ethylene Response Factor-like Genes Regulates Metabolic and Developmental Acclimation Responses to Submergence in Rice. Plant Cell 2006, 18, 2021–2034. [Google Scholar] [CrossRef] [PubMed]
  251. Fukao, T.; Bailey-Serres, J. Ethylene—A key regulator of submergence responses in rice. Plant Sci. 2008, 175, 43–51. [Google Scholar] [CrossRef]
  252. Jackson, M.; Armstrong, W. Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence. Plant Biol. 1999, 1, 274–287. [Google Scholar] [CrossRef]
  253. COLMER, T.D. Aerenchyma and an Inducible Barrier to Radial Oxygen Loss Facilitate Root Aeration in Upland, Paddy and Deep-water Rice (Oryza sativa L.). Ann. Bot. 2003, 91, 301–309. [Google Scholar] [CrossRef] [PubMed]
  254. Kuroha, T.; Nagai, K.; Gamuyao, R.; Wang, D.R.; Furuta, T.; Nakamori, M.; Kitaoka, T.; Adachi, K.; Minami, A.; Mori, Y.; et al. Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Science 2018, 361, 181–186. [Google Scholar] [CrossRef] [PubMed]
  255. Nagai, K.; Mori, Y.; Ishikawa, S.; Furuta, T.; Gamuyao, R.; Niimi, Y.; Hobo, T.; Fukuda, M.; Kojima, M.; Takebayashi, Y.; et al. Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature 2020, 584, 109–114. [Google Scholar] [CrossRef]
  256. Reynoso, M.A.; Kajala, K.; Bajic, M.; West, D.A.; Pauluzzi, G.; Yao, A.I.; Hatch, K.; Zumstein, K.; Woodhouse, M.; Rodriguez-Medina, J.; et al. Evolutionary flexibility in flooding response circuitry in angiosperms. Science 2019, 365, 1291–1295. [Google Scholar] [CrossRef]
  257. Straeten, D.; Zhou, Z.; Prinsen, E.; Onckelen, H.A.; Montagu, M.C.; Van Der Straeten, D.; Zhou, Z.; Prinsen, E.; Van Onckelen, H.A.; Van Montagu, M.C. A Comparative Molecular-Physiological Study of Submergence Response in Lowland and Deepwater Rice. Plant Physiol. 2001, 125, 955–968. [Google Scholar] [CrossRef]
  258. Zarembinski, T.I.; Theologis, A. Expression characteristics of OS-ACS1 and OSACS2, two members of the 1-aminocyclopropane-1-carboxylate synthase gene family in rice (Oryza sativa L. Cv. Habiganj Aman II) during partial submergence. Plant Mol. Biol 1997, 33, 71–77. [Google Scholar] [CrossRef] [PubMed]
  259. Kurokawa, Y.; Nagai, K.; Huan, P.D.; Shimazaki, K.; Qu, H.; Mori, Y.; Toda, Y.; Kuroha, T.; Hayashi, N.; Aiga, S.; et al. Rice leaf hydrophobicity and gas films are conferred by a wax synthesis gene (LGF 1) and contribute to flood tolerance. New Phytol. 2018, 218, 1558–1569. [Google Scholar] [CrossRef] [PubMed]
  260. Kretzschmar, T.; Pelayo, M.A.F.; Trijatmiko, K.R.; Gabunada, L.F.M.; Alam, R.; Jimenez, R.; Mendioro, M.S.; Slamet-Loedin, I.H.; Sreenivasulu, N.; Bailey-Serres, J.; et al. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat. Plants 2015, 1, 15124. [Google Scholar] [CrossRef] [PubMed]
  261. Panda, D.; Sarkar, R.K. Mechanism associated with nonstructural carbohydrate accumulation in submergence tolerant rice (Oryza sativa L.) cultivars. J. Plant Interact. 2014, 9, 62–68. [Google Scholar] [CrossRef]
  262. Jisha, V.; Dampanaboina, L.; Vadassery, J.; Mithöfer, A.; Kappara, S.; Ramanan, R. Overexpression of an AP2/ERF Type Transcription Factor OsEREBP1 Confers Biotic and Abiotic Stress Tolerance in Rice. PLoS ONE 2015, 10, e0127831. [Google Scholar] [CrossRef]
  263. Lee, K.-W.; Chen, P.-W.; Lu, C.-A.; Chen, S.; Ho, T.-H.D.; Yu, S.-M. Coordinated Responses to Oxygen and Sugar Deficiency Allow Rice Seedlings to Tolerate Flooding. Sci. Signal. 2009, 2, 61. [Google Scholar] [CrossRef] [PubMed]
  264. Nagai, K.; Kurokawa, Y.; Mori, Y.; Minami, A.; Reuscher, S.; Wu, J.; Matsumoto, T.; Ashikari, M. SNORKEL Genes Relating to Flood Tolerance Were Pseudogenized in Normal Cultivated Rice. Plants 2022, 11, 376. [Google Scholar] [CrossRef]
  265. Nemoto, K.; Ukai, Y.; Tang, D.-Q.; Kasai, Y.; Morita, M. Inheritance of early elongation ability in floating rice revealed by diallel and QTL analyses. Theor. Appl. Genet. 2004, 109, 42–47. [Google Scholar] [CrossRef]
  266. Tang, D.-Q.; Kasai, Y.; Miyamoto, N.; Ukai, Y.; Nemoto, K. Comparison of QTLs for Early Elongation Ability between Two Floating Rice Cultivars with a Different Phylogenetic Origin. Breed. Sci. 2005, 55, 1–5. [Google Scholar] [CrossRef]
  267. Hattori, Y.; Miura, K.; Asano, K.; Yamamoto, E.; Mori, H.; Kitano, H.; Matsuoka, M.; Ashikari, M. A Major QTL Confers Rapid Internode Elongation in Response to Water Rise in Deepwater Rice. Breed. Sci. 2007, 57, 305–314. [Google Scholar] [CrossRef]
  268. Kawano, R.; Doi, K.; Yasui, H.; Mochizuki, T.; Yoshimura, A. Mapping of QTLs for floating ability in rice. Breed. Sci. 2008, 58, 47–53. [Google Scholar] [CrossRef]
  269. Septiningsih, E.M.; Pamplona, A.M.; Sanchez, D.L.; Neeraja, C.N.; Vergara, G.V.; Heuer, S.; Ismail, A.M.; Mackill, D.J. Development of submergence-tolerant rice cultivars: The Sub1 locus and beyond. Ann. Bot. 2009, 103, 151–160. [Google Scholar] [CrossRef] [PubMed]
  270. Fukao, T.; Yeung, E.; Bailey-Serres, J. The Submergence Tolerance Gene SUB1A Delays Leaf Senescence under Prolonged Darkness through Hormonal Regulation in Rice. Plant Physiol. 2012, 160, 1795–1807. [Google Scholar] [CrossRef] [PubMed]
  271. Debona, D.; Rodrigues, F.A.; Datnoff, L.E. Silicon’s Role in Abiotic and Biotic Plant Stresses. Annu. Rev. Phytopathol. 2017, 55, 85–107. [Google Scholar] [CrossRef] [PubMed]
  272. Pan, T.; Zhang, J.; He, L.; Hafeez, A.; Ning, C.; Cai, K. Silicon Enhances Plant Resistance of Rice against Submergence Stress. Plants 2021, 10, 767. [Google Scholar] [CrossRef] [PubMed]
  273. Guo, P.; Du, H.; Wang, D.; Ma, M. Effects of Mercury Stress on Methylmercury Production in Rice Rhizosphere, Methylmercury Uptake in Rice and Physiological Changes of Leaves. Sci. Total Environ. 2021, 765, 142682. [Google Scholar] [CrossRef] [PubMed]
  274. Lutts, S.; Kinet, J.M.; Bouharmont, J. Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J. Exp. Bot. 1995, 46, 1843–1852. [Google Scholar] [CrossRef]
  275. Bundó, M.; Martín-Cardoso, H.; Pesenti, M.; Gómez-Ariza, J.; Castillo, L.; Frouin, J.; Serrat, X.; Nogués, S.; Courtois, B.; Grenier, C.; et al. Integrative Approach for Precise Genotyping and Transcriptomics of Salt Tolerant Introgression Rice Lines. Front. Plant Sci. 2022, 12, 797141. [Google Scholar] [CrossRef]
  276. Rodríguez-Navarro, A.; Rubio, F. High-affinity potassium and sodium transport systems in plants. J. Exp. Bot. 2006, 57, 1149–1160. [Google Scholar] [CrossRef]
  277. Ali, A.; Raddatz, N.; Pardo, J.M.; Yun, D. HKT sodium and potassium transporters in Arabidopsis thaliana and related halophyte species. Physiol. Plant. 2021, 171, 546–558. [Google Scholar] [CrossRef]
  278. Assaha, D.V.M.; Ueda, A.; Saneoka, H.; Al-Yahyai, R.; Yaish, M.W. The Role of Na(+) and K(+) Transporters in Salt Stress Adaptation in Glycophytes. Front. Physiol. 2017, 8, 509. [Google Scholar] [CrossRef]
  279. Khatun, S.; Rizzo, C.A.; Flowers, T.J. Genotypic variation in the effect of salinity on fertility in rice. Plant Soil 1995, 173, 239–250. [Google Scholar] [CrossRef]
  280. Rao, P.S.; Mishra, B.; Gupta, S.R. Effects of Soil Salinity and Alkalinity on Grain Quality of Tolerant, Semi-Tolerant and Sensitive Rice Genotypes. Rice Sci. 2013, 20, 284–291. [Google Scholar] [CrossRef]
  281. Zeng, Y.; Zhang, H.; Li, Z.; Shen, S.; Sun, J.; Wang, M.; Liao, D.; Liu, X.; Wang, X.; Xiao, F.; et al. Evaluation of Genetic Diversity of Rice Landraces (Oryza sativa L.) in Yunnan, China. Breed. Sci. 2007, 57, 91–99. [Google Scholar] [CrossRef]
  282. Yeo, A.R.; Yeo, M.E.; Flowers, S.A.; Flowers, T.J. Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theor. Appl. Genet. 1990, 79, 377–384. [Google Scholar] [CrossRef] [PubMed]
  283. Razzaq, A.; Ali, A.; Safdar, L.B.; Zafar, M.M.; Rui, Y.; Shakeel, A.; Shaukat, A.; Ashraf, M.; Gong, W.; Yuan, Y. Salt stress induces physiochemical alterations in rice grain composition and quality. J. Food Sci. 2020, 85, 14–20. [Google Scholar] [CrossRef] [PubMed]
  284. Munns, R.; Tester, M. Mechanisms of Salinity Tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef] [PubMed]
  285. Xiao, F.; Zhou, H. Plant salt response: Perception, signaling, and tolerance. Front. Plant Sci. 2023, 13, 1053699. [Google Scholar] [CrossRef] [PubMed]
  286. Hussain, S.; Zhang, J.; Hua, J.; Zhong, C.; Zhu, L.; Feng, L.F.; Cao, X.; Chuan, X.; Chuang, Y.S.; Miao, S.; et al. Effects of Salt Stress on Rice Growth, Development Characteristics, and the Regulating Ways: A Review. J. Integr. Agric. 2017, 16, 2357–2374. [Google Scholar] [CrossRef]
  287. Cha-Um, S.; Supaibulwattana, K.; Kirdmanee, C. Comparative Effects of Salt Stress and Extreme pH Stress Combined on Glycinebetaine Accumulation, Photosynthetic Abilities and Growth Characters of Two Rice Genotypes. Rice Sci. 2009, 16, 274–282. [Google Scholar] [CrossRef]
  288. Ran, X.; Wang, X.; Huang, X.; Ma, C.; Liang, H.; Liu, B. Study on the Relationship of Ions (Na, K, Ca) Absorption and Distribution to Photosynthetic Response of Salix matsudana Koidz Under Salt Stress. Front. Plant Sci. 2022, 13, 860111. [Google Scholar] [CrossRef] [PubMed]
  289. Hoang, T.M.L.; Tran, T.N.; Nguyen, T.K.T.; Williams, B.; Wurm, P.; Bellairs, S.; Mundree, S. Improvement of Salinity Stress Tolerance in Rice: Challenges and Opportunities. Agronomy 2016, 6, 54. [Google Scholar] [CrossRef]
  290. Vaidyanathan, H.; Sivakumar, P.; Chakrabarty, R.; Thomas, G. Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)—Differential response in salt-tolerant and sensitive varieties. Plant Sci. 2003, 165, 1411–1418. [Google Scholar] [CrossRef]
  291. Yamane, K.; Mitsuya, S.; Kawasaki, M.; Taniguchi, M.; Miyake, H. Antioxidant Capacity and Damages Caused by Salinity Stress in Apical and Basal Regions of Rice Leaf. Plant Prod. Sci. 2009, 12, 319–326. [Google Scholar] [CrossRef]
  292. Schmidt, R.; Schippers, J.H.M.; Mieulet, D.; Watanabe, M.; Hoefgen, R.; Guiderdoni, E.; Mueller-Roeber, B. SALT-RESPONSIVE ERF1 Is a Negative Regulator of Grain Filling and Gibberellin-Mediated Seedling Establishment in Rice. Mol. Plant 2014, 7, 404–421. [Google Scholar] [CrossRef] [PubMed]
  293. Rajendran, K.; Tester, M.; Roy, S.J. Quantifying the three main components of salinity tolerance in cereals. Plant. Cell Environ. 2009, 32, 237–249. [Google Scholar] [CrossRef] [PubMed]
  294. Moradi, F.; Ismail, A.M. Responses of Photosynthesis, Chlorophyll Fluorescence and ROS-Scavenging Systems to Salt Stress During Seedling and Reproductive Stages in Rice. Ann. Bot. 2007, 99, 1161–1173. [Google Scholar] [CrossRef]
  295. Maathuis, F. K + Nutrition and Na + Toxicity: The Basis of Cellular K+/Na+ Ratios. Ann. Bot. 1999, 84, 123–133. [Google Scholar] [CrossRef]
  296. Rodrigues, C.R.F.; Silva, E.N.; Ferreira-Silva, S.L.; Voigt, E.L.; Viégas, R.A.; Silveira, J.A.G. High K + supply avoids Na + toxicity and improves photosynthesis by allowing favorable K + : Na + ratios through the inhibition of Na + uptake and transport to the shoots of Jatropha curcas plants. J. Plant Nutr. Soil Sci. 2013, 176, 157–164. [Google Scholar] [CrossRef]
  297. Lee, K.-S.; Choi, W.-Y.; Ko, J.-C.; Kim, T.-S.; Gregorio, G.B. Salinity tolerance of japonica and indica rice (Oryza sativa L.) at the seedling stage. Planta 2003, 216, 1043–1046. [Google Scholar] [CrossRef]
  298. Ghosh, N.; Adak, M.K.; Ghosh, P.D.; Gupta, S.; Sen Gupta, D.N.; Mandal, C. Differential responses of two rice varieties to salt stress. Plant Biotechnol. Rep. 2011, 5, 89–103. [Google Scholar] [CrossRef]
  299. Kader, M.A.; Lindberg, S. Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI. J. Exp. Bot. 2005, 56, 3149–3158. [Google Scholar] [CrossRef] [PubMed]
  300. Johnson, M.K.; Johnson, E.J.; MacElroy, R.D.; Speer, H.L.; Bruff, B.S. Effects of Salts on the Halophilic Alga Dunaliella viridis. J. Bacteriol. 1968, 95, 1461–1468. [Google Scholar] [CrossRef] [PubMed]
  301. Yancey, P.H.; Clark, M.E.; Hand, S.C.; Bowlus, R.D.; Somero, G.N. Living with Water Stress: Evolution of Osmolyte Systems. Science 1982, 217, 1214–1222. [Google Scholar] [CrossRef] [PubMed]
  302. Garg, A.K.; Kim, J.; Owens, T.G.; Ranwala, A.P.; Choi, Y.D.; Kochian, L.V.; Wu, R.J. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. USA 2002, 99, 15898–15903. [Google Scholar] [CrossRef] [PubMed]
  303. Singh, P.; Choudhary, K.K.; Chaudhary, N.; Gupta, S.; Sahu, M.; Tejaswini, B.; Sarkar, S. Salt Stress Resilience in Plants Mediated through Osmolyte Accumulation and Its Crosstalk Mechanism with Phytohormones. Front. Plant Sci. 2022, 13, 1006617. [Google Scholar] [CrossRef] [PubMed]
  304. Greenberg, J.T. Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci. USA 1996, 93, 12094–12097. [Google Scholar] [CrossRef]
  305. Liu, S.-H.; Fu, B.-Y.; Xu, H.-X.; Zhu, L.-H.; Zhai, H.-Q.; Li, Z.-K. Cell death in response to osmotic and salt stresses in two rice (Oryza sativa L.) ecotypes. Plant Sci. 2007, 172, 897–902. [Google Scholar] [CrossRef]
  306. Li, J.; Jiang, A.; Zhang, W. Salt Stress-induced Programmed Cell Death in Rice Root Tip Cells. J. Integr. Plant Biol. 2007, 49, 481–486. [Google Scholar] [CrossRef]
  307. Khoso, M.A.; Hussain, A.; Ritonga, F.N.; Ali, Q.; Channa, M.M.; Alshegaihi, R.M.; Meng, Q.; Ali, M.; Zaman, W.; Brohi, R.D.; et al. WRKY transcription factors (TFs): Molecular switches to regulate drought, temperature, and salinity stresses in plants. Front. Plant Sci. 2022, 13, 1039329. [Google Scholar] [CrossRef]
  308. Gumi, A.M.; Guha, P.K.; Mazumder, A.; Jayaswal, P.; Mondal, T.K. Characterization of OglDREB2A gene from African rice (Oryza glaberrima), comparative analysis and its transcriptional regulation under salinity stress. Biotech 2018, 8, 91. [Google Scholar] [CrossRef]
  309. Liu, C.; Mao, B.; Ou, S.; Wang, W.; Liu, L.; Wu, Y.; Chu, C.; Wang, X. OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol. Biol. 2014, 84, 19–36. [Google Scholar] [CrossRef] [PubMed]
  310. Jan, A.; Maruyama, K.; Todaka, D.; Kidokoro, S.; Abo, M.; Yoshimura, E.; Shinozaki, K.; Nakashima, K.; Yamaguchi-Shinozaki, K. OsTZF1, a CCCH-Tandem Zinc Finger Protein, Confers Delayed Senescence and Stress Tolerance in Rice by Regulating Stress-Related Genes. Plant Physiol. 2013, 161, 1202–1216. [Google Scholar] [CrossRef] [PubMed]
  311. Qiu, D.; Xiao, J.; Xie, W.; Liu, H.; Li, X.; Xiong, L.; Wang, S. Rice Gene Network Inferred from Expression Profiling of Plants Overexpressing OsWRKY13, a Positive Regulator of Disease Resistance. Mol. Plant 2008, 1, 538–551. [Google Scholar] [CrossRef] [PubMed]
  312. Qiu, D.; Xiao, J.; Ding, X.; Xiong, M.; Cai, M.; Cao, Y.; Li, X.; Xu, C.; Wang, S. OsWRKY13 Mediates Rice Disease Resistance by Regulating Defense-Related Genes in Salicylate- and Jasmonate-Dependent Signaling. Mol. Plant-Microbe Interact. 2007, 20, 492–499. [Google Scholar] [CrossRef]
  313. Liu, C.; Chen, K.; Zhao, X.; Wang, X.; Shen, C.; Zhu, Y.; Dai, M.; Qiu, X.; Yang, R.; Xing, D.; et al. Identification of Genes for Salt Tolerance and Yield-Related Traits in Rice Plants Grown Hydroponically and under Saline Field Conditions by Genome-Wide Association Study. Rice 2019, 12, 88. [Google Scholar] [CrossRef]
  314. Wang, H.; Zhang, M.; Guo, R.; Shi, D.; Liu, B.; Lin, X.; Yang, C. Effects of salt stress on ion balance and nitrogen metabolism of old and young leaves in rice (Oryza sativa L.). BMC Plant Biol. 2012, 12, 194. [Google Scholar] [CrossRef]
  315. Chen, G.; Hu, Q.; Luo, L.; Yang, T.; Zhang, S.; Hu, Y.; Yu, L.; Xu, G. Rice Potassium Transporter OsHAK1 Is Essential for Maintaining Potassium-Mediated Growth and Functions in Salt Tolerance over Low and High Potassium Concentration Ranges. Plant Cell Environ. 2015, 38, 2747–2765. [Google Scholar] [CrossRef]
  316. Blumwald, E. Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol. 2000, 12, 431–434. [Google Scholar] [CrossRef]
  317. Bassil, E.; Coku, A.; Blumwald, E. Cellular ion homeostasis: Emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J. Exp. Bot. 2012, 63, 5727–5740. [Google Scholar] [CrossRef]
  318. Kurotani, K.I.; Hayashi, K.; Hatanaka, S.; Toda, Y.; Ogawa, D.; Ichikawa, H.; Ishimaru, Y.; Tashita, R.; Suzuki, T.; Ueda, M.; et al. Elevated Levels of CYP94 Family Gene Expression Alleviate the Jasmonate Response and Enhance Salt Tolerance in Rice. Plant Cell Physiol. 2015, 56, 779–789. [Google Scholar] [CrossRef]
  319. Asano, T.; Hayashi, N.; Kobayashi, M.; Aoki, N.; Miyao, A.; Mitsuhara, I.; Ichikawa, H.; Komatsu, S.; Hirochika, H.; Kikuchi, S.; et al. A Rice Calcium-Dependent Protein Kinase OsCPK12 Oppositely Modulates Salt-Stress Tolerance and Blast Disease Resistance. Plant J. 2012, 69, 26–36. [Google Scholar] [CrossRef]
  320. Guan, Q.; Ma, H.; Wang, Z.Z.; Wang, Z.Z.; Bu, Q.; Liu, S. A rice LSD1-like-type ZFP gene OsLOL5 enhances saline-alkaline tolerance in transgenic Arabidopsis thaliana, yeast and rice. BMC Genom. 2016, 17, 142. [Google Scholar] [CrossRef] [PubMed]
  321. Jeong, M.-J.; Lee, S.-K.; Kim, B.-G.; Kwon, T.-R.; Cho, W.-S.; Park, Y.-T.; Lee, J.-O.; Kwon, H.-B.; Byun, M.-O.; Park, S.-C. A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell. Tissue Organ Cult. 2006, 85, 151–160. [Google Scholar] [CrossRef]
  322. Gao, Q.; Yin, X.; Wang, F.; Hu, S.; Liu, W.; Chen, L.; Dai, X.; Liang, M. OsJRL40, a Jacalin-Related Lectin Gene, Promotes Salt Stress Tolerance in Rice. Int. J. Mol. Sci. 2023, 24, 7441. [Google Scholar] [CrossRef] [PubMed]
  323. Diédhiou, C.J.; Popova, O.V.; Dietz, K.-J.; Golldack, D. The SNF1-type serine-threonine protein kinase SAPK4regulates stress-responsive gene expression in rice. BMC Plant Biol. 2008, 8, 49. [Google Scholar] [CrossRef] [PubMed]
  324. Obata, T.; Kitamoto, H.K.; Nakamura, A.; Fukuda, A.; Tanaka, Y. Rice Shaker Potassium Channel OsKAT1 Confers Tolerance to Salinity Stress on Yeast and Rice Cells. Plant Physiol. 2007, 144, 1978–1985. [Google Scholar] [CrossRef] [PubMed]
  325. Vishal, B.; Krishnamurthy, P.; Ramamoorthy, R.; Kumar, P.P. OsTPS8 controls yield-related traits and confers salt stress tolerance in rice by enhancing suberin deposition. New Phytol. 2019, 221, 1369–1386. [Google Scholar] [CrossRef] [PubMed]
  326. Hasthanasombut, S.; Ntui, V.; Supaibulwatana, K.; Mii, M.; Nakamura, I. Expression of Indica rice OsBADH1 gene under salinity stress in transgenic tobacco. Plant Biotechnol. Rep. 2010, 4, 75–83. [Google Scholar] [CrossRef]
  327. Zhu, N.; Cheng, S.; Liu, X.; Du, H.; Dai, M.; Zhou, D.X.; Yang, W.; Zhao, Y. The R2R3-Type MYB Gene OsMYB91 Has a Function in Coordinating Plant Growth and Salt Stress Tolerance in Rice. Plant Sci. 2015, 236, 146–156. [Google Scholar] [CrossRef]
  328. Liu, S.; Zheng, L.; Xue, Y.; Zhang, Q.; Wang, L.; Shou, H. Overexpression of OsVP1 and OsNHX1 Increases Tolerance to Drought and Salinity in Rice. J. Plant Biol. 2010, 53, 444–452. [Google Scholar] [CrossRef]
  329. Ren, Z.H.; Gao, J.P.; Li, L.G.; Cai, X.L.; Huang, W.; Chao, D.Y.; Zhu, M.Z.; Wang, Z.Y.; Luan, S.; Lin, H.X. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 2005, 37, 1141–1146. [Google Scholar] [CrossRef] [PubMed]
  330. Suzuki, K.; Yamaji, N.; Costa, A.; Okuma, E.; Kobayashi, N.I.; Kashiwagi, T.; Katsuhara, M.; Wang, C.; Tanoi, K.; Murata, Y.; et al. OsHKT1: 4-Mediated Na+ Transport in Stems Contributes to Na+ Exclusion from Leaf Blades of Rice at the Reproductive Growth Stage upon Salt Stress. BMC Plant Biol. 2016, 16, 22. [Google Scholar] [CrossRef] [PubMed]
  331. Wang, R.; Jing, W.; Xiao, L.; Jin, Y.; Shen, L.; Zhang, W. The Rice High-Affinity Potassium Transporterl: L Is Involved in Salt Tolerance and Regulated by an MYB-Type Transcription Factor. Plant Physiol. 2015, 168, 1076–1090. [Google Scholar] [CrossRef] [PubMed]
  332. Horie, T.; Sugawara, M.; Okada, T.; Taira, K.; Kaothien-Nakayama, P.; Katsuhara, M.; Shinmyo, A.; Nakayama, H. Rice sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells. J. Biosci. Bioeng. 2011, 111, 346–356. [Google Scholar] [CrossRef] [PubMed]
  333. Tisarum, R.; Theerawitaya, C.; Samphumphuang, T.; Polispitak, K.; Thongpoem, P.; Singh, H.P.; Cha-um, S. Alleviation of Salt Stress in Upland Rice (Oryza sativa L. Ssp. Indica Cv. Leum Pua) Using Arbuscular Mycorrhizal Fungi Inoculation. Front. Plant Sci. 2020, 11, 348. [Google Scholar] [CrossRef] [PubMed]
  334. Jallad, K.N. Heavy metal exposure from ingesting rice and its related potential hazardous health risks to humans. Environ. Sci. Pollut. Res. 2015, 22, 15449–15458. [Google Scholar] [CrossRef] [PubMed]
  335. Wysocki, R.; Tamás, M.J. How Saccharomyces cerevisiae copes with toxic metals and metalloids. FEMS Microbiol. Rev. 2010, 34, 925–951. [Google Scholar] [CrossRef]
  336. Sharma, S.K.; Goloubinoff, P.; Christen, P. Non-native Proteins as Newly-Identified Targets of Heavy Metals and Metalloids. In Cellular Effects of Heavy Metals; Springer: Dordrecht, The Netherlands, 2011; pp. 263–274. [Google Scholar] [CrossRef]
  337. Hu, T.; Zhu, S.; Tan, L.; Qi, W.; He, S.; Wang, G. Overexpression of OsLEA4 enhances drought, high salt and heavy metal stress tolerance in transgenic rice (Oryza sativa L.). Environ. Exp. Bot. 2016, 123, 68–77. [Google Scholar] [CrossRef]
  338. Liang, J.; Zhou, M.; Zhou, X.; Jin, Y.; Xu, M.; Lin, J. JcLEA, a Novel LEA-Like Protein from Jatropha curcas, Confers a High Level of Tolerance to Dehydration and Salinity in Arabidopsis thaliana. PLoS ONE 2013, 8, e83056. [Google Scholar] [CrossRef]
  339. Mahajan, S.; Tuteja, N. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 2005, 444, 139–158. [Google Scholar] [CrossRef] [PubMed]
  340. Guillod-Magnin, R.; Brüschweiler, B.J.; Aubert, R.; Haldimann, M. Arsenic species in rice and rice-based products consumed by toddlers in Switzerland. Food Addit. Contam. Part A 2018, 35, 1164–1178. [Google Scholar] [CrossRef] [PubMed]
  341. Murugaiyan, V.; Zeibig, F.; Anumalla, M.; Siddiq, S.A.; Frei, M.; Murugaiyan, J.; Ali, J. Arsenic Stress Responses and Accumulation in Rice. In Rice Improvement; Springer: Berlin/Heidelberg, Germany, 2021; pp. 281–313. [Google Scholar] [CrossRef]
  342. Rahman, M.A.; Hasegawa, H.; Rahman, M.M.; Miah, M.A.M.; Tasmin, A. Straighthead disease of rice (Oryza sativa L.) induced by arsenic toxicity. Environ. Exp. Bot. 2008, 62, 54–59. [Google Scholar] [CrossRef]
  343. Choudhury, B.; Chowdhury, S.; Biswas, A.K. Regulation of growth and metabolism in rice (Oryza sativa L.) by arsenic and its possible reversal by phosphate. J. Plant Interact. 2011, 6, 15–24. [Google Scholar] [CrossRef]
  344. Dubey, S.; Shri, M.; Misra, P.; Lakhwani, D.; Bag, S.K.; Asif, M.H.; Trivedi, P.K.; Tripathi, R.D.; Chakrabarty, D. Heavy metals induce oxidative stress and genome-wide modulation in transcriptome of rice root. Funct. Integr. Genom. 2014, 14, 401–417. [Google Scholar] [CrossRef]
  345. Mishra, S.; Jha, A.B.; Dubey, R.S. Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 2011, 248, 565–577. [Google Scholar] [CrossRef] [PubMed]
  346. Haider, F.U.; Liqun, C.; Coulter, J.A.; Cheema, S.A.; Wu, J.; Zhang, R.; Wenjun, M.; Farooq, M. Cadmium Toxicity in Plants: Impacts and Remediation Strategies. Ecotoxicol. Environ. Saf. 2021, 211, 111887. [Google Scholar] [CrossRef] [PubMed]
  347. Sun, L.; Wang, J.; Song, K.; Sun, Y.; Qin, Q.; Xue, Y. Transcriptome Analysis of Rice (Oryza Sativa L.) Shoots Responsive to Cadmium Stress. Sci. Rep. 2019, 9, 10177. [Google Scholar] [CrossRef]
  348. Fu, H.; Yu, H.; Li, T.; Wu, Y. Effect of Cadmium Stress on Inorganic and Organic Components in Xylem Sap of High Cadmium Accumulating Rice Line (Oryza sativa L.). Ecotoxicol. Environ. Saf. 2019, 168, 330–337. [Google Scholar] [CrossRef]
  349. Yang, H.; Yu, H.; Tang, H.; Huang, H.; Zhang, X.; Zheng, Z.; Wang, Y.; Li, T. Physiological responses involved in cadmium tolerance in a high-cadmium-accumulating rice (Oryza sativa L.) line. Environ. Sci. Pollut. Res. 2021, 28, 41736–41745. [Google Scholar] [CrossRef]
  350. Mostofa, M.G.; Hossain, M.A.; Fujita, M.; Tran, L.S.P. Physiological and Biochemical Mechanisms Associated with Trehalose-Induced Copper-Stress Tolerance in Rice. Sci. Rep. 2015, 5, 11433. [Google Scholar] [CrossRef] [PubMed]
  351. Mostofa, M.G.; Rahman, M.M.; Ansary, M.M.U.; Fujita, M.; Tran, L.S.P. Interactive Effects of Salicylic Acid and Nitric Oxide in Enhancing Rice Tolerance to Cadmium Stress. Int. J. Mol. Sci. 2019, 20, 5798. [Google Scholar] [CrossRef] [PubMed]
  352. Wang, Y.; Jiang, X.; Li, K.; Wu, M.; Zhang, R.; Zhang, L.; Chen, G. Photosynthetic responses of Oryza sativa L. seedlings to cadmium stress: Physiological, biochemical and ultrastructural analyses. BioMetals 2014, 27, 389–401. [Google Scholar] [CrossRef] [PubMed]
  353. Rizwan, M.; Ali, S.; Adrees, M.; Rizvi, H.; Zia-ur-Rehman, M.; Hannan, F.; Qayyum, M.F.; Hafeez, F.; Ok, Y.S. Cadmium stress in rice: Toxic effects, tolerance mechanisms, and management: A critical review. Environ. Sci. Pollut. Res. 2016, 23, 17859–17879. [Google Scholar] [CrossRef] [PubMed]
  354. Aslam, M.; Aslam, A.; Sheraz, M.; Ali, B.; Ulhassan, Z.; Najeeb, U.; Zhou, W.; Gill, R.A. Lead Toxicity in Cereals: Mechanistic Insight Into Toxicity, Mode of Action, and Management. Front. Plant Sci. 2021, 11, 2248. [Google Scholar] [CrossRef] [PubMed]
  355. Khan, M.; Rolly, N.K.; Al Azzawi, T.N.I.; Imran, M.; Mun, B.G.; Lee, I.J.; Yun, B.W. Lead (Pb)-Induced Oxidative Stress Alters the Morphological and Physio-Biochemical Properties of Rice (Oryza Sativa L.). Agronomy 2021, 11, 409. [Google Scholar] [CrossRef]
  356. Khan, F.; Hussain, S.; Tanveer, M.; Khan, S.; Hussain, H.A.; Iqbal, B.; Geng, M. Coordinated effects of lead toxicity and nutrient deprivation on growth, oxidative status, and elemental composition of primed and non-primed rice seedlings. Environ. Sci. Pollut. Res. 2018, 25, 21185–21194. [Google Scholar] [CrossRef]
  357. Li, Y.F.; Zhao, J.; Li, Y.F.; Xu, X.; Zhang, B.; Liu, Y.; Cui, L.; Li, B.; Gao, Y.; Chai, Z. Comparative Metalloproteomic Approaches for the Investigation Proteins Involved in the Toxicity of Inorganic and Organic Forms of Mercury in Rice (Oryza sativa L.) Roots. Metallomics 2016, 8, 663–671. [Google Scholar] [CrossRef]
  358. Mao, Q.; Tang, L.; Ji, W.; Rennenberg, H.; Hu, B.; Ma, M. Elevated CO2 and Soil Mercury Stress Affect Photosynthetic Characteristics and Mercury Accumulation of Rice. Ecotoxicol. Environ. Saf. 2021, 208, 111605. [Google Scholar] [CrossRef]
  359. Palmieri, J.; Rzigalinski, B.; Benjamin, B.; Collins, E.; Kaur, G.; Brunette, J.; Council-Troche, M.; Wilson, M.; Meacham, S.; Guthrie, T. Implications and Significance of Mercury in Rice. J. Food Nutr. Metab. 2020, 3, 1–5. [Google Scholar] [CrossRef]
  360. Meng, B.; Feng, X.; Qiu, G.; Anderson, C.W.N.; Wang, J.; Zhao, L. Localization and Speciation of Mercury in Brown Rice with Implications for Pan-Asian Public Health. Environ. Sci. Technol. 2014, 48, 7974–7981. [Google Scholar] [CrossRef] [PubMed]
  361. Rao, G.; Ashraf, U.; Huang, S.; Cheng, S.; Abrar, M.; Mo, Z.; Pan, S.; Tang, X. Ultrasonic seed treatment improved physiological and yield traits of rice under lead toxicity. Environ. Sci. Pollut. Res. 2018, 25, 33637–33644. [Google Scholar] [CrossRef] [PubMed]
  362. Ashraf, U.; Tang, X. Yield and Quality Responses, Plant Metabolism and Metal Distribution Pattern in Aromatic Rice under Lead (Pb) Toxicity. Chemosphere 2017, 176, 141–155. [Google Scholar] [CrossRef] [PubMed]
  363. Hartley-Whitaker, J.; Ainsworth, G.; Meharg, A.A. Copper- and Arsenate-Induced Oxidative Stress in Holcus Lanatus L. Clones with Differential Sensitivity. Plant Cell Environ. 2001, 24, 713–722. [Google Scholar] [CrossRef]
  364. Duan, G.-L.; Hu, Y.; Liu, W.-J.; Kneer, R.; Zhao, F.-J.; Zhu, Y.-G. Evidence for a role of phytochelatins in regulating arsenic accumulation in rice grain. Environ. Exp. Bot. 2011, 71, 416–421. [Google Scholar] [CrossRef]
  365. Kong, D.; Ju, C.; Parihar, A.; Kim, S.; Cho, D.; Kwak, J.M. Arabidopsis Glutamate Receptor Homolog3.5 Modulates Cytosolic Ca2+ Level to Counteract Effect of Abscisic Acid in Seed Germination. Plant Physiol. 2015, 167, 1630–1642. [Google Scholar] [CrossRef] [PubMed]
  366. Jiang, M.; Jiang, J.; Li, S.; Li, M.; Tan, Y.; Song, S.; Shu, Q.; Huang, J. Glutamate Alleviates Cadmium Toxicity in Rice via Suppressing Cadmium Uptake and Translocation. J. Hazard. Mater. 2020, 384, 121319. [Google Scholar] [CrossRef]
  367. Ahsan, N.; Lee, S.H.; Lee, D.G.; Lee, H.; Lee, S.W.; Bahk, J.D.; Lee, B.H. Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. Comptes Rendus Biol. 2007, 330, 735–746. [Google Scholar] [CrossRef]
  368. Chen, Y.-A.; Chi, W.-C.; Trinh, N.N.; Huang, L.-Y.; Chen, Y.-C.; Cheng, K.-T.; Huang, T.-L.; Lin, C.-Y.; Huang, H.-J. Transcriptome Profiling and Physiological Studies Reveal a Major Role for Aromatic Amino Acids in Mercury Stress Tolerance in Rice Seedlings. PLoS ONE 2014, 9, e95163. [Google Scholar] [CrossRef]
  369. Kalita, J.; Pradhan, A.K.; Shandilya, Z.M.; Tanti, B. Arsenic Stress Responses and Tolerance in Rice: Physiological, Cellular and Molecular Approaches. Rice Sci. 2018, 25, 235–249. [Google Scholar] [CrossRef]
  370. Liu, J.; Cao, C.; Wong, M.; Zhang, Z.; Chai, Y. Variations between rice cultivars in iron and manganese plaque on roots and the relation with plant cadmium uptake. J. Environ. Sci. 2010, 22, 1067–1072. [Google Scholar] [CrossRef] [PubMed]
  371. Islam, E.; Khan, M.T.; Irem, S. Biochemical mechanisms of signalling: Perspectives in plant under arsenic stress. Ecotoxicol. Environ. Saf. 2015, 114, 126–133. [Google Scholar] [CrossRef] [PubMed]
  372. Kumar, S.; Trivedi, P.K. Heavy Metal Stress Signaling in Plants. In Plant Metal Interaction; Ahmad, P., Ed.; Elsevier: Amsterdan, The Netherlands, 2016; pp. 585–603. [Google Scholar] [CrossRef]
  373. Rao, K.P.; Vani, G.; Kumar, K.; Wankhede, D.P.; Misra, M.; Gupta, M. Arsenic stress activates MAP kinase in rice roots and leaves. Arch. Biochem. Biophys. 2011, 506, 73–82. [Google Scholar] [CrossRef] [PubMed]
  374. Conde, A.; Chaves, M.M.; Geros, H. Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 2011, 52, 1583–1602. [Google Scholar] [CrossRef] [PubMed]
  375. Steinhorst, L.; Kudla, J. Calcium and reactive oxygen species rule the waves of signaling. Plant Physiol. 2013, 163, 471–485. [Google Scholar] [CrossRef] [PubMed]
  376. Lin, Y.F.; Aarts, M.G. The molecular mechanism of zinc and cadmium stress response in plants. Cell. Mol. Life Sci. 2012, 69, 3187–3206. [Google Scholar] [CrossRef] [PubMed]
  377. Tiwari, S.; Lata, C.; Singh Chauhan, P.; Prasad, V.; Prasad, M. A functional genomic perspective on drought signalling and its crosstalk with phytohormone-mediated signalling pathways in plants. Curr. Genom. 2017, 18, 469–482. [Google Scholar] [CrossRef] [PubMed]
  378. Yeh, C.M.; Hsiao, L.J.; Huang, H.J. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol. 2004, 45, 1306–1312. [Google Scholar] [CrossRef]
  379. Liu, X.M.; Kim, K.E.C.; Kim, K.E.C.; Nguyen, X.C.; Han, H.J.; Jung, M.S. Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochemistry 2010, 71, 614–618. [Google Scholar] [CrossRef]
  380. Singh, I.; Shah, K. Exogenous application of methyl jasmonate lowers the effect of cadmium-induced oxidative injury in rice seedlings. Phytochemistry 2014, 108, 57–66. [Google Scholar] [CrossRef]
  381. Chakrabarty, D.; Trivedi, P.K.; Misra, P.; Tiwari, M.; Shri, M.; Shukla, D. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 2009, 74, 688–702. [Google Scholar] [CrossRef] [PubMed]
  382. Shi, S.; Wang, T.; Chen, Z.; Tang, Z.; Wu, Z.; Salt, D.E.; Chao, D.Y.; Zhao, F.J. OsHAC1;1 and OsHAC1;2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol. 2016, 172, 1708–1719. [Google Scholar] [CrossRef]
  383. Tang, L.; Mao, B.; Li, Y.; Lv, Q.; Zhang, L.; Chen, C.; He, H.; Wang, W.; Zeng, X.; Shao, Y.; et al. Knockout of OsNramp5 Using the CRISPR/Cas9 System Produces Low Cd-Accumulating Indica Rice without Compromising Yield. Sci. Rep. 2017, 7, 14438. [Google Scholar] [CrossRef] [PubMed]
  384. Lu, C.; Zhang, L.; Tang, Z.; Huang, X.Y.; Ma, J.F.; Zhao, F.J. Producing cadmium-free Indica rice by overexpressing OsHMA3. Environ. Int. 2019, 126, 619–626. [Google Scholar] [CrossRef]
  385. Arya, G.C.; Sarkar, S.; Manasherova, E.; Aharoni, A.; Cohen, H. The Plant Cuticle: An Ancient Guardian Barrier Set Against Long-Standing Rivals. Front. Plant Sci. 2021, 12, 663165. [Google Scholar] [CrossRef] [PubMed]
  386. Tang, L.; Dong, J.; Tan, L.; Ji, Z.; Li, Y.; Sun, Y.; Chen, C.; Lv, Q.; Mao, B.; Hu, Y.; et al. Overexpression of OsLCT2, a Low-Affinity Cation Transporter Gene, Reduces Cadmium Accumulation in Shoots and Grains of Rice. Rice 2021, 14, 89. [Google Scholar] [CrossRef]
  387. Mishra, N.; Srivastava, A.P.; Esmaeili, N.; Hu, W.; Shen, G. Overexpression of the Rice Gene OsSIZ1 in Arabidopsis Improves Drought-, Heat-, and Salt-Tolerance Simultaneously. PLoS ONE 2018, 13, 201716. [Google Scholar] [CrossRef]
  388. Liu, X.S.; Feng, S.J.; Zhang, B.Q.; Wang, M.Q.; Cao, H.W.; Rono, J.K.; Chen, X.; Yang, Z.M. OsZIP1 Functions as a Metal Efflux Transporter Limiting Excess Zinc, Copper and Cadmium Accumulation in Rice. BMC Plant Biol. 2019, 19, 283. [Google Scholar] [CrossRef]
  389. Rono, J.K.; Le Wang, L.; Wu, X.C.; Cao, H.W.; Zhao, Y.N.; Khan, I.U.; Yang, Z.M. Identification of a New Function of Metallothionein-like Gene OsMT1e for Cadmium Detoxification and Potential Phytoremediation. Chemosphere 2021, 265, 129136. [Google Scholar] [CrossRef]
  390. Ogo, Y.; Itai, R.N.; Kobayashi, T.; Aung, M.S.; Nakanishi, H.; Nishizawa, N.K. OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol. Biol. 2011, 75, 593–605. [Google Scholar] [CrossRef]
  391. Tao, J.; Lu, L. Advances in Genes-Encoding Transporters for Cadmium Uptake, Translocation, and Accumulation in Plants. Toxics 2022, 10, 411. [Google Scholar] [CrossRef] [PubMed]
  392. Yamazaki, S.; Ueda, Y.; Mukai, A.; Ochiai, K.; Matoh, T. Rice Phytochelatin Synthases OsPCS1 and OsPCS2 Make Different Contributions to Cadmium and Arsenic Tolerance. Plant Direct 2018, 2, e00034. [Google Scholar] [CrossRef] [PubMed]
  393. Shimo, H.; Ishimaru, Y.; An, G.; Yamakawa, T.; Nakanishi, H.; Nishizawa, N.K. Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J. Exp. Bot. 2011, 62, 5727–5734. [Google Scholar] [CrossRef] [PubMed]
  394. Sahoo, R.K.; Tuteja, N. OsSUV3 functions in cadmium and zinc stress tolerance in rice (Oryza sativa L. cv IR64). Plant Signal. Behav. 2014, 9, e27389. [Google Scholar] [CrossRef] [PubMed]
  395. Ding, Y.; Ye, Y.; Jiang, Z.; Wang, Y.; Zhu, C. MicroRNA390 Is Involved in Cadmium Tolerance and Accumulation in Rice. Front. Plant Sci. 2016, 7, 235. [Google Scholar] [CrossRef] [PubMed]
  396. Hu, S.; Yu, Y.; Chen, Q.; Mu, G.; Shen, Z.; Zheng, L. OsMYB45 plays an important role in rice resistance to cadmium stress. Plant Sci. 2017, 264, 1–8. [Google Scholar] [CrossRef] [PubMed]
  397. Ding, Y.; Gong, S.; Wang, Y.; Wang, F.; Bao, H.; Sun, J.; Cai, C.; Yi, K.; Chen, Z.; Zhu, C. MicroRNA166 Modulates Cadmium Tolerance and Accumulation in Rice. Plant Physiol. 2018, 177, 1691–1703. [Google Scholar] [CrossRef]
Figure 1. Effects of different abiotic stresses on rice.
Figure 1. Effects of different abiotic stresses on rice.
Plants 12 03948 g001
Figure 2. A simplified diagram illustrating how rice plants respond to various abiotic stresses. The overall signaling pathways in plants are triggered when they perceive signals related to abiotic stress, leading to the activation of stress responses.
Figure 2. A simplified diagram illustrating how rice plants respond to various abiotic stresses. The overall signaling pathways in plants are triggered when they perceive signals related to abiotic stress, leading to the activation of stress responses.
Plants 12 03948 g002
Figure 3. A schematic diagram showing a heavy metal stress signaling cascade that enhances stress-responsive gene expression in rice.
Figure 3. A schematic diagram showing a heavy metal stress signaling cascade that enhances stress-responsive gene expression in rice.
Plants 12 03948 g003
Table 1. Identified genes linked to drought stress tolerance in rice.
Table 1. Identified genes linked to drought stress tolerance in rice.
Name of GenesFunctionReference
DRO1Stimulates the growth of roots, resulting in increased length and deeper penetration into the soil[75]
EcNAC67Enhances water content, postpones leaf curling, and increases the mass of roots and shoots[78]
DsM1Assists in removing reactive oxygen species and enhances drought resistance during the early growth (seedling) phase[77]
OsPYL/RCAR5Causes the closure of stomata and controls the weight of leaves[33]
OsDREB2BLength of roots and the amount of root growth[73]
OsNAC5Increases the size of the roots and improves the amount of grain produced[79]
SNAC1Enhances spikelet fertility[80]
OsLEA3-1Enhances grain yield[81]
OsbZIP23Increase grain yield[82]
OsbZIP72Enhancing tolerance to drought and increasing sensitivity to ABA (upregulating ABA)[83]
AP37Improves the process of seed filling and increases the weight of the grain[84]
OsNAC10Enhances resistance to drought during the vegetative phase, enhances root size, and enhances crop productivity[79,85]
EDT1/HDG11Increases water use efficiency, the buildup of compatible osmolytes, heightened antioxidant enzymatic activity, and improves photosynthesis[86]
AtDREB1AOsmolytes accumulation, maintenance of chlorophyll, increment in relative water content, and reduction in ion leakage[87]
OsCPK9Enhances drought tolerance in transgenics through improved stomatal closure and osmoregulation[88]
ADCEnhances resistance to drought by synthesis of polyamines such as putrescine and spermine [61]
OsOATEnhances resistance to drought and promotes higher seed production[89]
OsTPS1Enhances rice seedling’s tolerance to drought, cold, and salinity stress[90]
P5CSEnhances biomass production under salinity and drought stresses[91]
HVA1Plasma membrane stability, increases leaf relative water content (RWC) and growth under drought stress[92]
Hrf1Drought resistance via antioxidants generation, ABA signaling, and regulating stomata closure[93]
JERF1Enhances drought resistance[94]
OsRDCP1Improves drought stress tolerance[95]
OsSDIR1Regulates stomata under drought stress[96]
OsSRO1cRegulates stomatal closure and enhances oxidative stress tolerance [97]
Table 2. Identified genes linked to heat stress tolerance in rice.
Table 2. Identified genes linked to heat stress tolerance in rice.
Name of GenesFunctionReference
OsMYB55Enhances amino acids’ metabolic process, enhancing the ability to withstand high temperatures[139]
OsAREB1Controls abiotic stress-responsive gene expression utilizing an ABA-dependent mechanism[143]
OsHSF7Increases the expression of HSPs and other genes that protect against exposure to high temperatures, resulting in enhanced resistance to heat[144]
HSP101The effects of heat training in rice seedlings are prolonged by post-transcriptional interactions of HSA32/HSP101 after heat treatment[145]
GAD3Participate in the ability to withstand high temperatures[139]
OsHTASImproves rice’s ability to withstand heat by mediating stomata closure caused by H2O2[146]
TCM5Plays a vital role in the development of chloroplasts and the maintenance of PSII function in high temperatures[147]
EG1Enhances homeostasis in floral organs and the ability to withstand temperature changes by activating a pathway involving mitochondrial lipase in response to high temperatures[147]
OsTT1Breaks down poisonous denatured proteins while preserving the high-temperature response process[127]
TOGR1Plays a role in the normal processing of rRNA precursors at high temperatures and acts as a chaperone for the nucleolar SSU complex, crucial for cell growth in high-temperature environments[148]
OsHES1Plays a crucial part in adjusting to heat stress and ensuring the proper functioning of chloroplasts.[149]
OsAET1Plays a dual function in regulating the response to high temperatures through tRNA modification and control of translation[150]
OsNTL3Plays a crucial role in thermotolerance by interacting with OsbZIP74[151]
OsHsfA2cInvolved in regulating the transcription of the HSP100 gene in the cytoplasm of rice[152]
OsHCI1Facilitates the nuclear export of target proteins, and its heterologous expression enhanced thermotolerance[141]
OsNSUN2Controls the mRNA modification of 5-methylcytosine (m5C), which improves mRNA translation efficiency and sustains normal development at higher temperatures[153]
OsTT3.1TT3.2 is ubiquitinated by TT3.1 for vacuolar degradation, and TT3.1 may function as a thermosensor[154]
OsTT3.2Chloroplasts rely on mature TT3.2 proteins to protect thylakoids against the detrimental effects of heat stress[154]
OsANN1Enhances SOD and CAT activity, controls H2O2 content and redox homeostasis, to provide cell protection against abiotic stress[155]
Table 3. Identified genes linked to cold stress tolerance in rice.
Table 3. Identified genes linked to cold stress tolerance in rice.
Name of GenesFunctionReference
OsLTPL159Reduces the toxic effects of ROS, increases cell wall’s cellulose deposition, and increases osmolyte accumulation in rice, which increases the plant’s ability to withstand cold temperatures in its early seedling stages[200]
qPSST6Long-chain fatty acid production, involved in rice’s cold-tolerance during the booting stage[201]
OsCOINProtein induced by cold enhances cold, drought, and salt tolerance[202]
Osa-MIR319aIncreased leaf blade width[203]
OsGH3-2Regulates ABA and auxin levels during cold and drought stress[204]
OsMYB3R-2Regulates cell cycle (especially G2/M phase) to mediate cold tolerance in rice[205]
SNAC2Enhances cold and salt tolerance in rice[206]
OsDREB1FEnhances cold tolerance in rice[207]
ASR3Enhances cold/draught tolerance mediated by hormonal/sugar signaling[208]
OsFAD2An essential enzyme that raises grain yield and germination rate under LTS (low-temperature stress conditions)[209]
OsLti6bProduces hydrophobic protein in the ovaries and stamens of flowers undergoing cold treatment[210]
OsWRKY45Has a significant role in the signaling of ABA and serves as a means of communication between abiotic and biotic stresses[211]
OsRAN2GTPase that enhances cold tolerance through cell cycle regulation[212]
OsSPX1Participates in phosphate signaling as well as the interplay between the oxidative and cold stress tolerance mechanisms.[213]
OsDEG10Produces RNA-binding protein and has a key role in cold tolerance as well as response to other stresses (anoxia, photooxidative, and salinity)[214]
Oscrr6It has a key role in rice growth/photosynthesis at colder temperatures[215]
OsPIP2Participates in water homeostasis during cold stress tolerance [216]
OsPRP3Involved in the enhancement of cold tolerance in rice[217]
OsAsr1Involved in both vegetative and reproductive stages of cold tolerance[218]
MYBS3Modulates cold tolerance signaling pathways[219]
OVP1Involved in lowering malondialdehyde levels and increasing proline accumulation to increase tolerance to cold[220]
Table 4. Identified genes linked to submergence stress tolerance in rice.
Table 4. Identified genes linked to submergence stress tolerance in rice.
Name of GenesFunctionReference
OsACS1Involved in ethylene production and the rapid elongation of the stem in submerged rice[257,258]
OsACS5Involved in ethylene production and the rapid elongation of the stem in submerged rice[257,258]
SNORKEL1 (SK1)ERFs that modulate the internode elongation of deepwater rice during submergence[247]
SNORKEL2 (SK2)ERFs that regulate the internode elongation of deepwater rice during submergence[247]
Submergence 1A (SUB1A)Plant quiescence and plant survival under complete submergence[249]
SDIInvolved in internode elongation[254]
OsHSD1Involved in underwater photosynthesis in submerged rice[259]
OsTPP7Involved in anaerobic germination[260]
AGPPasePromotes increased non-structural carbohydrate (NSC) buildup, which is accessible for a quick recovery after submersion[261]
EREBP1enhances resistance to submersion and facilitates better recovery from extended submersion[262]
CIPK15Involved in the regulation of sugar and energy production enabling growth of rice under floodwater[263]
Table 5. Identified genes linked to salt stress tolerance in rice.
Table 5. Identified genes linked to salt stress tolerance in rice.
Name of GenesFunctionReference
OsCPK12Increases resistance to high salt levels by decreasing ROS buildup [319]
OsLOL5Enhance ROS scavenging and rice tolerance under salinity stress[320]
OsMAPK44Participates in ion homeostasis under salinity stress[321]
OsJRL40Increases antioxidant enzymatic activities and maintains the balance of Na+/K+ during salinity stress. Manages rice’s salt stress by regulating the expression of genes responsible for transporting Na+/K+, as well as genes involved in salt-responsive transcription factors and proteins [322]
OsSAPK4Modulates ion homeostasis as well as the growth and development of rice in a salinized environment[323]
OsKAT1Enhances rice’s salinity tolerance by enhancing K+ uptake and thus decreasing Na+ accumulation [324]
OsTPS8Controls the ability of rice to tolerate salinity stress by managing the levels of soluble sugars and regulating the activity of genes related to ABA signaling through the regulation of SAPK9[325]
OsBADH1Enhances salinity stress tolerance by positively regulating osmoprotectant biosynthesis[326]
OsMYB91Manages the growth of rice and its ability to tolerate salt stress.[327]
OsVP1 and OsNHX1Enhances the tolerance of salt by decreasing the accumulation of Na+ in leaves, photosynthesis activity, and increase root biomass[328]
OsHKT1;1, OsHKT1;4 and OsHKT1;5Enhance the tolerance of salt by decreasing the accumulation of Na+ in shoots when exposed to salt stress[329,330,331]
OsHAK5Enhance rice’s salinity tolerance by contributing to cation homeostasis[332]
Table 6. Identified genes linked to heavy metals stress tolerance in rice.
Table 6. Identified genes linked to heavy metals stress tolerance in rice.
Name of GenesFunctionReference
OsHAC1;1 and OsHAC1;2Drastically influence limiting the accumulation of As in both the shoots and grains of rice[382]
OsNRAMP5Enhances resistance to the toxicity of Cd[383]
OsHMA3Enhances resistance to the toxicity of Cd[384]
OsABCG31Enhances resistance to the toxicity of Cd and Pb[385]
OsLCT1Enhances resistance to the toxicity of Cd Al [386]
OsSIZEnhances resistance to the toxicity of Cd [387]
OsZIP1Enhances resistance to the toxicity of Cd, Zn, [388]
OsNAC5Enhances resistance to the toxicity of Cd and Pb[79]
OsMT1eEncodes a metal-detoxifying protein[389]
OsIRO2TF that modulates the activity of genes related to Fe balance in rice[390]
OsIRT1Participates in Cd absorption in rice. It is involved in Cd stress tolerance[391]
OsPCS1It is involved in detoxifying heavy metals and involved in Cd stress tolerance [392]
OsLCDInvolved in Cd compartmentation[393]
OsSUV3Improved Cd and Zn stress tolerance[394]
OsSRKIncreases the uptake and transfer of Cd[395]
OsHMA2Improves transfer of Cd from roots to shoots[395]
OsMYB45Improves Cd stress tolerance[396]
OsHB4Improves Cd accumulation and tolerance[397]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sarma, B.; Kashtoh, H.; Lama Tamang, T.; Bhattacharyya, P.N.; Mohanta, Y.K.; Baek, K.-H. Abiotic Stress in Rice: Visiting the Physiological Response and Its Tolerance Mechanisms. Plants 2023, 12, 3948.

AMA Style

Sarma B, Kashtoh H, Lama Tamang T, Bhattacharyya PN, Mohanta YK, Baek K-H. Abiotic Stress in Rice: Visiting the Physiological Response and Its Tolerance Mechanisms. Plants. 2023; 12(23):3948.

Chicago/Turabian Style

Sarma, Bhaskar, Hamdy Kashtoh, Tensangmu Lama Tamang, Pranaba Nanda Bhattacharyya, Yugal Kishore Mohanta, and Kwang-Hyun Baek. 2023. "Abiotic Stress in Rice: Visiting the Physiological Response and Its Tolerance Mechanisms" Plants 12, no. 23: 3948.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop