Next Article in Journal
Myrrh and Chamomile Flower Extract Inhibit Mediator Release from IgE-stimulated Mast-Cell-Like RBL-2H3 Cells
Next Article in Special Issue
Environmental Filtering Drives Fungal Phyllosphere Community in Regional Agricultural Landscapes
Previous Article in Journal
Phytoprofiling of Sorbus L. Inflorescences: A Valuable and Promising Resource for Phenolics
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 11
Issue 24
10.3390/plants11243417
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Serendipita indica—A Review from Agricultural Point of View

by
Sana Saleem
1,*,
Agnieszka Sekara
2 and
Robert Pokluda
1
1
Department of Vegetable Sciences and Floriculture, Faculty of Horticulture, Mendel University in Brno, Valticka 337, 691 44 Lednice, Czech Republic
2
Department of Horticulture, Faculty of Biotechnology and Horticulture, University of Agriculture, 31-120 Krakow, Poland
*
Author to whom correspondence should be addressed.
Plants 2022, 11(24), 3417; https://doi.org/10.3390/plants11243417
Submission received: 5 October 2022 / Revised: 1 December 2022 / Accepted: 5 December 2022 / Published: 7 December 2022
(This article belongs to the Special Issue Phytomicrobiome Research for Disease and Pathogen Management)
Browse Figures
Review Reports Versions Notes

Abstract

:
Fulfilling the food demand of a fast-growing population is a global concern, resulting in increased dependence of the agricultural sector on various chemical formulations for enhancing crop production. This leads to an overuse of chemicals, which is not only harmful to human and animal health, but also to the environment and the global economy. Environmental safety and sustainable production are major responsibilities of the agricultural sector, which is inherently linked to the conservation of the biodiversity, the economy, and human and animal health. Scientists, therefore, across the globe are seeking to develop eco-friendly and cost-effective strategies to mitigate these issues by putting more emphasis on the use of beneficial microorganisms. Here, we review the literature on Serendipita indica, a beneficial endophytic fungus, to bring to the fore its properties of cultivation, the ability to enhance plant growth, improve the quality of produced crops, mitigate various plant stresses, as well as protect the environment. The major points in this review are as follows: (1) Although various plant growth promoting microorganisms are available, the distinguishing character of S. indica being axenically cultivable with a wide range of hosts makes it more interesting for research. (2) S. indica has numerous functions, ranging from promoting plant growth and quality to alleviating abiotic and biotic stresses, suggesting the use of this fungus as a biofertiliser. It also improves the soil quality by limiting the movement of heavy metals in the soil, thus, protecting the environment. (3) S. indica’s modes of action are due to interactions with phytohormones, metabolites, photosynthates, and gene regulation, in addition to enhancing nutrient and water absorption. (4) Combined application of S. indica and nanoparticles showed synergistic promotion in crop growth, but the beneficial effects of these interactions require further investigation. This review concluded that S. indica has a great potential to be used as a plant growth promoter or biofertiliser, ensuring sustainable crop production and a healthy environment.

1. Introduction

A diverse range of microorganisms in soil play critical functions, such as nutrient acquisition, organic matter cycling, soil and plant health maintenance, soil restoration and ecosystem primary production, and are thus considered as beneficial organisms [1]. By increasing crop yield, quality, and shielding the plants from various biotic and abiotic challenges, these microbes have shown several positive effects on the farming system. In addition, environmental protection, an increasing concern across the globe, is the main advantage these creatures provide [2]. Moreover, the rising demand and growing awareness of high-quality food has stimulated the development of sustainable and environmentally friendly agricultural production practices. These methods could be achieved by reducing the usage of chemicals and encouraging the application of beneficial microorganisms [3]. Apart from contributing to sustainability, beneficial microorganisms are also economically efficient [4]. These microorganisms can be symbiotic or non-symbiotic bacteria, actinomycetes, and mycorrhizal and endophytic fungi [5]. Throughout the study of various microorganisms, an emphasis is placed on studying endophytic fungi, as they can yield tangible beneficial effects within the host plant, such as improve plant growth, quality, and enhance host resistance to abiotic and biotic stresses, thereby confirming their significance in the agricultural sector [6,7].
Serendipita indica, formerly known as Piriformospora indica, belonging to the order Sebacinales (Basidiomycota), is one of the beneficial endophytic fungi known to possess numerous advantages and has been studied extensively for decades. S. indica, obtained by Ajeet Verma from the roots of Prosopis juliflora and Zizyphus nummularia in the Thar desert in Northwest India, is characterised by the formation of pear-shaped spores known as chlamydospores [8]. These spores are produced by thin walled, hyaline, and septate hyphae [9]. S. indica is distinguished by the unique trait that it can be cultivated without any plant material on a variety of artificial media, such as aspergillus medium, modified aspergillus medium, potato dextrose agar (PDA) or broth (PDB), malt extract, modified Melin-Norkrans (MMN) medium [10], and jaggery containing medium [11]. This property differentiates it from arbuscular mycorrhizal fungi (AMF), with which it shares biological similarities (Figure 1).
This endophytic fungus can colonise a wide range of plant species and develop symbiotic associations with them [12,13]. Mainly, colonisation takes place in the root zone and begins with the germination of chlamydospores, followed by the formation of a hyphal network on and inside the root. Hyphae form branches and continue to grow by penetrating the subepidermal layers of roots, and eventually, cover the rhizodermal and cortical cells (Figure 2). Mature root segments show intra- and intercellular colonisation patterns, while conductive tissues are free from colonisation. This fungus colonises different root zones, with maximum colonisation in the zone of cell differentiation. In addition, the fungus penetrates root hair cells, forming hyphae from germinating spores [14,15] (Figure 3). This process begins with the biotrophic phase, followed by the cell death phase, to build the symbiotic relationship with the host rhizosphere [16,17].
Moreover, a successful symbiosis between S. indica and the host plant depends on administering the right quantity of inoculum, which can be assessed using a qPCR test [18]. According to Rokni et al. [19], optimising the S. indica inoculum concentration had an impact on the host plant’s development. Plant growth was enhanced by a 1–3% w/w concentration; however, higher doses did not show any positive benefits.
The production of calcium and lectin protein kinase induced during symbiotic association are suggested to be the early signalling factors in S. indica–host plant colonisation [20,21]. Additionally, the synthesis of the plant hormone ethylene is considered crucial for the interaction between plant hosts and fungi [22].
S. indica has been reported to provide numerous advantages to host plants upon colonisation of roots. These advantages include enhanced plant growth, nutrient uptake, and antioxidant activities; increased photosynthetic pigments, crop quality and yields; as well as the ability to mitigate various biotic and abiotic stresses [3,23,24,25,26,27,28]. Although mycelia and spores from fungi are typically considered the beneficial form of inoculum, some studies have demonstrated that cell wall extracts and culture filtrates from S. indica have a positive effect on plant growth [29,30].
Furthermore, to commercialise S. indica, biofertiliser formulation, known as ‘rootonic’, has been developed by culturing this fungus in a bioreactor [12,31,32] and mixing with carrier magnesium sulphite [33]. This endophytic fungus is proving to be an efficient source of bio-inoculant for the agricultural sector, with the least environmental hazards and improved agricultural sustainability.
In this review, we have summarised the effect of S. indica on the host plant and the underlying mechanisms. This review also includes the management of various plant stresses by S. indica and a brief description of its interactions with nanoparticles.

2. S. indica as a Growth Promoter

S. indica has been found to be a prime beneficial microorganism that improved the growth and development of various plant species under normal and stress conditions [3,28] (Figure 4). This endophytic fungus improved the germination rate in various plant species, such as chilli, cabbage, cucumber, eggplant, maize, okra, spinach, rice, and tobacco [11,34,35,36]. Improved seed germination under intense cold conditions in beetroot, carrot, cauliflower, onion, and radish has also been reported [17]. The application of S. indica has been reported to promote seedling growth and development by enhancing root and shoot growth, biomass, photosynthetic pigment production, and seedling vigour. [36,37,38]. Sheramati et al. [39] reported that S. indica improved the growth of Arabidopsis and tobacco seedlings by enhancing the nitrogen accumulation and expression of genes governing nitrogen reductase and the starch degrading enzyme glucan-water dikinase in their roots. These enzymes are responsible for nitrogen and starch metabolism in seedlings, which is essential for their growth and development.
This fungus is reported to promote the plant vegetative development in terms of height, leaf number, shoot and root growth, fresh weight, dry weight, as well as photosynthetic pigment and phytohormone synthesis [3,22,25,34,40,41]. Stimulation of nutrient uptake and their efficiency is also reported due to S. indica colonisation leading to improved plant growth, quality, and yield [25,42]. Improvement in other plant physiological attributes, such as inflorescence development, duration of flowering, flower size and number of flowers, have been reported with the application of the endophytic fungus S. indica [25,30,34,43]. Therefore, S. indica promotes plant growth and development by inducing earliness of host plant reproduction [44]. Furthermore, S. indica improved crop yields by elevating chlorophyll content, flower setting, grain yield, and pod number and size in crops, such as black pepper [43], fennel [45], rice [44,46], rapeseed [25], sweet potato [47], sunflower [48], and tomato [49,50].
In addition to improving the growth and production of crops, S. indica has improved the quality of the products. This impact may be attributable to increased root growth and root hair formation in plants treated with S. indica, which results in improved mineral nutrition acquisition and water uptake [9,45,51]. Singhal et al. [24] further proposed that nutrient uptake promoted by this endophytic fungus could be attributable to fungal hyphae penetrating deeper into the soil than root hair and thus absorbing more nutrients from the soil. Assimilation of macronutrients, such as nitrogen, phosphorus, potassium, sulphur, and magnesium is improved in crops, such as Poncirus trifoliata, Triticum aestivum, Brassica napus, Oryza sativa, Panicum miliaceum, Arabidopsis thaliana, etc. [7,25,46,52,53,54].
S. indica improves the availability of nitrogen by transforming the unavailable form into nitrate, which is taken up by plants [9]. Moreover, it stimulates the expression of the gene governing NADH-dependent nitrate reductase, which is responsible for nitrate assimilation in crops [9,55,56]. S. indica is able to convert organic phosphorus into plant-available form, thus improving the phosphorus uptake by plants under normal as well as under phosphorus-deficient conditions [17,57,58]. It also improves the acid phosphatase and alkaline phosphatase activities, leading to an improvement in phosphorus uptake in rice and rapeseed [58,59]. In addition to promoting soil phosphatase activities, S. indica upregulated the expression of the phosphate transporter genes (PT3, PT5, and PT6) in Poncirus trifoliata and thereby enhanced the phosphorus absorption by the plant [7]. S. indica colonisation improved the potassium concentration in tomatoes, resulting in higher levels of lycopene and ascorbic acid and therefore improving the quality of tomatoes [60]. Several studies have reported a significant increase in absorption of other macronutrients, such as calcium, magnesium, and sulphur [7,25,61,62,63]. An increase in the absorption of magnesium and sulphur is suggested due to the enhanced expression of transporters PiMgT1 and PiSulT, respectively, in plants treated with S. indica [62,63]. Moreover, the application of S. indica improved the acquisition of iron and zinc in rapeseed [25] and zinc in lettuce and Brassica napus [64,65]. Furthermore, inoculation with S. indica increased iron content in sugarcane plants by enhancing iron transportation [33,66]. Therefore, the application of S. indica has proven to enhance nutrient uptake in plants, and thus is considered as an emerging plant growth promoter. Table 1 summarises the effects of S. indica on the growth and quality of different host plants.
Furthermore, S. indica not only improves the nutritional status of plants, but also develops resilience in host plants against many stresses. Additionally, it reduces the concentration and effect of various harmful substances and heavy metals, thus enhancing soil health [91], which is further discussed in the review.

3. The Mechanism behind the Improvement in Growth, Yield, and Quality of Crops by S. indica

Since endophytic fungi are known to enter and survive inside a host plant, these fungi need to pass through the host’s defence system, which comprises specific receptors, such as pattern recognition receptors and intracellular receptors. These receptors capture the microbe or pathogen by recognizing the microbe- or pathogen-associated molecular patterns (MAMPs or PAMPs) located on the cell surface, thus resulting in MAMP- or PAMP-triggered immunity in the hosts. Other defence-related receptors are intracellular receptors, which recognise effector proteins secreted by the microbes, leading to effector-triggered immunity (ETI) [92,93]. Endophytic fungi produce some molecular patterns, such as β-glucan and chitin, which are recognised by the pattern recognition receptors present on host cell walls [94]. Then, chitin is converted into chitin oligomers by chitinase produced by the host plant, resulting in defensive reactions [95,96]. However, fungal endophytes produce chitin deacetylases that convert chitin oligomers to deacetylated chitosan oligomers, which are thus not recognised by the host plant’s receptors and prevent triggering the plant immune system [93]. In the case of S. indica, β-glucan-stimulated immunity is suppressed due to the presence of the fungal glucan-binding 1 protein gene, which encodes β-glucan-binding lectin that modifies the fungal cell wall, thus suppressing the recognition process in plant hosts [97]. Therefore, endophytic fungi have the capacity to survive in the plant root and offer various benefits, such as improving plant immunity and enhancing the response of plants toward various biotic and abiotic stresses [98] in exchange for carbohydrates as food.
Once the fungus successfully enters the host plant, it begins to develop a symbiotic association with the plant. It exhibits an impact on the plant by inducing an array of physiological and molecular changes, such as enhancing transportation and uptake of nutrients, promoting nutrient solubilisation, reducing heavy metal toxicity, and maintaining optimum pH. These modifications constitute the direct mechanism of S. indica mediated plant growth [56,91]. In contrast, indirect mechanisms are affiliated with changes in hosts, such as enhanced antioxidants and secondary metabolites production [99,100], decreased anti-nutrient contents, as well as modulation of gene expression and phytohormone production [91]. Moreover, S. indica enhances chlorophyll content, thus improving the rate of photosynthesis, and consequently, the growth of the plant [3]. Hua et al. [100] performed a global metabolic analysis in Chinese cabbage inoculated with S. indica and reported improvements in metabolite production, fatty acid content, and activity of the TCA cycle, leading to increased carbohydrate production in plants to support the growth and development of the root system.
Furthermore, S. indica-mediated growth involves interactions with phytohormones, such as auxin, gibberellin, cytokinin, and ethylene [101]. This fungus interferes with the synthesis and signalling of phytohormones to stimulate plant growth, development, and defence responses. Plants respond to S. indica by adjusting their hormone levels in the roots to ensure the growth and colonisation of this fungus [101]. Auxin, the major growth phytohormone, is reported to promote the growth and development of host plants under S. indica colonisation by regulating auxin-related genes and proteins, which are involved in transport and signal transduction of auxin, such as auxin influx carriers (AUX1), auxin efflux carriers (PINs), and auxin receptor (TIR1) [102]. Moreover, Dong et al. [103] reported the upregulation of auxin-responsive genes, which resulted in improving plant growth. In Chinese cabbage, auxin and its intermediates were enhanced under S. indica colonisation [100]. Other phytohormone levels, including gibberellin and ethylene, are also enhanced in S. indica-colonised plants, resulting in earlier blooming and better root colonisation [91,104,105]. Enhanced expressions of gibberellin biosynthetic genes, such as gibberellin 20-oxidase 2, gibberellin 3-oxidase 1, and gibberellin requiring 1 was reported in response to S. indica application [101]. Additionally, the cytokinin levels were elevated in plants upon S. indica colonisation by upregulating cytokinin receptor genes (CRE1, AHK2, and AHK3), cytokinin-responsive gene (ARR), and trans-zeatin cytokinin biosynthesis genes, thus enhancing plant growth [106,107].
Gene regulation is suggested as an important part of plant growth promotion mediated by S. indica colonisation. As mentioned, several gene expressions are regulated by S. indica colonisation to ameliorate the phytohormonal balance in the host plant. According to Ghorbani et al. [108] and Yang et al. [7], the use of S. indica enhanced the expression of host genes responsible for the uptake of nutrients, such as iron (IRO2, YSL1, and FRDL1) and phosphorus (PtPT3, PtPT5, and PtPT6) in rice and Poncirus trifoliata. Moreover, it has affected the expression of various other genes in host plants, such as sucrose synthase (SUS) and invertase (INV) genes, to improve the phosphorus concentration in Arabidopsis thaliana by altering the sugar metabolism and obtaining fructose and glucose from the host plant [109]. Furthermore, S. indica resulted in the upregulation of phytochelatin biosynthesis genes, such as PCS1 and PCS2 in rice plants, enhancing the phytochelatin that removes the toxic metals from the host plants [108]. In Brassica napus, expressions of genes, such as trans-2, 3-enoyl-CoA reductase (BnECR) and 3-ketoacyl-CoA synthase (BnFAE1) were downregulated by applying S. indica. These genes are responsible for encoding some enzymes that cause the biosynthesis of erucic acids, considered as an unhealthy substance [25]. Moreover, rapeseed fatty acid content was enhanced by upregulating the expression of fatty acid regulation genes, such as 3-ketoacyl-CoA reductase 1 (Bnkcr1) and 3-ketoacyl-CoA reductase 2 (Bnkcr2) [25]. Furthermore, the application of S. indica to tobacco seedlings increased the expression of many genes involved in plant metabolism, including nitropropane dioxygenase (2NpdO), glucan-water dikinase (GWD), and nitrate reductase (Nia2) [39] (Figure 5).
Therefore, S. indica has an impact on a variety of plant physiological and biochemical processes, which are modulated at the molecular level through genes regulation. The integrated changes in plant physiological, biochemical, and molecular processes that are affected by the endophytic fungus is responsible for enhancing plant growth and development.

4. Influence of S. indica on Biotic and Abiotic Stress

Plants are exposed to various forms of stressful conditions that limit their growth, development, and production, due to the formation of reactive oxygen species (ROS), e.g., hydroxyl (OH·−), superoxide (O2·−), and hydrogen peroxide (H2O2). These stresses are classified as biotic and abiotic stresses. Biotic stresses include pathogen infection, whereas abiotic stresses include drought, salinity, heat, and cold stress [110]. Nevertheless, plants are bestowed with various protective barriers against these stresses, such as the production of secondary metabolites, phytohormones, toxic substances that halt the enzymatic activity of pathogens, and some physical barriers, such as cell walls and cuticles, to limit pathogen entry [9]. Moreover, plants produce various solutes, such as proline, sucrose, polyols, glycine, and betaine, as well as antioxidative enzymes, such as catalase, ascorbate peroxidase, and superoxide dismutase as a protection against various stresses. However, ROS production can be higher under various stresses than the plant’s defence system, leading to oxidative stresses [111]. Therefore, controlling these stresses is essential to preventing further crop losses.
S. indica has been reported to alleviate both biotic and abiotic stresses upon colonisation, protecting the host plants from the adverse effects of stressors [14].

4.1. Biotic Stress Management by S. indica

S. indica, as one of the most promising microorganisms, can protect plants against various stresses by regulating multiple processes, such as the synthesis of antioxidants, secondary metabolites, osmolytes, defence-related phytohormones, etc. [9]. Resistance to biotic stresses, such as bacterial, viral, and fungal diseases in plant hosts have been reported following S. indica colonisation [9,12,112]. Extensive evidence is available to support S. indica as a biocontrol agent, such as resistance against the black spot of cabbage caused by Alternaria brassicicola [3], Stemphylium leaf blight of onion [28], Rhizoctonia solani in tomato [113], Verticillium wilt caused by Verticillium dahliae [112], and root rot caused by Fusarium graminearum [114]. The effect of S. indica on biotic stress in various crops is summarised in Table 2.
To develop resistance against various pathogens, S. indica builds molecular relations with the host plants in addition to following physiological and biochemical pathways [121]. Many hypotheses have been proposed to explain the use of S. indica as a biocontrol agent. As suggested by Li et al. [122], S. indica follows indirect and complex mechanisms to trigger pathogen resistance in plants, such as intervention in MAMPs, which include oxidative burst and upregulation of defence-related genes. Moreover, Li et al. [122] reported the involvement of S. indica in mitogen-activated protein (MAP) kinase and phenylpropanoid biosynthesis pathways, which are responsible for plant immunity. Therefore, S. indica triggers an immune response in the host plant by modifying the transcriptomic changes induced by pathogens. In the case of leaf pathogens, systemic resistance was triggered in tomato, maize, wheat, barley, and Arabidopsis. It has been associated with jasmonic acid (JA)-dependent signalling [123], synthesis of antioxidants [77,124], reducing H2O2 content [99], elevating relative water content, increasing the membrane stability index [122], and upregulating the gene expression in defence-related pathways [115,125]. However, the fungus, induces direct antioxidant action against root pathogens [28]. Moreover, it was established that under stress conditions, S. indica activated antioxidant capacity in the host plant by increasing the concentration of antioxidant enzymes, such as ascorbate peroxidase (APX), superoxide dismutase (SOD), glutathione peroxidase (GPX), and catalase (CAT). These enzymes, associated with induced systemic resistance, are of key importance in defence mechanisms. They cause the detoxification of reactive oxygen species generated by pathogens and thus act as a barrier against pathogen attacks [28,69]. Furthermore, Roylawar et al. [28] reported a decrease in malondialdehyde accumulation, resulting in protection against ROS damage. Peroxidase, on the other hand, can also stimulate lignin and phenol biosynthesis, which hinders the growth of the pathogen [126]. In addition, S. indica alters the synthesis of defence hormones, such as ethylene, thus protecting the host plant against different pathogens [9].
S. indica also mediates the upregulation of defence-related genes, such as the lipoxygenase (LOX) gene, leading to increased expression of AcLOX1 and AcLOX2 lipoxygenases and AcCHI chitinase, which are considered essential for salicylic acid (SA) and jasmonic acid (JA) pathways, thereby regulating induced systemic resistance (ISR) [28,127,128]. It was suggested that the application of S. indica upregulated the expression of WRKY genes involved in defence pathways, resulting in resistance against early blight disease in tomatoes and sharp eyespot and Fusarium head blight in wheat through modulating the expression of pathogenesis-related (PR) genes [115,122]. Moreover, a recent discovery by Ntana et al. [13] reported an upregulation of the expression of the terpenoid synthase gene (SiTPS) upon the colonisation of S. indica in tomato roots. It resulted in the production of viridiflorol, which inhibits the growth of the phytopathogenic fungus Colletotrichum truncatum. In S. indica-colonised taro crop, Lakshmipriya et al. [69] found activation of defence-related genes, such as senescence-associated genes, as well as genes encoding cytochrome P450, Delta (12) oleic acid desaturase FAD2, and calcium-dependent protein kinases (CDPKs), resulting in the reduction in taro leaf blight. Figure 6 depicts the effect of S. indica on host plants under biotic stress.
Based on these findings, it is reasonable to conclude that S. indica has a favourable impact on disease tolerance in a range of plants and might be exploited to be developed into an effective biocontrol agent.

4.2. Abiotic Stress Management by S. indica

Crop plants are also exposed to various types of abiotic stresses, such as drought, floods, salinity, heavy metal toxicity, and low-high temperatures, which affect crop development and productivity [129]. S. indica has proven to minimise the abiotic stress levels in several crops, as presented in Table 3. The mechanism involves the establishment of a ROS scavenging system [27,51,68,121,130], the activation of genes, such as those encoding dehydration responsive element binding proteins 2A (DREB2A) and calcineurin B-like protein (CBL1), responsive-to-dehydration 29A (RD29A) gene, and other defence-related genes (PR, LOX2, and ERF1 genes), as well as the promotion of the production of organic osmolytes, such as proline [14,26] and glycine betaine [14]. However, Abdelaziz et al. [131] reported a decrease in proline content in S. indica-treated plants, which might be attributed to an improvement in plant response toward drought stress following the application of S. indica. It was further proposed that S. indica colonisation not only increased the plant’s hormonal and metabolic activity, but also controlled the ionic homeostasis of sodium (Na+) and potassium (K+) ions. Therefore, protecting the plants against stress [132]. Figure 7 summarises the impact of S. indica on plants under abiotic stress.

4.2.1. Drought Stress

One of the most devastative abiotic stresses, causing significant crop loss is a drought stress which needs to be mitigated. In this context, several studies have demonstrated the positive effects of S. indica on various crops under drought stress conditions, including higher water use efficiency (WUE), nutrient uptake, and rise in chlorophyll content by upregulating chlorophyll biosynthesis genes [44,51,131,133]. Additionally, it increased the activities of antioxidant enzymes, such as catalase (CAT) and peroxidase (POD) [101,131,134]. Upregulation of the ROS scavenging system, accumulation of soluble proteins, increases in sugars and amino acids, such as proline [26,27,101,135], as well as changes in hormones, such as an increase in indole-3-acetic acid (IAA) content, a decrease in ABA and ethylene [131], and a reduction in malondialdehyde (MDA) levels [44,131] were also reported.
Furthermore, S. indica improves morphological parameters under drought conditions, such as root length, shoot length, grain yield and biomass, thus confirming resistance against drought in several crops, including globe artichoke [136], maize [137], Chinese cabbage [68], walnut [27], rice [44] and sesame [138]. Various drought-related genes, such as responsive-to-dehydration 29A gene (RD29A), (ANAC072), phospholipase D delta (PLDδ), and those encoding early response to dehydration 1 (ERD1), dehydration-response element binding protein 2A (DREB2A), salt and drought-induced ring finger 1 (SDIR1), calcineurin B-like protein (CBL1), CBL-interacting protein kinase 3 (CIPK3), and histone acetyltransferase (HAT) were upregulated following the application of S. indica, resulting in drought stress tolerance in the Arabidopsis plant [39]. Moreover, Azizi et al. [50] reported enhancement in the expression of late embryogenesis abundant 14 (LEA14), a dehydrin (TAS14) and pyrroline-5-carboxylate synthase (P5CS) gene under drought stress after the application of S. indica in tomato. Upregulation of these genes is known to ameliorate drought tolerance in plants. In addition to gene regulation, it has been observed that S. indica increased the calcium sensing regulator (CAS) protein, which regulates the stomatal movements in Chinese cabbage leaves, thus inducing drought tolerance [68].

4.2.2. Cold Stress

Tolerance to cold stress has been reported in certain studies following the application of S. indica to host plants. According to Li et al. [139], banana crops responded positively to S. indica colonisation under cold stress due to accumulating osmolytes, activating antioxidant capacity, and increasing the expression of the cold stress-related genes in banana leaves. S. indica colonisation has also resulted in cold stress tolerance in Arabidopsis by increasing ascorbic acid content, proline content, phytohormone levels, such as brassinolide (BR), abscisic acid (ABA), and regulating cold stress-related genes, such as C-repeat-binding factor (CBFs), cold-regulated genes (CORs), brassinazole-resistant (BZR1), senescence-associated gene (SAG1), and pyrabactin resistance 1-like (PYL6). Moreover, lower H2O2 and malondialdehyde (MDA) levels were recorded in Arabidopsis seedlings following S. indica colonisation [140]. Furthermore, S. indica increased the yield of barley crops under low temperatures by enhancing nutrient uptake [42].

4.2.3. Salinity Stress

Salinity stress is detrimental to agricultural production and results in massive crop losses. However, the application of S. indica has been reported to promote plant growth under salt stress by enhancing chlorophyll content, biomass, root growth, and antioxidant activity in Arabidopsis thaliana, Cucumis melo, and Medicago truncatula [90,141,142]. Singh et al. [143] reported that S. indica increased antioxidant enzymes, carotenoid, α-tocopherol, and proline levels while decreasing relative membrane permeability, lipid peroxidation, and lipoxygenase enzyme activity in wheat under salinity stress. S. indica has shown to mitigate the salt stress in other crops by increasing proline content [37]. Furthermore, salt tolerance induced by S. indica is mediated by the high osmolarity glycerol (HOG) mitogen-activated protein (MAP) kinase signalling pathway, in which the upregulation of genes, such as SiHOG1 plays an important role in root colonisation and improves the condition of the host plant under salt stress [144]. In barley crops, S. indica governs the ethylene biosynthesis pathway and carbohydrate and nitrogen metabolism, thus resulting in salt tolerance [145]. Moreover, salinity stress was ameliorated in Chinese cabbage by modulation of phytohormones, such as salicylic acid and gibberellic acid, as well as by enhancing the activities of antioxidant enzymes [146]. Furthermore, this endophytic fungus conferred resistance to salt stress in tomato seedlings owing to its ability to boost the uptake of nutrients, such as nitrogen, phosphorus, and calcium, and to enhance K+/Na+ homoeostasis by regulating the expression of various genes, such as sodium/hydrogen exchanger 2 (NHX2), Na+/H+ antiporter (SOS1), and cyclic nucleotide-gated channel (CNGC15). These genes regulate the function of aquaporins, thus maintaining water status in plants [147]. Additionally, Boorboori et al. [148] recently highlighted the relevance of S. indica in resisting drought and salt stress in plants, consequently increasing agricultural output.

4.2.4. Heavy Metal Stress

Alleviation of heavy metal stress by application of S. indicia has been reported in several host plants by reducing the concentration and absorption of heavy metals, such as lead, arsenic, and cadmium in various plants, such as sunflower, wheat, barley, and alfalfa [41,52,149,150,151]. Moreover, the concentration of lead was alleviated in the shoots of the sweet basil plant with the application of S. indica [152]. This effect of reducing the concentration of heavy metals by S. indica colonisation can be attributed to the binding of these heavy metals to the cell wall of fungal hyphae, thereby reducing their uptake into the aerial plant parts [60]. Mohd et al. [153] suggested that the compartmentalisation, adsorption, and precipitation of these metals are thought to limit their mobility, resulting in decreased translocation into the shoot.
Additionally, a significant improvement in growth parameters has been recorded in host plants treated with S. indica under metal toxicity conditions, such as an increase in photosynthetic rate and pigments, biomass, antioxidant enzymes, flavonoids, and proline content, and a reduction in H2O2 and MDA content in the host plant, including rice [108], wheat [150], sunflower [149], and tobacco [154]. Moreover, an increase in the expression of stress-related genes, such as phytochelatin synthase-related genes (TaPCS1, oas1, Gsh2), GPX, and heat shock proteins (Hsp70) was reported in tobacco under cadmium stress in S. indica colonised plants [154]. Furthermore, S. indica can act as a detoxifying agent in heavy metal-contaminated soils by immobilising these metals in the root zone, limiting their release, and improving soil quality [80].
Table
Table 3. Effects of S. indica on host plants under abiotic stress conditions.
Table 3. Effects of S. indica on host plants under abiotic stress conditions.
Host PlantAbiotic StressesEffect of S. indica on Host Plant under Abiotic Stress ConditionsReference
Eggplant (Solanum melongena)DroughtIncrease in root and shoot length, biomass, proline, chlorophyll, and water content, catalase activity, and guaiacol peroxidase activity-[155]
Chinese cabbage (Brassica oleracea)DroughtIncrease in chlorophyll content, antioxidant enzyme activity, drought-related genes expression, and CAS protein-[68]
Globe artichoke (Cynara scolymus)DroughtIncrease in plant biomass, photosynthetic pigment, carotenoid, proline, and potassium levels in leavesDecrease in sodium content[136]
Tomato (Lycopersicon esculentum)DroughtIncrease in shoot fresh and dry weight, proline and relative water content-[50]
Rice (Oryza sativa)DroughtIncrease in grain yield, stomatal closure, leaf surface temperature, antioxidant enzyme activity-[44]
Increase in seedling growth, seedling biomass, uptake of phosphorus and zinc, chlorophyll fluorescence, proline, and total antioxidant capacity in leaves-[156]
Maize (Zea mays)Drought and mechanical stressIncrease in plant adaptability, root length and volume, relative water content, leaf water potential, and chlorophyll content-[26]
Maize (Zea mays)DroughtIncrease in leaf size, root length, and number of tap roots-[101]
Increase in oxidative potential of the roots, and expression of genes responsible for hormonal functions-[107]
Barley (Hor deumvulgare)DroughtIncrease in fresh and dry weight of plant, root growth, number of tillers, proteins involved in photosynthesis, and antioxidant enzyme activity-[157]
Increase in activity of photosystem and electron transport chain and accumulation of drought responsive proteins-[135]
Finger millets (Eleusine coracana)DroughtIncrease in plant growth, biomass, total chlorophyll, proline, total and soluble sugar content Decrease in MDA and hydrogen peroxide content[158]
Walnut (Juglans regia)DroughtIncrease in plant height, total fresh biomass, root/shoot ratio, relative growth rate, leaf relative water and chlorophyll content, gas exchange parameters, photochemical efficiency, photochemical quenching, and photosystem II quantum yield, osmotic adjustment and antioxidant activity-[27]
Quinoa (Chenopodium quinoa)DroughtIncrease in total biomass, water balance, and leaf gas exchange-[51]
Aloe vera (Aloe barbadensis)SalinityIncrease in plant biomass, shoot and root length, number of shoots and roots, chlorophyll, gel, phenols, flavonoid, and aloin content, and radical scavenging activity-[78]
Gerbera (Gerbera jamesonii)SalinityIncrease in plant biomass, photosynthesis, and salt toleranceDecrease in MDA and hydrogen peroxide content[86]
Melon (Cucumis melo)SalinityIncrease in antioxidant content, dry weightDecrease in salinity stress[90]
Sweet basil (Ocimum basilicum)SalinityIncrease in plant dry weight area, essential oil content, and yield-[85]
Tomato (Lycopersicon esculentum)SalinityIncrease in plant growth, photosynthetic pigments, proline and glycine betaine, potassium content, water potential, net photosynthesis, stomatal conductance, and transpiration rate-[147]
Arabidopsis (Arabidopsis thaliana)Salinity-Decrease in sodium content[159]
Rice (Oryza sativa)SalinityIncrease in fresh weight, dry weight, length of root and shoot, photosynthetic pigment, and salt tolerance-[37]
Increase in proline concentration and antioxidant enzyme activity, potassium concentration, salt toleranceDecrease in MDA and sodium ion concentration[160]
Barley (Hordeum vulgare)SalinityIncrease in plant growth, ascorbic acid activity of antioxidant enzymes, metabolic heat efflux, and fatty acid desaturation in leavesDecrease in NaCl-induced lipid peroxidation[161]
Banana (Musa acumunata)ColdIncrease in superoxide dismutase (SOD) and catalase (CAT) activity and soluble sugar (SS) and proline contentDecrease in MDA and hydrogen peroxide content[139]
Barley (Hordeum vulgare)ColdIncrease in grain dry weight, nutrient uptake, and early flowering-[42]
Arabidopsis (Arabidopsis thaliana)ColdIncrease in soluble proteins, proline and ascorbic acid, cold tolerance-[140]
Banana (Musa acumunata)High temperatureIncrease in proline content, MDA, hydrogen peroxide and ABA, and resistance to high temperatureDecrease in IAA and GA content in banana leaves[162]
Heavy metal stress
Artemisia (Artemisia annum)ArsenicIncrease in plant growth, biomass, flavonoids, artemisinin, super oxidase dismutase, peroxidase activity, phenolic acid, and phenolic compounds-[80]
Wheat (Triticum aestivum)CadmiumIncrease in plant growth, photosynthetic pigments, antioxidant enzymes, proline contentDecrease in cadmium accumulation in stem and root[150]
Rice (Oryza sativa)ArsenicIncrease in plant growth, chlorophyll contentDecrease in MDA content and arsenic uptake[108]
CadmiumIncrease in nutrient uptake, photosynthesis, antioxidant enzyme activity, maintenance of cellular structuresDecrease in cadmium concentration in shoot[163]
Barley (Hordeum vulgare)Arsenic Increase in iron concentrationDecrease in arsenic concentration in shoot[151]
Sunflower (Helianthus annuus)CadmiumIncrease in plant growth, chlorophyll content, proline content, Fv/Fm, and electron transport rate valuesDecrease in cadmium content in plant[149]
Alfalfa (Medicago sativa)CadmiumIncrease in growth rate, shoot dry weight, antioxidant enzyme activityDecrease in cadmium concentration in shoot[84]
Tobacco (Nicotiana tabacum)CadmiumIncrease in chlorophyll content, antioxidant enzymes, and proline content, enhanced expression of stress-related phytochelatin biosynthesis genesDecrease in MDA[154]
Soybean (Glycine max)CadmiumIncrease in plant growth, dry weight, shoot height and photosynthesis, transpiration ratio and stomatal conductance, and antioxidant activity Decrease in cadmium content[164]
According to research on S. indica, this endophytic fungus could serve as a potential biofertiliser, reducing various biotic and abiotic challenges while enhancing plant development and, eventually, agricultural productivity.

5. Interaction of Serendipita indica with Nanoparticles

Nanotechnology, an emerging science, is gaining immense attention in the field of agriculture due to its small size and higher efficiency over bulk materials [165,166]. Therefore, integrating this technology with beneficial microorganisms could unfold novel approaches for improving agricultural outputs. It was reported that applying S. indica and copper nanoparticles together increased plant growth, making the combination useful as a nanofertiliser [165]. Varma et al. [167] developed nano-embedded S. indica, as a potential biofertiliser, including a combination of S. indica and nanoparticles, such as zinc oxide, titanium oxide, and carbon nanotubes. The interaction between nanoparticles and the fungus resulted in increased fungal biomass, spore number, thicker hyphae, and fewer vacuoles [167]. Rane et al. [168] suggested the combined application of calcium phosphate nanoparticles with S. indica to be a more efficient plant growth enhancer than a sole application of nanoparticles or endophytic fungus. Another study revealed that the combined application of nitrogen nanoparticles with S. indica did not show significant improvement in the treated plants, but the application of S. indica alone was found to be better than nanoparticles [3]. However, insufficient understanding of the usage and application of nanoparticles in agriculture might lead to significant risks to humans and the environment. These particles can penetrate deep into the biological system, resulting in serious threats to both mammals and the environment [169]. Moreover, organic nanoparticles produced biologically pose less risk than those produced using chemical and physical methods [170]. Nevertheless, each technology has its pros and cons; therefore, the vital factor is using the optimum dosage and appropriate techniques for applying nanotechnology in the agricultural sector to control the risks associated with nanoparticles [171].
As a result, additional research on the beneficial application of nanomaterials and plant growth-promoting microorganisms is required to develop more efficient and practical nano biofertilisers for agricultural production.

6. Conclusions

Based on the above discussion, we presented the influence of the beneficial endophytic fungus on plant growth, quality, and yield, thus improving global food security and the nutritional prospects of the produce. S. indica ensures environmental protection while being economical at the same time. In addition, the protection of plants from biotic and abiotic stresses is attained through the application of S. indica. Moreover, its wide range of host acceptability and its axenic culturing ability have made it one of the promising beneficial microorganisms in the field of agriculture. However, a gap still exists between the research and its widespread release, which needs to be bridged by focusing on the nutrient uptake mechanisms mediated by S. indica and conducting in-depth research on molecular mechanisms that would create opportunities for the commercial viability of endophytic fungus S. indica.

Author Contributions

R.P. and S.S. contributed to the conception and design of the review manuscript. S.S. performed the literature research and data analysis. The manuscript was written by S.S., R.P. and A.S. critically revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the project of Internal grant agency of Mendel university in Brno No. IGA-ZF/2021-SI1004 Cultivation techniques and inoculation of vegetables by symbiotic microbes. Microscopic analyses were conducted on infrastructure supported by project OP VVV CZ.02.1.01/0.0/0.0/16_017/0002334 Research infrastructure for young scientists financed from the structural funds of EU and Ministry of education of the Czech Republic.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data generated or analysed during this study are included in this published article.

Acknowledgments

Authors are thankful to Sarka Frankova for providing help with sample preparation and microscopy.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

ABAabscisic acid
AMFarbuscular mycorrhizal fungi
APXascorbate peroxidase
AUXauxin
BRbrassinolide
CAScalcium-sensing
CATcatalase
CKcytokinin
ETIeffector-triggered immunity
Ftfluorescence level
Fv/Fmvariable fluorescence/maximum fluorescence
GAgibberellic acid
GPXglutathione peroxidase
GSHglutathione
H2O2hydrogen peroxide
HOGhigh osmolarity glycerol
Hspheat shock proteins
IAAindole-3-acetic acid
INVinvertase
ISRinduced systemic resistance
JAjasmonic acid
Kpotassium
MAMPs or PAMPsmicrobe- or pathogen-associated molecular patterns
MAPmitogen-activated protein
MDAmalondialdehyde
MMNmodified Melin-Norkrans
Nnitrogen
Nasodium
NDVInormalized difference vegetation index
OH·−hydroxyl
O2·−superoxide
Pphosphorus
PCSphytochelatin biosynthesis
PDApotato dextrose agar
PDBpotato dextrose broth
PTphosphate transporter
PODperoxidase
PRpathogenesis-related
ROSreactive oxygen species
SAsalicylic acid
SODsuperoxide dismutase
SUSsucrose synthase
TCAtricarboxylic acid cycle
WUEwater use efficiency

References

  1. Jacoby, R.; Peukert, M.; Succurro, A.; Koprivova, A.; Kopriva, S. The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions. Front. Plant Sci. 2017, 8, 1617. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Koskey, G.; Mburu, S.W.; Awino, R.; Njeru, E.M.; Maingi, J.M. Potential use of beneficial microorganisms for soil amelioration, phytopathogen biocontrol, and sustainable crop production in smallholder agroecosystems. Fron. Sustain. Food Syst. 2021, 5, 606308. [Google Scholar] [CrossRef]
  3. Saleem, S.; Bytešníková, Z.; Richtera, L.; Pokluda, R. The Effects of Serendipita indica and Guanidine-Modified Nanomaterial on Growth and Development of Cabbage Seedlings and Black Spot Infestation. Agriculture 2021, 11, 1295. [Google Scholar] [CrossRef]
  4. Garg, M.; Sharma, N.; Sharma, S.; Kapoor, P.; Kumar, A.; Chunduri, V.; Arora, P. Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world. Front. Nutr. 2018, 5, 12. [Google Scholar] [CrossRef]
  5. Meena, V.S.; Meena, S.K.; Verma, J.P.; Kumar, A.; Aeron, A.; Mishra, P.K.; Bisht, J.K.; Pattanayak, A.; Naveed, M.; Dotaniya, M.L. Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: A review. Ecol. Eng 2017, 107, 8–32. [Google Scholar] [CrossRef]
  6. Bingzhu, Y.; Yanbin, W.; Xin, Z.; Ruoqing, Z.; Jinzhong, W.; Zhang, C.; Rahman, K.; Qin, L.; Han, T.; Zheng, C. Beneficial effects of endophytic fungi from the Anoectochilus and Ludisia species on the growth and secondary metabolism of Anoectochilus Roxburghii. ACS Omega 2020, 5, 3487–3497. [Google Scholar] [CrossRef] [Green Version]
  7. Yang, L.; Zou, Y.N.; Tian, Z.H.; Wu, Q.S.; Kuča, K. Effects of beneficial endophytic fungal inoculants on plant growth and nutrient absorption of trifoliate orange seedlings. Sci. Hortic. 2021, 277, 109815. [Google Scholar] [CrossRef]
  8. Verma, S.; Varma, A.; Rexer, K.H.; Hassel, A.; Kost, G.; Sarbhoy, A.; Bisen, P.; Bütehorn, B.; Franken, P. Piriformospora indica, gen. et sp. nov., a new root-colonising fungus. Mycologia 1998, 90, 896–903. [Google Scholar] [CrossRef]
  9. Jha, Y.; Yadav, A.N. Piriformospora indica: Biodiversity, Ecological Significances, and Biotechnological Applications for Agriculture and Allied Sectors. In Industrially Important Fungi for Sustainable Development; Springer: Cham, Switzerland, 2021; pp. 363–392. [Google Scholar] [CrossRef]
  10. Pham, G.H.; Kumari, R.; Singh, A.; Malla, R.; Prasad, R.; Sachdev, M.; Kaldorf, M.; Buscot, F.; OelmŘller, R.; Hampp, R.; et al. Axenic culture of symbiotic fungus Piriformospora indica. In Plant Surface Microbiology; Springer: Berlin/Heidelberg, Germany, 2008; pp. 593–613. [Google Scholar] [CrossRef]
  11. Attri, M.K.; Varma, A. Comparative Study of Growth of Piriformospora indica by using different Sources of Jaggery. J. Pure Appl. Microbiol. 2018, 12, 933–942. [Google Scholar] [CrossRef]
  12. Qiang, X.; Weiss, M.; Kogel, K.H.; Schafer, P. Piriformospora indica—A mutualistic basidiomycete with an exceptionally large plant host range. Mol. Plant. Pathol. 2011, 13, 508–518. [Google Scholar] [CrossRef]
  13. Ntana, F.; Bhat, W.W.; Johnson, S.R.; Jørgensen, H.J.; Collinge, D.B.; Jensen, B.; Hamberger, B. A sesquiterpene synthase from the endophytic fungus Serendipita indica catalyzes formation of viridiflorol. Biomolecules 2021, 11, 898. [Google Scholar] [CrossRef]
  14. Gill, S.S.; Gill, R.; Trivedi, D.K.; Anjum, N.A.; Sharma, K.K.; Ansari, M.W.; Tuteja, N. Piriformospora indica: Potential and significance in plant stress tolerance. Front. Microbiol. 2016, 7, 332. [Google Scholar] [CrossRef] [Green Version]
  15. Bleša, D. Orchideoid Mycorrhizal Fungi as Endophytes. Diploma Thesis, Masaryk University, Brno, Czech Republic, 2018. [Google Scholar]
  16. Deshmukh, S.; Hückelhoven, R.; Schäfer, P.; Imani, J.; Sharma, M.; Weiss, M.; Kogel, K.H. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Natl. Acad. Sci. USA 2006, 103, 18450–18457. [Google Scholar] [CrossRef] [Green Version]
  17. Mensah, R.A.; Li, D.; Liu, F.; Tian, N.; Sun, X.; Hao, X.; Cheng, C. Versatile Piriformospora indica and its potential applications in horticultural crops. Hortic. Plant J. 2020, 6, 111–121. [Google Scholar] [CrossRef]
  18. Abin, N.; Rokni, N.; Shafeinia, A.R.; Borhan, M.H.; Huyghe, C. Quantification of endophyte Serendipita indica in Brassica napus roots by qPCR. Crop. Pasture Sci. 2021, 72, 985–993. [Google Scholar] [CrossRef]
  19. Rokni, N.; Alizadeh, H.S.; Bazgir, E.; Darvishnia, M.; Mirzaei-Najafgholi, H. The tripartite consortium of Serendipita indica, Trichoderma simmonsii, and bell pepper (Capsicum annum). Biol. Control 2021, 158, 104608. [Google Scholar] [CrossRef]
  20. Vadassery, J.; Ranf, S.; Drzewiecki, C.; Mithöfer, A.; Mazars, C.; Scheel, D.; Lee, J.; Oelmüller, R. A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J. 2009, 59, 193–206. [Google Scholar] [CrossRef]
  21. Nivedita, Verma, P.K.; Upadhyaya, K.C. Lectin Protein Kinase Is Induced in Plant Roots in Response to the Endophytic Fungus, Piriformospora indica. Plant Mol. Biol. Rep. 2017, 35, 323–332. [Google Scholar] [CrossRef]
  22. Camehl, I.; Sherameti, I.; Seebald, E.; Johnson, J.M.; Oelmüller, R. Role of defence compounds in the beneficial interaction between Arabidopsis thaliana and Piriformospora indica. In Piriformospora Indica; Springer: Berlin/Heidelberg, Germany, 2013; pp. 239–250. [Google Scholar] [CrossRef]
  23. Unnikumar, K.R.; Sree, K.S.; Varma, A. Piriformospora indica: A versatile root endophytic symbiont. Symbiosis 2013, 60, 107–113. [Google Scholar] [CrossRef]
  24. Singhal, U.; Prasad, R.; Varma, A. Piriformospora indica (Serendipita indica): The Novel Symbiont. In Mycorrhiza—Function, Diversity, State of the Art; Varma, A., Prasad, R., Tuteja, N., Eds.; Springer: Cham, Switzerland, 2017; pp. 349–364. [Google Scholar] [CrossRef]
  25. Su, Z.Z.; Wang, T.; Shrivastava, N.; Chen, Y.Y.; Liu, X.; Sun, C.; Yin., Y.; Gao, Q.K.; Lou, B.G. Piriformospora indica promotes growth, seed yield and quality of Brassica napus L. Microbiol. Res. 2017, 199, 29–39. [Google Scholar] [CrossRef]
  26. Hosseini, F.; Mosaddeghi, M.R.; Dexter, A.R.; Sepehri, M. Maize water status and physiological traits as affected by root endophytic fungus Piriformospora indica under combined drought and mechanical stresses. Planta 2018, 247, 1229–1245. [Google Scholar] [CrossRef] [PubMed]
  27. Liu, B.; Jing, D.; Liu, F.; Ma, H.; Liu, X.; Peng, L. Serendipita indica alleviates drought stress responses in walnut (Juglans regia L.) seedlings by stimulating osmotic adjustment and antioxidant defence system. Appl. Microbiol. Biotechnol. 2021, 105, 8951–8968. [Google Scholar] [CrossRef] [PubMed]
  28. Roylawar, P.; Khandagale, K.; Randive, P.; Shinde, B.; Murumkar, C.; Ade, A.; Singh, M.; Gawande, S.; Morelli, M. Piriformospora indica Primes Onion Response against Stemphylium Leaf Blight Disease. Pathogens 2021, 10, 1085. [Google Scholar] [CrossRef] [PubMed]
  29. Upadhyaya, C.P.; Gururani, M.A.; Prasad, R.; Verma, A. A Cell Wall Extract from Piriformospora indica Promotes Tuberization in Potato (Solanum tuberosum L.) Via Enhanced Expression of Ca+2 Signaling Pathway and Lipoxygenase Gene. Appl. Biochem. Biotechnol. 2013, 170, 743–755. [Google Scholar] [CrossRef] [PubMed]
  30. Bagde, U.S.; Prasad, R.; Varma, A. Impact of culture filtrate of Piriformospora indica on biomass and biosynthesis of active ingredient aristolochic acid in Aristolochia Elegans Mart. Int. J. Biol. 2014, 6, 29. [Google Scholar] [CrossRef] [Green Version]
  31. Oelmüller, R.; Sherameti, I.; Tripathi, S.; Varma, A. Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 2009, 49, 1–17. [Google Scholar] [CrossRef]
  32. Bagde, U.S.; Prasad, R.; Varma, A. Mass cultivation of Piriformospora indica in new brunswick fermenter and its formulation as biofertilizer. Asian J. Microbiol. Biotechnol. Environ. Sci. 2010, 12, 911–916. [Google Scholar]
  33. Shrivastava, S.; Varma, A. From Piriformospora indica to rootonic: A review. Afr. J. Microbiol. Res. 2014, 8, 2984–2992. [Google Scholar] [CrossRef] [Green Version]
  34. Barazani, O.; Benderoth, M.; Groten, K.; Kuhlemeier, C.; Baldwin, I.T. Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 2005, 146, 234–243. [Google Scholar] [CrossRef]
  35. Varma, A.; Bakshi, M.; Lou, B.; Hartmann, A.; Oelmüller, R. Piriformospora indica: A Novel Plant Growth-Promoting Mycorrhizal Fungus. Agric. Res. 2012, 1, 117–131. [Google Scholar] [CrossRef]
  36. Jisha, S.; Sabu, K.K.; Manjula, S. Multifunctional aspects of Piriformospora indica in plant endosymbiosis. Mycology 2019, 10, 182. [Google Scholar] [CrossRef] [Green Version]
  37. Jogawat, A.; Saha, S.; Bakshi, M.; Dayaman, V.; Kumar, M.; Dua, M.; Varma, A.; Oelmüller, R.; Tuteja, N.; Johri, A.K. Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal. Behav. 2013, 8, e26891. [Google Scholar] [CrossRef] [Green Version]
  38. Liu, B.; Liu, X.; Liu, F.; Ma, H.; Ma, B.; Zhang, W.; Peng, L. Growth improvement of Lolium multiflorum Lam. induced by seed inoculation with fungus suspension of Xerocomus badius and Serendipita indica. AMB Expr. 2019, 9, 145. [Google Scholar] [CrossRef]
  39. Sherameti, I.; Shahollari, B.; Venus, Y.; Altschmied, L.; Varma, A.; Oelmüller, R. The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J. Biol. Chem. 2005, 280, 26241–26247. [Google Scholar] [CrossRef] [Green Version]
  40. Bagde, U.S.; Prasad, R.; Varma, A. Influence of culture filtrate of Piriformospora indica on growth and yield of seed oil in Helianthus annus. Symbiosis 2011, 53, 83–88. [Google Scholar] [CrossRef]
  41. Li, L.; Zhu, P.; Wang, X.; Zhang, Z. Phytoremediation effect of Medicago sativa colonised by Piriformospora indica in the phenanthrene and cadmium co-contaminated soil. BMC Biotechnol. 2020, 20, 20. [Google Scholar] [CrossRef]
  42. Murphy, B.R.; Doohan, F.M.; Hodkinson, T.R. Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis 2014, 62, 29–39. [Google Scholar] [CrossRef]
  43. Anith, K.N.; Aswini, S.; Varkey, S.; Radhakrishnan, N.V.; Nair, D.S. Root colonization by the endophytic fungus Piriformospora indica improves growth, yield and piperine content in black pepper (Piper nigurm L.). Biocatal. Agric. Biotechnol. 2018, 14, 15–220. [Google Scholar] [CrossRef]
  44. Tsai, H.J.; Shao, K.H.; Chan, M.T.; Cheng, C.P.; Yeh, K.W.; Oelmüller, R.; Wang, S.J. Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ROS scavenging systems. Plant Signal. Behav. 2020, 15, 1722447. [Google Scholar] [CrossRef]
  45. Dolatabadi, H.K.; Goltapeh, E.M.; Jaimand, K.; Rohani, N.; Varma, A. Effects of Piriformospora indica and Sebacina vermifera on growth and yield of essential oil in fennel (Foeniculum vulgare) under greenhouse conditions. J. Basic Microbiol. 2011, 51, 33–39. [Google Scholar] [CrossRef]
  46. Bakhshandeh, E.; Pirdashti, H.; Lendeh, K.S.; Zahra, G.; Khanghahi, M.Y.; Crecchio, C. Effects of plant growth promoting microorganisms inoculums on mineral nutrition, growth and productivity of rice (Oryza sativa L.). J. Plant Nutr. 2020, 43, 1643–1660. [Google Scholar] [CrossRef]
  47. Li, Q.; Kuo, Y.W.; Lin, K.H.; Huang, W.; Deng, C.; Yeh, K.W.; Chen, S.P. Piriformospora indica colonization increases the growth, development, and herbivory resistance of sweet potato (Ipomoea batatas L.). Plant Cell Rep. 2021, 40, 339–350. [Google Scholar] [CrossRef] [PubMed]
  48. Eliaspour, S.; Seyed, Sharifi, R.; Shirkhani, A. Evaluation of interaction between Piriformospora indica, animal manure and NPK fertilizer on quantitative and qualitative yield and absorption of elements in sunflower. Food Sci. Nutr. 2020, 8, 2789–2797. [Google Scholar] [CrossRef]
  49. Wang, H.; Zheng, J.; Ren, X.; Yu, T.; Varma, A.; Lou, B.; Zheng, X. Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistant to TYCLV. Plant Growth Regul. 2015, 76, 303–313. [Google Scholar] [CrossRef]
  50. Azizi, M.; Fard, E.M.; Ghabooli, M. Piriformospora indica affect drought tolerance by regulation of genes expression and some morphophysiological parameters in tomato (Solanum lycopersicum L.). Sci. Hortic. 2021, 287, 110260. [Google Scholar] [CrossRef]
  51. Hussin, S.; Khalifa, W.; Geissler, N.; Koyro, H.W. Influence of the root endophyte Piriformospora indica on the plant water relations, gas exchange and growth of Chenopodium quinoa at limited water availability. J. Agron. Crop. Sci. 2016, 203, 373–384. [Google Scholar] [CrossRef]
  52. Baghaie, A.H.; Aghilizefreei, A. Iron enriched green manure can increase wheat Fe concentration in Pb-polluted soil in the presence of Piriformospora indica (P. indica). Soil Sediment Contam. 2020, 29, 721–743. [Google Scholar] [CrossRef]
  53. Ahmadvand, G.; Hajinia, S. Effect of endophytic fungus Piriformospora indica on yield and some physiological traits of millet (Panicum miliaceum) under water stress. Crop Pasture Sci. 2018, 69, 594–605. [Google Scholar] [CrossRef]
  54. Johnson, J.M.; Alex, T.; Oelmüller, R. Piriformospora indica: The versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J. Trop. Agric 2014, 52, 103–122. [Google Scholar]
  55. Serfling, A.; Wirsel, S.G.; Lind, V.; Deising, H.B. Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 2007, 97, 523–531. [Google Scholar] [CrossRef] [Green Version]
  56. Khalid, M.; Rahman, S.U.; Huang, D. Molecular mechanism underlying Piriformospora indica-mediated plant improvement/protection for sustainable agriculture. Acta Biochim. Biophys. Sin. 2019, 51, 229–242. [Google Scholar] [CrossRef]
  57. Swetha, S.; Padmavathi, T. Study of acid phosphatase in solubilization of inorganic phosphates by Piriformospora indica. Pol. J. Microbiol. 2016, 65, 7. [Google Scholar] [CrossRef] [Green Version]
  58. Wu, M.; Wei, Q.; Xu, L.; Li, H.; Oelmüller, R.; Zhang, W. Piriformospora indica enhances phosphorus absorption by stimulating acid phosphatase activities and organic acid accumulation in Brassica napus. Plant Soil 2018, 432, 333–344. [Google Scholar] [CrossRef]
  59. Das, J.; Ramesh, K.V.; Maithri, U.; Mutangana, D.; Suresh, C.K. Response of aerobic rice to Piriformospora indica. Indian J. Exp. Biol. 2014, 52, 237–251. Available online: http://nopr.niscpr.res.in/handle/123456789/27348 (accessed on 10 February 2022).
  60. Baghaie, A.H.; Aghili, F. Contribution of Piriformospora indica on improving the nutritional quality of greenhouse tomato and its resistance against cu toxicity after humic acid addition to soil. Environ. Sci. Pollut. Res. 2021, 28, 64572–64585. [Google Scholar] [CrossRef]
  61. Moreira, B.C.; Mendes, F.C.; Mendes, I.R.; Paula, T.A.; Junior, P.P.; Salomão, L.C.; Stürmer, S.L.; Otoni, W.C.; Kasuya, M.C. The interaction between arbuscular mycorrhizal fungi and Piriformospora indica improves the growth and nutrient uptake in micropropagation-derived pineapple plantlets. Sci. Hortic. 2015, 14, 183–192. [Google Scholar] [CrossRef]
  62. Prasad, D.; Verma, N.; Bakshi, M.; Narayan, O.P.; Singh, A.K.; Dua, M.; Johri, A.K. Functional characterization of a magnesium transporter of root endophytic fungus Piriformospora indica. Front. Microbiol. 2019, 9, 3231. [Google Scholar] [CrossRef] [Green Version]
  63. Narayan, O.P.; Verma, N.; Singh, A.K.; Oelmüller, R.; Kumar, M.; Prasad, D.; Kapoor, R.; Dua, M.; Johri, A.K. Antioxidant enzymes in chickpea colonised by Piriformospora indica participate in defence against the pathogen Botrytis Cinerea. Sci. Rep. 2017, 7, 13553. [Google Scholar] [CrossRef] [Green Version]
  64. Padash, A.; Shahabivand, S.; Behtash, F.; Aghaee, A. A practicable method for zinc enrichment in lettuce leaves by the endophyte fungus Piriformospora indica under increasing zinc supply. Sci. Hortic. 2016, 213, 367–372. [Google Scholar] [CrossRef]
  65. Chen, Y.Y.; Lou, B.G.; Gao, Q.K.; Lin, F.C. Preliminary study on mechanisms of drought resistance in Brassica napus L. conferred by Piriformospora indica. Biocatal. Agric. Biotechnol. 2013, 21, 72–281. [Google Scholar]
  66. Gosal, S.K.; Sharma, M.; Gosal, S.S.; Chhibba, I.M.; Bhatnagar, K.; Varma, A. Bio hardening with Piriformospora indica improves survival rate, growth, iron uptake and cane yield of micro propagated sugarcane. Int. Sugar J. 2011, 113, 382–388. [Google Scholar]
  67. Abdelaziz, E.M.; Sabra, M.; Ali, M. Colonising Lettuce (Lactuca sativa L.) with Rhizophagus irregularis and Piriformospora indica fungi enhance plant yield and quality in sand soil. Middle East J. Appl. Sci. 2018, 8, 1173–1180. [Google Scholar]
  68. Sun, C.; Johnson, J.M.; Cai, D.; Sherameti, I.; Oelmüller, R.; Lou, B. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 2010, 167, 009–1017. [Google Scholar] [CrossRef] [PubMed]
  69. Lakshmipriya, P.; Nath, V.S.; Veena, S.S.; Anith, K.N.; Sreekumar, J.; Jeeva, M.L. Piriformospora indica, a cultivable endophyte for growth promotion and disease management in Taro (Colocasia esculenta (L.). J. Root Crops 2016, 42, 107–114. [Google Scholar]
  70. Waller, F.; Achatz, B.; Baltruschat, H.; Fodor, J.; Becker, K.; Fischer, M.; Heier, T.; Hückelhoven, R.; Neumann, C.; von Wettstein, D.; et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA 2005, 102, 13386–13391. [Google Scholar] [CrossRef] [Green Version]
  71. Arunkumar, G.P.; Shivaprakash, M.K. Influence of novel endophytic fungus Piriformospora indica on growth and yield of finger millet (Eleusine coracana G.) in combination with N fixer and P solubilizer. Int. J. Curr. Microbiol. App. Sci. 2017, 6, 1037–1042. [Google Scholar] [CrossRef]
  72. Tarte, S.H.; Kareppa, B.M.; Kharde, A.V. Impact of Piriformospora indica on growth and yield parameters of groundnut (Arachis hypogea L.). Pharma innov. 2019, 8, 766–769. [Google Scholar]
  73. Ray, J.G.; Valsalakumar, N. Arbuscular mycorrhizal fungi and Piriformospora indica individually and in combination with rhizobium on green gram. J. Plant Nutr. 2010, 33, 285–298. [Google Scholar] [CrossRef]
  74. Meena, K.K.; Mesapogu, S.; Kumar, M.; Yandigeri, M.S.; Singh, G.; Saxena, A.K. Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol. Fertil. Soils. 2010, 46, 169–174. [Google Scholar] [CrossRef]
  75. Bajaj, R.; Agarwal, A.; Rajpal, K.; Asthana, S.; Kumar, R.; Prasad, R.; Kharkwal, A.C.; Sherameti, I.; Oelmüller, R.; Varma, A. Co-cultivation of Curcuma longa with Piriformospora indica enhances the yield and active ingredients. Am. J. Curr. Microbiol. 2014, 2, 6–17. [Google Scholar]
  76. Dolatabadi, H.K.; Goltapeh, E.M.; Moieni, A.; Jaimand, K.; Sardrood, B.P.; Varma, A. Effect of Piriformospora indica and Sebacina vermifera on plant growth and essential oil yield in Thymus vulgaris in vitro and in vivo experiments. Symbiosis 2011, 53, 29–35. [Google Scholar] [CrossRef]
  77. Prasad, R.; Kamal, S.; Sharma, P.K.; Oelmüller, R.; Varma, A. Root endophyte Piriformospora indica DSM 11827 alters plant morphology, enhances biomass and antioxidant activity of medicinal plant Bacopa monniera. J. Basic Microbiol. 2013, 53, 1016–1024. [Google Scholar] [CrossRef]
  78. Sharma, P.; Kharkwal, A.C.; Abdin, M.Z.; Varma, A. Piriformospora indica improves micropropagation, growth and phytochemical content of Aloe vera L. plants. Symbiosis 2014, 64, 11–23. [Google Scholar] [CrossRef]
  79. Arora, M.; Saxena, P.; Choudhary, D.K.; Abdin, M.Z.; Varma, A. Dual symbiosis between Piriformospora indica and Azotobacter chroococcum enhances the artemisinin content in Artemisia annua L. World J. Microbiol. Biotechnol. 2016, 32, 19. [Google Scholar] [CrossRef]
  80. Rahman, S.U.; Khalid, M.; Kayani, S.I.; Tang, K. The ameliorative effects of exogenous inoculation of Piriformospora indica on molecular, biochemical and physiological parameters of Artemisia annua L. under arsenic stress condition. Ecotoxicol. Environ. Saf. 2020, 206, 111202. [Google Scholar] [CrossRef]
  81. Satheesan, J.; Narayanan, A.K.; Sakunthala, M. Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica. Mycorrhiza 2012, 22, 195–202. [Google Scholar] [CrossRef]
  82. Das, A.; Kamal, S.; Shakil, N.A.; Sherameti, I.; Oelmüller, R.; Dua, M.; Tuteja, N.; Johri, A.K.; Varma, A. The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signal. Behav. 2012, 7, 103–112. [Google Scholar] [CrossRef] [Green Version]
  83. Kumar, P.; Chaturvedi, R.; Sundar, D.; Bisaria, V.S. Piriformospora indica enhances the production of pentacyclic triterpenoids in Lantana camara L. suspension cultures Plant Cell Tissue Organ Cult. 2016, 125, 23–29. [Google Scholar] [CrossRef]
  84. Sepehri, M.; Khatabi, B. Combination of siderophore-producing bacteria and Piriformospora indica provides an efficient approach to improve cadmium tolerance in alfalfa. Microb. Ecol. 2020, 202, 717–730. [Google Scholar] [CrossRef]
  85. Keramati, S.; Pirdashti, H.; Babaeizad, V.; Dehestani, A. Essential oil composition of sweet basil (Ocimum basilicum L.) in symbiotic relationship with Piriformospora indica and paclobutrazol application under salt stress. Acta. Biol. Hung. 2016, 67, 412–423. [Google Scholar] [CrossRef] [Green Version]
  86. Chen, W.; Lin, F.; Lin, K.H.; Chen, C.; Xia, C.; Liao, Q.; Chen, S.P.; Kuo, Y.W. Growth promotion and salt-tolerance improvement of Gerbera jamesonii by root colonization of Piriformospora indica. Plant Growth Regul. 2021, 41, 1219–1228. [Google Scholar] [CrossRef]
  87. Lin, H.F.; Xiong, J.; Zhou, H.M.; Chen, C.M.; Lin, F.Z.; Xu, X.M.; Oelmüller, R.; Xu, W.F.; Yeh, K.W. Growth promotion and disease resistance induced in Anthurium colonised by the beneficial root endophyte Piriformospora indica. BMC Plant Biol. 2019, 19, 40. [Google Scholar] [CrossRef] [PubMed]
  88. Madaan, G.; Gosal, S.K.; Gosal, S.S.; Saroa, G.S.; Gill, M.I. Effect of microbial inoculants on the growth and yield of micropropagated banana (Musa indica) cv. Grand. Naine. J. Hortic. Sci. Biotechnol. 2013, 88, 643–649. [Google Scholar] [CrossRef]
  89. Yan, C.; Rizwan, H.M.; Liang, D.; Reichelt, M.; Mithöfer, A.; Scholz, S.S.; Oelmüller, R.; Chen, F. The effect of the root colonising Piriformospora indica on passion fruit (Passiflora edulis) development: Initial defence shifts to fitness benefits and higher fruit quality. Food Chem. 2021, 359, 129671. [Google Scholar] [CrossRef] [PubMed]
  90. Hassani, D.; Khalid, M.; Huang, D.; Zhang, Y.D. Morphophysiological and molecular evidence supporting the augmentative role of Piriformospora indica in mitigation of salinity in Cucumis melo L. Acta Biochim. Biophys. Sin. 2019, 51, 301–312. [Google Scholar] [CrossRef]
  91. Shekhawat, P.K.; Jangir, P.; Bishnoi, A.; Roy, S.; Ram, H.; Soni, P. Serendipita indica: Harnessing its versatile potential for food and nutritional security. Physiol. Mol. Plant Pathol. 2021, 116, 101708. [Google Scholar] [CrossRef]
  92. Mendoza-Mendoza, A.; Zaid, R.; Lawry, R.; Hermosa, R.; Monte, E.; Horwitz, B.A.; Mukherjee, P.K. Molecular dialogues between Trichoderma and roots: Role of the fungal secretome. Fungal Biol. Rev. 2018, 32, 62–85. [Google Scholar] [CrossRef]
  93. Mishra, D.; Kumar, A.; Tripathi, S.; Chitara, M.K.; Chaturvedi, P. Endophytic fungi as biostimulants: An efficient tool for plant growth promotion under biotic and abiotic stress conditions. In Biostimulants for Crops from Seed Germination to Plant Development; Academic Press: Cambridge, MA, USA, 2021; pp. 365–391. [Google Scholar] [CrossRef]
  94. Newman, M.A.; Sundelin, T.; Nielsen, J.T.; Erbs, G. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 2013, 4, 139. [Google Scholar] [CrossRef] [Green Version]
  95. Liu, T.; Liu, Z.; Song, C.; Hu, Y.; Han, Z.; She, J.; Fan, F.; Wang, J.; Jin, C.; Chang, J.; et al. Chitin-induced dimerization activates a plant immune receptor. Science 2012, 336, 1160–1164. [Google Scholar] [CrossRef] [Green Version]
  96. Sanchez-Vallet, A.; Mesters, J.R.; Thomma, B.P. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol. Rev. 2015, 39, 171–183. [Google Scholar] [CrossRef] [Green Version]
  97. Wawra, S.; Fesel, P.; Widmer, H.; Timm, M.; Seibel, J.; Leson, L.; Kesseler, L.; Nostadt, R.; Hilbert, M.; Langen, G.; et al. The fungal-specific β-glucan-binding lectin FGB1 alters cell-wall composition and suppresses glucan-triggered immunity in plants. Nat. Commun. 2016, 7, 13188. [Google Scholar] [CrossRef] [PubMed]
  98. Vandenkoornhuyse, P.; Quaiser, A.; Duhamel, M.; Le Van, A.; Dufresne, A. The importance of the microbiome of the plant holobiont. New Phytol. 2015, 206, 1196–1206. [Google Scholar] [CrossRef] [PubMed]
  99. Nassimi, Z.; Taheri, P. Endophytic fungus Piriformospora indica induced systemic resistance against rice sheath blight via affecting hydrogen peroxide and antioxidants. Biocontrol. Sci. Technol. 2017, 27, 252–267. [Google Scholar] [CrossRef]
  100. Hua, M.D.S.; Senthil Kumar, R.; Shyur, L.F.; Cheng, Y.B.; Tian, Z.; Oelmüller, R.; Yeh, K.W. Metabolomic compounds identified in Piriformospora indica-colonised Chinese cabbage roots delineate symbiotic functions of the interaction. Sci. Rep. 2017, 7, 9291. [Google Scholar] [CrossRef] [PubMed]
  101. Xu, L.; Wu, C.; Oelmueller, R.; Zhang, W. Role of phytohormones in Piriformospora indica-induced growth promotion and stress tolerance in plants: More questions than answers. Front. Microbiol. 2018, 9, 1646. [Google Scholar] [CrossRef] [Green Version]
  102. Lee, Y.C.; Johnson, J.M.; Chien, C.T.; Sun, C.; Cai, D.; Lou, B.; Oelmüller, R.; Yeh, K.W. Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol. Plant Microbe Interact. 2011, 24, 421–431. [Google Scholar] [CrossRef] [Green Version]
  103. Dong, S.; Tian, Z.; Chen, P.J.; Senthil Kumar, R.; Shen, C.H.; Cai, D.; Oelmüllar, R.; Yeh, K.W. The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots. J. Exp. Bot. 2013, 64, 4529–4540. [Google Scholar] [CrossRef] [Green Version]
  104. Kim, D.; Abdelaziz, M.E.; Ntui, V.O.; Guo, X.; Al-Babili, S. Colonization by the endophyte Piriformospora indica leads to early flowering in Arabidopsis thaliana likely by triggering gibberellin biosynthesis. Biochem. Biophys. Res. Commun. 2017, 490, 1162–1167. [Google Scholar] [CrossRef] [Green Version]
  105. Pan, R.; Xu, L.; Wei, Q.; Wu, C.; Tang, W.; Oelmüller, R.; Zhang, W. Piriformospora indica promotes early flowering in Arabidopsis through regulation of the photoperiod and gibberellin pathways. PLoS ONE 2017, 12, e0189791. [Google Scholar] [CrossRef] [Green Version]
  106. Varma, A.; Sherameti, I.; Tripathi, S.; Prasad, R.; Das, A.; Sharma, M.; Bakshi, M.; Johnson, J.M.; Bhardwaj, S.; Arora, M.; et al. The symbiotic fungus Piriformospora indica: Review. Mycota Fungal Assoc. 2012, 9, 231–254. [Google Scholar] [CrossRef]
  107. Zhang, W.Y.; Wang, J.; Xu, L.; Wang, A.A.; Huang, L.; Du, H.W.; Qiu, L.J.; Oelmüller, R. Drought stress responses in maize are diminished by Piriformospora indica. Plant Signal. Behav. 2018, 13, e1414121. [Google Scholar] [CrossRef] [Green Version]
  108. Ghorbani, A.; Tafteh, M.; Roudbari, N.; Pishkar, L.; Zhang, W.; Wu, C. Piriformospora indica augments arsenic tolerance in rice (Oryza sativa) by immobilising arsenic in roots and improving iron translocation to shoots. Ecotoxicol. Environ. Saf. 2021, 209, 111793. [Google Scholar] [CrossRef]
  109. Opitz, M.W.; Daneshkhah, R.; Lorenz, C.; Ludwig, R.; Steinkellner, S.; Wieczorek, K. Serendipita indica changes host sugar and defence status in Arabidopsis thaliana: Cooperation or exploitation? Planta 2021, 253, 74. [Google Scholar] [CrossRef]
  110. Gull, A.; Lone, A.A.; Wani, N.U.I. Biotic and abiotic stresses in plants. In Abiotic and Biotic Stress in Plants; IntechOpen: London, UK, 2019; pp. 1–19. [Google Scholar] [CrossRef]
  111. Hayat, S.; Hayat, Q.; Alyemeni, M.N.; Wani, A.S.; Pichtel, J.; Ahmad, A. Role of proline under changing environments: A review. Plant Signal. Behave. 2012, 7, 1456–1466. [Google Scholar] [CrossRef] [Green Version]
  112. Fakhro, A.; Andrade-Linares, D.R.; von Bargen, S.; Bandte, M.; Büttner, C.; Grosch, R.; Schwarz, D.; Franken, P. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 2010, 20, 191–200. [Google Scholar] [CrossRef]
  113. Del Barrio-Duque, A.; Ley, J.; Samad, A.; Antonielli, L.; Sessitsch, A.; Compant, S. Beneficial endophytic bacteria-Serendipita indica interaction for crop enhancement and resistance to phytopathogens. Front. Microbiol. 2019, 10, 2888. [Google Scholar] [CrossRef]
  114. Deshmukh, S.D.; Kogel, K.H. Piriformospora indica protects barley from root rot caused by Fusarium Graminearum. J. Plant Dis. Prot. 2007, 114, 263–268. [Google Scholar] [CrossRef]
  115. Roylawar, P.; Panda, S.; Kamble, A. Comparative analysis of BABA and Piriformospora indica mediated priming of defence-related genes in tomato against early blight. Physiol. Mol. Plant. Pathol. 2015, 91, 88–95. [Google Scholar] [CrossRef]
  116. Panda, S.; Busatto, N.; Hussain, K.; Kamble, A. Piriformospora indica-primed transcriptional reprogramming induces defence response against early blight in tomato. Sci. Hortic. 2019, 255, 209–219. [Google Scholar] [CrossRef]
  117. Khalid, M.; Hui, N.; Rahman, S.U.; Hayat, K.; Huang, D. Suppression of clubroot (Plasmodiophora brassicae) development in Brassica campestris sp. chinensis L. via exogenous inoculation of Piriformospora indica. J. Radiat. Res. Appl. Sci. 2020, 13, 180–190. [Google Scholar] [CrossRef] [Green Version]
  118. Bajaj, R.; Hu, W.; Huang, Y.; Chen, S.; Prasad, R.; Varma, A.; Bushley, K.E. The beneficial root endophyte Piriformospora indica reduces egg density of the soybean cyst nematode. Biol. Control. 2015, 90, 193–199. [Google Scholar] [CrossRef]
  119. Trzewik, A.; Orlikowska, T.; Kowalczyk, W.; Maciorowski, R.; Marasek-Ciołakowska, A.; Klocke, E. Stimulation of ex vitro growth of Rhododendron hybrids ‘Nova Zembla’ and ‘Alfred’ by inoculation of roots with Serendipita indica. Hortic. Sci. 2020, 47, 194–202. [Google Scholar] [CrossRef]
  120. Trzewik, A.; Marasek-Ciolakowska, A.; Orlikowska, T. Protection of Highbush Blueberry Plants against Phytophthora cinnamomi Using Serendipita indica. Agron. J. 2020, 10, 1598. [Google Scholar] [CrossRef]
  121. Ansari, M.W.; Trivedi, D.K.; Sahoo, R.K.; Gill, S.S.; Tuteja, N. A critical review on fungi mediated plant responses with special emphasis to Piriformospora indica on improved production and protection of crops. Plant Physiol. Biochem. 2013, 70, 403–410. [Google Scholar] [CrossRef] [PubMed]
  122. Li, L.; Guo, N.; Feng, Y.; Duan, M.; Li, C. Effect of Piriformospora indica-Induced Systemic Resistance and Basal Immunity Against Rhizoctonia cerealis and Fusarium graminearum in Wheat. Front. Plant Sci. 2022, 13, 836940. [Google Scholar] [CrossRef]
  123. Stein, E.; Molitor, A.; Kogel, K.H.; Waller, F. Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol. 2008, 49, 1747–1751. [Google Scholar] [CrossRef]
  124. Franken, P. The plant strengthening root endophyte Piriformospora indica: Potential application and the biology behind. Appl. Microbiol. Biotechnol. 2012, 96, 1455–1464. [Google Scholar] [CrossRef] [Green Version]
  125. Zarea, M.J.; Hajinia, S.; Karimi, N.; Goltapeh, E.M.; Rejali, F.; Varma, A. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol. Biochem. 2012, 45, 139–146. [Google Scholar] [CrossRef]
  126. Cheng, C.; Li, D.; Qi, Q.; Sun, X.; Anue, M.R.; David, B.M.; Zhang, Y.; Hao, X.; Zhang, Z.; Lai, Z. The root endophytic fungus Serendipita indica improves resistance of banana to Fusarium oxysporum f. sp. cubense tropical race 4. Eur. J. Plant Pathol. 2020, 156, 87–100. [Google Scholar] [CrossRef]
  127. Atri, C.; Akhatar, J.; Gupta, M.; Gupta, N.; Goyal, A.; Rana, K.; Kaur, R.; Mittal, M.; Sharma, A.; Singh, M.P.; et al. Molecular and genetic analysis of defensive responses of Brassica juncea–B. fruticulosa introgression lines to Sclerotinia infection. Sci. Rep. 2019, 9, 1–12. [Google Scholar] [CrossRef] [Green Version]
  128. Poveda, J.; Hermosa, R.; Monte, E.; Nicolás, C. Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Sci. rep. 2019, 9, 11650. [Google Scholar] [CrossRef] [Green Version]
  129. Šamec, D.; Karalija, E.; Šola, I.; Vujčić Bok, V.; Salopek-Sondi, B. The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants 2021, 10, 118. [Google Scholar] [CrossRef]
  130. Kumar, M.; Yadav, V.; Tuteja, N.; Johri, A.K. Antioxidant enzyme activities in maize plants colonised with Piriformospora indica. Microbiology 2009, 155, 780–790. [Google Scholar] [CrossRef]
  131. Abdelaziz, M.E.; Atia, M.A.; Abdelsattar, M.; Abdelaziz, S.M.; Ibrahim, T.A.; Abdeldaym, E.A. Unravelling the Role of Piriformospora indica in combating water deficiency by modulating physiological performance and chlorophyll metabolism-related genes in Cucumis sativus. Horticulturae 2021, 7, 399. [Google Scholar] [CrossRef]
  132. Tyagi, J.; Chaudhary, P.; Mishra, A.; Khatwani, M.; Dey, S.; Varma, A. Role of endophytes in abiotic stress tolerance: With special emphasis on Serendipita indica. Int. J. Environ. Res. 2022, 16, 62. [Google Scholar] [CrossRef]
  133. Atia, M.A.; Abdeldaym, E.A.; Abdelsattar, M.; Ibrahim, D.S.; Saleh, I.; Abd Elwahab, M.; Osman, G.H.; Arif, I.A.; Abdelaziz, M.E. Piriformospora indica promotes cucumber tolerance against root-knot nematode by modulating photosynthesis and innate responsive genes. Saudi J. Biol. Sci. 2020, 27, 279–287. [Google Scholar] [CrossRef]
  134. Jangir, P.; Shekhawat, P.K.; Bishnoi, A.; Ram, H.; Soni, P. Role of Serendipita indica in enhancing drought tolerance in crops. Physiol. Mol. Plant. Pathol. 2021, 116, 101691. [Google Scholar] [CrossRef]
  135. Ghaffari, M.R.; Mirzaei, M.; Ghabooli, M.; Khatabi, B.; Wu, Y.; Zabet-Moghaddam, M.; Mohammadi-Nejad, G.; Haynes, P.A.; Hajirezaei, M.R.; Sepehri, M.; et al. Root endophytic fungus Piriformospora indica improves drought stress adaptation in barley by metabolic and proteomic reprogramming. Environ. Ex. Bot. 2019, 157, 197–210. [Google Scholar] [CrossRef]
  136. Tanha, S.R.; Ghasemnezhad, A.; Babaeizad, V. A study on the effect of endophyte fungus, Piriformospora indica, on the yield and phytochemical changes of globe artichoke (Cynara scolymus L.) leaves under water stress. Int. J. Adv. Biol. Biomed. Res. 2014, 2, 1907–1921. [Google Scholar] [CrossRef]
  137. Xu, L.; Wang, A.; Wang, J.; Wei, Q.; Zhang, W. Piriformospora indica confers drought tolerance on Zea mays L. through enhancement of antioxidant activity and expression of drought-related genes. Crop. J. 2017, 5, 251–258. [Google Scholar] [CrossRef] [Green Version]
  138. Zhang, W.Y.; Wang, A.A.; Hao, R.C.; Yang, T. Endophytic fungus Piriformospora indica promotes growth and confers drought tolerance in sesame (Sesamum indicum L.). Chin. J. Oil Crop Sci. 2014, 36, 11. [Google Scholar] [CrossRef]
  139. Li, D.; Bodjrenou, D.M.; Zhang, S.; Wang, B.; Pan, H.; Yeh, K.W.; Lai, Z.; Cheng, C. The endophytic fungus Piriformospora indica reprograms banana to cold resistance. Int. J. Mol. Sci. 2021, 22, 4973. [Google Scholar] [CrossRef] [PubMed]
  140. Jiang, W.; Pan, R.; Buitrago, S.; Wu, C.; Abdelaziz, M.E.; Oelmüller, R.; Zhang, W. (Transcriptome analysis of Arabidopsis reveals freezing-tolerance related genes induced by root endophytic fungus Piriformospora indica. Physiol. Mol. Biol. Plants 2021, 27, 189–201. [Google Scholar] [CrossRef] [PubMed]
  141. Li, L.; Li, L.; Wang, X.; Zhu, P.; Wu, H.; Qi, S. Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Plant Physiol. Biochem. 2017, 119, 211–223. [Google Scholar] [CrossRef] [PubMed]
  142. Abdelaziz, M.E.; Kim, D.; Ali, S.; Fedoroff, N.V.; Al-Babili, S. The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na+/K+ homeostasis under salt stress conditions. Plant Sci. 2017, 263, 107–115. [Google Scholar] [CrossRef] [Green Version]
  143. Singh, M.; Tiwari, N. Microbial amelioration of salinity stress in HD 2967 wheat cultivar by up-regulating antioxidant defence. Commun. Integr. Biol. 2021, 114, 136–150. [Google Scholar] [CrossRef]
  144. Jogawat, A.; Vadassery, J.; Verma, N.; Oelmüller, R.; Dua, M.; Nevo, E.; Johri, A.K. PiHOG1, a stress regulator MAP kinase from the root endophyte fungus Piriformospora indica, confers salinity stress tolerance in rice plants. Sci. Rep. 2016, 6, 36765. [Google Scholar] [CrossRef]
  145. Ghaffari, M.R.; Ghabooli, M.; Khatabi, B.; Hajirezaei, M.R.; Schweizer, P.; Salekdeh, G.H. Metabolic and transcriptional response of central metabolism affected by root endophytic fungus Piriformospora indica under salinity in barley. Plant Mol. Biol. 2016, 90, 699–717. [Google Scholar] [CrossRef]
  146. Khalid, M.; Hassani, D.; Liao, J.; Xiong, X.; Bilal, M.; Huang, D. An endosymbiont Piriformospora indica reduces adverse effects of salinity by regulating cation transporter genes, phytohormones, and antioxidants in Brassica campestris ssp. Chinensis. Environ. Exp. Bot. 2018, 153, 89–99. [Google Scholar] [CrossRef]
  147. Ghorbani, A.; Omran, V.O.G.; Razavi, S.M.; Pirdashti, H.; Ranjbar, M. Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Rep. 2019, 38, 1151–1163. [Google Scholar] [CrossRef]
  148. Boorboori, M.R.; Zhang, H.-Y. The Role of Serendipita indica (Piriformospora indica) in Improving Plant Resistance to Drought and Salinity Stresses. Biology 2022, 11, 952. [Google Scholar] [CrossRef]
  149. Shahabivand, S.; Parvaneh, A.; Aliloo, A.A. Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity. Ecotoxicol. Environ. Saf. 2017, 145, 96–502. [Google Scholar] [CrossRef]
  150. Shahabivand, S.; Maivan, H.Z.; Goltapeh, E.M.; Sharifi, M.; Aliloo, A.A. The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol. Biochem. 2012, 60, 53–58. [Google Scholar] [CrossRef]
  151. Baghaie, A.H.; Jabari, A.G. Effect of nano Fe-oxide and endophytic fungus (P. indica) on petroleum hydrocarbons degradation in an arsenic contaminated soil under barley cultivation. J. Env. Health Sci. Eng. 2019, 17, 853–861. [Google Scholar] [CrossRef]
  152. Sabra, M.; Aboulnasr, A.; Franken, P.; Perreca, E.; Wright, L.P.; Camehl, I. Beneficial root endophytic fungi increase growth and quality parameters of sweet basil in heavy metal contaminated soil. Front. Plant Sci. 2018, 9, 1726. [Google Scholar] [CrossRef] [Green Version]
  153. Mohd, S.; Shukla, J.; Kushwaha, A.S.; Mandrah, K.; Shankar, J.; Arjaria, N.; Saxena, P.N.; Narayan, R.; Roy, S.K.; Kumar, M. Endophytic fungi Piriformospora indica mediated protection of host from arsenic toxicity. Front. Microbiol. 2017, 8, 754. [Google Scholar] [CrossRef] [Green Version]
  154. Hui, F.; Liu, J.; Gao, Q.; Lou, B. Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J. Environ. Sci. 2015, 1, 184–191. [Google Scholar] [CrossRef]
  155. Swetha, S.; Padmavathi, T. Mitigation of Drought Stress by Piriformospora indica in Solanum melongena L. cultivars. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 2020, 90, 585–593. [Google Scholar] [CrossRef]
  156. Saddique, M.A.; Ali, Z.; Khan, A.S.; Rana, I.A.; Shamsi, I.H. Inoculation with the endophyte Piriformospora indica significantly affects mechanisms involved in osmotic stress in rice. Rice 2018, 11, 34. [Google Scholar] [CrossRef] [Green Version]
  157. Ghabooli, M.; Khatabi, B.; Ahmadi, F.S.; Sepehri, M.; Mirzaei, M.; Amirkhani, A.; Jorrín-Novo, J.V.; Salekdeh, G.H. Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J. Proteom. 2013, 94, 289–301. [Google Scholar] [CrossRef]
  158. Tyagi, J.; Varma, A.; Pudake, R.N. Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. Eur. J. Soil. Biol. 2017, 1, 1–10. [Google Scholar] [CrossRef]
  159. Lanza, M.; Haro, R.; Conchillo, L.B.; Benito, B. The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: Fungal ENA ATPases are expressed and regulated at high pH and during plant co-cultivation in salinity. Environ. Microbiol. 2019, 21, 3364–3378. [Google Scholar] [CrossRef] [PubMed]
  160. Bagheri, A.A.; Saadatmand, S.; Niknam, V.; Nejadsatari, T.; Babaeizad, V. Effect of endophytic fungus, Piriformospora indica, on growth and activity of antioxidant enzymes of rice (Oryza sativa L.) under salinity stress. Int. J. Adv. Biol. Biomed. Res. 2013, 1, 1337–1350. Available online: http://www.ijabbr.com/article_7908.html (accessed on 10 February 2022).
  161. Baltruschat, H.; Fodor, J.; Harrach, B.D.; Niemczyk, E.; Barna, B.; Gullner, G.; Janeczko, A.; Kogel, K.H.; Schäfer, P.; Schwarczinger, I.; et al. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 2008, 180, 501–510. [Google Scholar] [CrossRef]
  162. David, B.M.; Sun, X.; Mensah, R.A.; Li, D.; Liu, F.; Tian, N.; Lai, Z.; Cheng, C. Physiological and biochemical mechanism of Piriformospora indica induced high temperature resistance in banana. Chin. J. Appl. Environ. Biol. 2020, 26, 1466–1472. [Google Scholar] [CrossRef]
  163. Sagonda, T.; Adil, M.F.; Sehar, S.; Rasheed, A.; Joan, H.I.; Ouyang, Y.; Shamsi, I.H. Physio-ultrastructural footprints and iTRAQ-based proteomic approach unravel the role of Piriformospora indica-colonization in counteracting cadmium toxicity in rice. Ecotoxicol. Environ. Saf. 2021, 1, 112390. [Google Scholar] [CrossRef]
  164. Wang, X.; Fan, X.; Wang, W.; Song, F. Combined Effects of Inoculating Serendipita Indica on Soybean Growth and Soil Health Under Cd Stress. Res. Square Preprint 2021, 10, 11. [Google Scholar] [CrossRef]
  165. Rajak, J.; Bawaskar, M.; Rathod, D.; Agarkar, G.; Nagaonkar, D.; Gade, A.; Rai, M. Interaction of copper nanoparticles and an endophytic growth promoter Piriformospora indica with Cajanus Cajan. J. Sci. Food Agric. 2017, 97, 4562–4570. [Google Scholar] [CrossRef]
  166. Nagaonkar, D.; Shende, S.; Rai, M. Biosynthesis of copper nanoparticles and its effect on actively dividing cells of mitosis in Allium cepa. Biotechnol. Prog. 2015, 31, 57–565. [Google Scholar] [CrossRef]
  167. Varma, A.; Uma, K.M. Role of nanoparticles on plant growth with special emphasis on Piriformospora indica: A Review. In Nanoscience and Plant–Soil Systems; Ghorbanpour, M., Manika, K., Varma, A., Eds.; Springer: Cham, Switzerland, 2017; pp. 387–403. [Google Scholar] [CrossRef]
  168. Rane, M.; Bawskar, M.; Rathod, D.; Nagaonkar, D.; Rai, M. Influence of calcium phosphate nanoparticles, Piriformospora indica and Glomus mosseae on growth of Zea mays. Adv. Nat. Sci. Nanosci. Nanotechnol. 2015, 6, 045014. [Google Scholar] [CrossRef]
  169. Nongbet, A.; Mishra, A.K.; Mohanta, Y.K.; Mahanta, S.; Ray, M.K.; Khan, M.; Baek, K.H.; Chakrabartty, I. Nanofertilizers: A Smart and Sustainable Attribute to Modern Agriculture. Plants 2022, 11, 2587. [Google Scholar] [CrossRef]
  170. Jaskulski, D.; Jaskulska, I.; Majewska, J.; Radziemska, M.; Bilgin, A.; Brtnicky, M. Silver nanoparticles (AgNPs) in urea solution in laboratory tests and field experiments with crops and vegetables. Materials 2022, 15, 870. [Google Scholar] [CrossRef]
  171. Mahapatra, D.M.; Satapathy, K.C.; Panda, B. Biofertilizers and nanofertilizers for sustainable agriculture: Phycoprospects and challenges. Sci. Total Environ. 2022, 803, 149990. [Google Scholar] [CrossRef]
Plants 11 03417 g001 550
Figure 1. Morphology of Serendipita indica. (a) Growth of S. indica colony on PDA media; scale bars of 10 mm. (b) Growth of S. indica colony in PDB media; scale bars of 10 mm. (c) Growth of S. indica from PDB medium; scale bars of 1 mm. (d) Chlamydospores (black arrows) and mycelium (red arrows) of S. indica observed under a bright field microscope; scale bars of 100 µm. (e,f) Mycelial structure of S. indica observed under an electron microscope.
Figure 1. Morphology of Serendipita indica. (a) Growth of S. indica colony on PDA media; scale bars of 10 mm. (b) Growth of S. indica colony in PDB media; scale bars of 10 mm. (c) Growth of S. indica from PDB medium; scale bars of 1 mm. (d) Chlamydospores (black arrows) and mycelium (red arrows) of S. indica observed under a bright field microscope; scale bars of 100 µm. (e,f) Mycelial structure of S. indica observed under an electron microscope.
Plants 11 03417 g001
Plants 11 03417 g002 550
Figure 2. The roots of cabbage inoculated with S. indica observed under a fluorescent microscope; scale bars of 50 μm. (a) The cortex of cabbage roots covered with spores. (b) Close view of spores covering cabbage roots. (c) The fungal mycelium developing externally. (d) The fungus covering the root tip. White and blue arrows point to spores and mycelium, respectively.
Figure 2. The roots of cabbage inoculated with S. indica observed under a fluorescent microscope; scale bars of 50 μm. (a) The cortex of cabbage roots covered with spores. (b) Close view of spores covering cabbage roots. (c) The fungal mycelium developing externally. (d) The fungus covering the root tip. White and blue arrows point to spores and mycelium, respectively.
Plants 11 03417 g002
Plants 11 03417 g003 550
Figure 3. Bright-field microscope photos of the cabbage roots with internal (a) and external (b) colonisation by S. indica; scale bars of 100 µm.
Figure 3. Bright-field microscope photos of the cabbage roots with internal (a) and external (b) colonisation by S. indica; scale bars of 100 µm.
Plants 11 03417 g003
Plants 11 03417 g004 550
Figure 4. Schematic representation of the effects of S. indica on plant growth, development, and response to various stresses.
Figure 4. Schematic representation of the effects of S. indica on plant growth, development, and response to various stresses.
Plants 11 03417 g004
Plants 11 03417 g005 550
Figure 5. Mutual interaction of S. indica with host plant resulting in enhanced plant metabolism by regulating the plant growth mechanism at molecular level. Genes which exhibit a fundamental role in this process are AUX1, PINS, TIR—auxin biosynthesis genes, AHK2, AHK3, CRE1—cytokinin receptor genes, ARR—cytokinin-responsive gene, ECR—trans-2, 3-enoyl-CoA reductase, ETR, EIN2, EIN3, EIN3/EIL1—ethylene biosynthesis genes, FAE1—3-ketoacyl-CoA synthase, FRDL1, IRO2, YSL1—iron transporter genes, GA3OIX1, GA2OIX2—gibberellic acid biosynthesis genes, GWD—glucan-water dikinase, INV—invertase, kcr1—3-ketoacyl-CoA reductase 1, kcr2—3-ketoacyl-CoA reductase 2, 2NpdO—nitropropane dioxygenase, Nia2—nitrate reductase, PT3, PT5, and PT6—phosphorus transporter genes. Upward and downward arrows represent upregulation and downregulation of genes or processes, respectively.
Figure 5. Mutual interaction of S. indica with host plant resulting in enhanced plant metabolism by regulating the plant growth mechanism at molecular level. Genes which exhibit a fundamental role in this process are AUX1, PINS, TIR—auxin biosynthesis genes, AHK2, AHK3, CRE1—cytokinin receptor genes, ARR—cytokinin-responsive gene, ECR—trans-2, 3-enoyl-CoA reductase, ETR, EIN2, EIN3, EIN3/EIL1—ethylene biosynthesis genes, FAE1—3-ketoacyl-CoA synthase, FRDL1, IRO2, YSL1—iron transporter genes, GA3OIX1, GA2OIX2—gibberellic acid biosynthesis genes, GWD—glucan-water dikinase, INV—invertase, kcr1—3-ketoacyl-CoA reductase 1, kcr2—3-ketoacyl-CoA reductase 2, 2NpdO—nitropropane dioxygenase, Nia2—nitrate reductase, PT3, PT5, and PT6—phosphorus transporter genes. Upward and downward arrows represent upregulation and downregulation of genes or processes, respectively.
Plants 11 03417 g005
Plants 11 03417 g006 550
Figure 6. Schematic representation of the effects of S. indica on plants under biotic stresses. S. indica maintains the plant growth and development throughout the growing stages by regulating various genes and antioxidant production, leading to the development of tolerance against stresses in host plants. Various genes are involved in the process consisting of FAD2—fatty acid desaturase 2, LOX—lipoxygenase, SiTPs—terpenoid synthase gene, senescence associated genes, WRKY—transcription factor. Upward and downward arrows represent upregulation and downregulation of genes or processes, respectively.
Figure 6. Schematic representation of the effects of S. indica on plants under biotic stresses. S. indica maintains the plant growth and development throughout the growing stages by regulating various genes and antioxidant production, leading to the development of tolerance against stresses in host plants. Various genes are involved in the process consisting of FAD2—fatty acid desaturase 2, LOX—lipoxygenase, SiTPs—terpenoid synthase gene, senescence associated genes, WRKY—transcription factor. Upward and downward arrows represent upregulation and downregulation of genes or processes, respectively.
Plants 11 03417 g006
Plants 11 03417 g007 550
Figure 7. Schematic description of the effects and the molecular mechanisms of S. indica on host plants under various abiotic stress. Cold tolerance genes: BZR1—brassinazole-resistant, CBFs—C-repeat-binding factor, CORs—cold-regulated genes, PYL6—pyrabactin resistance 1-like, SAG1s—senescence-associated gene; Drought tolerance genes: ANAC07—transcription factor gene, CBL1—calcineurin B-like protein, CIPK3—CBL-interacting protein kinase 3, DREB2A—dehydration-response element binding protein 2A, ERD1—early response to dehydration 1, HAT—histone acetyltransferase, LEA14—late embryogenesis abundant 14, P5CS—pyrroline-5-carboxylate synthase, RD29A—responsive-to-dehydration 29A gene, SDIR1—salt and drought-induced ring finger 1, TAS14—a dehydrin; Heavy metal tolerance genes: Gsh2, PCS1, PCS2, oas1, TaPCS1—phytochelatin synthase-related genes, GPX—glutathione peroxidase, Hsp70—heat shock proteins; Salt tolerance: CNGC15—cyclic nucleotide-gated channel, NHX2—sodium/hydrogen exchanger 2, SiHOG1—S. indica high osmolarity glycerol, SOS1—Na+/H+ antiporter. Upward and downward arrows represent upregulation and downregulation of genes or process, respectively.
Figure 7. Schematic description of the effects and the molecular mechanisms of S. indica on host plants under various abiotic stress. Cold tolerance genes: BZR1—brassinazole-resistant, CBFs—C-repeat-binding factor, CORs—cold-regulated genes, PYL6—pyrabactin resistance 1-like, SAG1s—senescence-associated gene; Drought tolerance genes: ANAC07—transcription factor gene, CBL1—calcineurin B-like protein, CIPK3—CBL-interacting protein kinase 3, DREB2A—dehydration-response element binding protein 2A, ERD1—early response to dehydration 1, HAT—histone acetyltransferase, LEA14—late embryogenesis abundant 14, P5CS—pyrroline-5-carboxylate synthase, RD29A—responsive-to-dehydration 29A gene, SDIR1—salt and drought-induced ring finger 1, TAS14—a dehydrin; Heavy metal tolerance genes: Gsh2, PCS1, PCS2, oas1, TaPCS1—phytochelatin synthase-related genes, GPX—glutathione peroxidase, Hsp70—heat shock proteins; Salt tolerance: CNGC15—cyclic nucleotide-gated channel, NHX2—sodium/hydrogen exchanger 2, SiHOG1—S. indica high osmolarity glycerol, SOS1—Na+/H+ antiporter. Upward and downward arrows represent upregulation and downregulation of genes or process, respectively.
Plants 11 03417 g007
Table
Table 1. Effects of S. indica on growth and quality of host plants.
Table 1. Effects of S. indica on growth and quality of host plants.
Host PlantMethod of ApplicationEffect of S. indica on GrowthEffect of S. indica on QualityReference
Tomato (Lycopersicon esculentum)Seedling root applicationIncrease in plant growth, yield, early floweringImproved firmness in fruits, total soluble solids, and acidity[49]
Lettuce (Lactuca sativa)Seedling applicationIncrease in plant height, fresh and dry weight, yieldIncrease in chlorophyll, nitrogen, phosphorus, and potassium content[67]
Seedling root applicationIncrease in zinc and manganese content[64]
Chinese cabbage (Brassica oleracea)Seedling root applicationIncrease in root and shoot growth, biomass, and lateral root formation_[68]
Cabbage (Brassica oleracea)Substrate application and Seed applicationIncrease in plant height, number of leaves, NDVI, fluorescence level (Ft)Increase in chlorophyll and carotenoids content, antioxidant capacity[3]
Bell pepper (Capsicum annuum)Seed treatmentIncrease in plant growth and yield_[19]
Spinach (Spinacia oleracea)Seed applicationIncrease in plant height, dry and fresh weight_[11]
Taro (Colocasia esculenta)Sterile soil applicationIncrease in plant height, number and area of leavesIncrease in total phenol content and defence-related enzymes[69]
Sweet potato (Ipomea batatas)Seedling irrigationIncrease in plant biomass, number of leaves, and lateral rootsIncrease in photosynthetic pigments, catalase, JA-mediated activity[47]
Wheat (Triticum aestivum)Seedling rootsIncrease in shoot dry biomassIncrease in nitrogen, phosphorus, and iron uptake[52]
Rice (Oryza sativa)Seed and Seedling rootsIncrease in plant growth, biomass, yieldNPK, chlorophyll, and sugar content[59]
Seed treatment and Soil treatmentIncrease in dry weight of plantIncrease in phosphorus and potassium uptake[46]
Barley (Hordeum vulgare)Seed applicationIncrease in crop yield_[70]
Finger Millets (Eleusine coracana)Seed applicationIncrease in plant height, number of tillers, plant biomass, ear heads, test weight, grain, and dry straw yieldIncrease in NPK content[71]
Groundnut (Arachis hypogaea)Seedling applicationIncrease in growth and number of pods, seeds per plant, shelling percentage, 100-seed weight, and pod yield_[72]
Green gram (Vigna radiata)Seed applicationIncrease in number of nodules per plant, leaf area, and yieldIncrease in minerals uptake, chlorophyll content[73]
Chickpeas (Cicer arietinum)Seed applicationIncrease in growth and yieldIncrease in phosphorus (P) uptake[74]
Sugarcane (Saccharum sp.)PlantletsIncrease in growth and yield, cane height, tilleringIncrease in iron and copper content, sugar content[66]
Rapeseed (Brassica napus)Seedling applicationIncrease in plant yield, biomass, early floweringIncrease in oil content, nutrient uptake, decrease in anti-nutrient content[25]
Black pepper (Piper nigrum)Root cuttingsIncrease in fresh and dry weight, number and area of leaves, early floweringIncrease in chlorophyll content[43]
Sunflower (Helianthus)Seedling applicationIncrease in growth of plant and seed yield.Increase in root and stem growth, number and area of leaves. Increase in flower diameter, dry weight, and total biomass Increase in seed oil content[40]
Turmeric (Curcuma sp.)Bud applicationIncrease in productivityIncrease in secondary metabolite curcumin and oil content[75]
Fennel (Foeniculum vulgare)SeedlingIncrease in plant height, dry weight of plant, fruit dry weightIncrease in essential oil content (anethole)[45]
Thyme (Thymus vulgaris)Shoot applicationIncrease in plant height, fresh and dry weight of shoot. Increase in root length, fresh and dry weight of rootsIncrease in essential oil content (thymol)[76]
Bacopa (Bacopa monnieri)Micro propagated plantsIncrease in plant growthIncrease in bacoside and antioxidant content[77]
Aloe vera (Aloe barbadensis)Root applicationIncrease in biomass, shoot and root length, shoot and root numberIncrease in chlorophyll, gel, aloin, and phenol content in leaves[78]
Artemisia (Artemisia annua)Seedling root applicationIncrease in plant height, dry weight, leaf yieldIncrease in chlorophyll, phosphorus, nitrogen, flavonoids, and artemisinin content[79]
Root application[80]
Centella asiaticaRoot applicationIncrease in shoot and root biomassIncrease in asiaticoside content[81]
Coleus forskohliiRoot applicationIncrease in aerial biomass, flower developmentIncrease in chlorophyll content, phosphorus acquisition[82]
Lantana camaraSuspension culture of plant_Increase in triterpenoids (ursolic acid, oleanolic acid, and betulinic acid) production[83]
Pine vines (Aristolochia elegans Mart.)Substrate applicationIncrease in plant height, number and length of leaves, total biomassIncrease in aristolochic acid in leaves[30]
Alfalafa (Medicago sativa)Seedling applicationIncrease in biomass, shoot dry weightIncrease in nutrient uptake, antioxidant enzyme activity[84]
Sweet basil (Ocimum basilicum)_Increase in plant growth, leaf area, leaf dry weight, yieldIncrease in oil content (Geranial, Neral, and Estragole)[85]
Gerbera (Gerbera jamesonii)Root seedling applicationIncrease in above and underground plant biomassIncrease in photochemical efficiency[86]
Anthurium sp.Seedling rootsIncrease in plant and root growthIncrease in phosphorus uptake and chlorophyll content[87]
Lolium multiflorumSeed applicationIncrease in plant height, basal diameter, biomass relative growth rateIncrease in leaf relative water content and chlorophyll content[38]
Banana (Musa acuminata)Plantlet rootsIncrease in plant height, number and area of leaves, stem diameter, number of suckers, number of fingers per bunch, and yield per plantIncrease in chlorophyll, nitrogen, and phosphorus content[88]
Passion fruit (Passiflora edulis)Soil applicationPlant growth in later stages, fruit sizeIncrease in fruit quality and secondary metabolites[89]
Trifolium orange(Poncirus trifoliata)Substrate applicationIncrease in plant height, number of leaves, leaf, stem, and root biomassIncrease in nitrogen, phosphorus, and magnesium content[7]
Melon (Cucumis melo)Substrate applicationIncrease in fresh and dry weight of plantsIncrease in chlorophyll content[90]
Pineapple (Ananas comosus)Substrate inoculation in root zoneIncrease in plant height, number of leaves, and shoot dry weightIncrease in photosynthetic efficiency, nitrogen, phosphorus, potassium, calcium, and magnesium content[61]
Table
Table 2. Effects of S. indica on host plants under biotic stress conditions.
Table 2. Effects of S. indica on host plants under biotic stress conditions.
Host PlantBiotic StressEffect of S. indica under Biotic StressReference
Tomato (Lycopersicon esculentum)Verticillium wiltIncrease in plant growth, dry and fresh weight content, disease resistance—[112]
Early blight-Decrease in disease severity[115]
Increase in plant growth, systemic defence response-[116]
Tomato (Lycopersicon esculentum)Leaf curl virusIncrease in root and plant growth, quality, and yield of fruitDecrease in disease incidence[49]
Chinese cabbage (Brassica oleracea)Club rootIncrease in biomass, flavonoidsDecrease in gall formation[117]
Cabbage (Brassica oleracea)Black spotIncrease in plant growth, chlorophyll content, antioxidant capacity, nitrogen content Decrease in disease severity[3]
Onion (Allium cepa)Stemphylium Leaf BlightIncrease in leaf growth and root biomass, enzymatic activity, defence-related genesDecrease in disease severity[28]
Taro (Colocasia esculenta)Leaf blightIncrease in plant growth, chitinase, β-1, 3 glucanase and total phenol, defence-related genes, disease resistance-[69]
Soyabean (Glycine max)Cyst nematodeIncrease in plant growth and developmentDecrease in nematode egg density[118]
Chickpea (Cicer arietinum)Grey moldIncrease in biomass, root growth, antioxidant enzyme defence system, protection from pathogen-[63]
Anthurium (Anthurium)Bacterial wiltIncrease in biomass, plant and root growth, photosynthetic rate, phosphorus uptake, disease resistance-[87]
Rhododendron (Rhododendron catawbiense)DiebackDelayed disease-[119]
Blueberry (Vaccinium corymbosum)DiebackIncrease in plant growthDecrease in disease severity and mortality rate[120]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Saleem, S.; Sekara, A.; Pokluda, R. Serendipita indica—A Review from Agricultural Point of View. Plants 2022, 11, 3417. https://doi.org/10.3390/plants11243417

AMA Style

Saleem S, Sekara A, Pokluda R. Serendipita indica—A Review from Agricultural Point of View. Plants. 2022; 11(24):3417. https://doi.org/10.3390/plants11243417

Chicago/Turabian Style

Saleem, Sana, Agnieszka Sekara, and Robert Pokluda. 2022. "Serendipita indica—A Review from Agricultural Point of View" Plants 11, no. 24: 3417. https://doi.org/10.3390/plants11243417

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