Next Article in Journal
Contrasting Regulators of the Onset and End of the Seed Release Phenology of a Temperate Desert Shrub Nitraria tangutorum
Next Article in Special Issue
Metabolomics Analysis Reveals Metabolites and Metabolic Pathways Involved in the Growth and Quality of Water Dropwort [Oenanthe javanica (Blume) DC.] under Nutrient Solution Culture
Previous Article in Journal
Breeding for Higher Yields of Wheat and Rice through Modifying Nitrogen Metabolism
Previous Article in Special Issue
Biochemical Insights into the Ability of Lemna minor L. Extract to Counteract Copper Toxicity in Maize
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 12
Issue 1
10.3390/plants12010086
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

Biomimetic Strategies for Developing Abiotic Stress-Tolerant Tomato Cultivars: An Overview

by
Gyanendra Kumar Rai
1,
Pradeep Kumar
2,*,
Sadiya Maryam Choudhary
1,
Rafia Kosser
1,
Danish Mushtaq Khanday
3,
Shallu Choudhary
4,
Bupesh Kumar
3,
Isha Magotra
1,
Ranjit Ranjan Kumar
5,
Chet Ram
6,
Youssef Rouphael
7,
Giandomenico Corrado
7,* and
Tusar Kanti Behera
8
1
School of Biotechnology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Jammu, Jammu 180009, India
2
Division of Integrated Farming System, ICAR—Central Arid Zone Research Institute, Jodhpur 342003, India
3
Division of Plant Breeding and Genetics, Sher-e-Kashmir University of Agricultural Sciences and Technology of Jammu, Jammu 180009, India
4
Division of Entomology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Jammu, Jammu 180009, India
5
Division of Biochemistry, ICAR—Indian Agricultural Research Institute, New Delhi 110001, India
6
Division of Crop Improvement, ICAR—Central Institute for Arid Horticulture, Bikaner 334006, India
7
Department of Agricultural Sciences, University of Naples Federico II, Portici, 80055 Naples, Italy
8
ICAR—Indian Institute of Vegetable Research, Jakhini (Shahanshapur), Varanasi 221305, India
*
Authors to whom correspondence should be addressed.
Plants 2023, 12(1), 86; https://doi.org/10.3390/plants12010086
Submission received: 1 December 2022 / Revised: 17 December 2022 / Accepted: 20 December 2022 / Published: 23 December 2022
(This article belongs to the Special Issue Morphological, Physiological, Metabolic, and Genetic Aspects of Eustress in Horticultural Crops)
Browse Figures
Versions Notes

Abstract

:
The tomato is one of the most important vegetables in the world. The demand for tomatoes is high in virtually any country, owing to their gastronomic versatility and nutritional and aromatic value. Drought, salinity, and inadequate temperature can be major factors in diminishing yield, affecting physiological and biochemical processes and altering various metabolic pathways, from the aggregation of low molecular–weight substances to the transcription of specific genes. Various biotechnological tools can be used to alter the tomato genes so that this species can more rapidly or better adapt to abiotic stress. These approaches range from the introgression of genes coding for specific enzymes for mitigating a prevailing stress to genetic modifications that alter specific metabolic pathways to help tomato perceive environmental cues and/or withstand adverse conditions. In recent years, environmental and social concerns and the high complexity of the plant response may increase the attention of applied plant biotechnology toward biomimetic strategies, generally defined as all the approaches that seek to develop more sustainable and acceptable strategies by imitating nature’s time-tested solutions. In this review, we provide an overview of some of the genetic sequences and molecules that were the objects of biotechnological intervention in tomato as examples of approaches to achieve tolerance to abiotic factors, improving existing nature-based mechanisms and solutions (biomimetic biotechnological approaches (BBA)). Finally, we discuss implications and perspectives within the GMO debate, proposing that crops modified with BBA should receive less stringent regulation.

1. Introduction

Despite yearly fluctuations, the tomato (Solanum lycopersicum L.) remains a widely grown vegetable and has significant nutritional and economic importance all over the world [1]. For example, the lycopene in tomato fruits provides antioxidative and anticancerous properties. Moreover, its versatility and vivid color make the tomato a favorite food in many countries. In 2020, the area under tomato production was approximately 5.05 Mha, with a fresh production of 186.8 Mtones [2]. The demand for tomatoes on a global scale has increased in the last century because of their wide range of uses as raw, cooked, and processed foods.
Tomato yield, like many other vegetables, is limited by abiotic stress, such as cold, heat, drought, and salinity [3,4]. The main environmental issues reducing tomato cultivation are low-quality water, extreme temperature, an imbalance in the nutritional content of the soil substrate, elemental toxicity, and high salinity [3,5,6]. Abiotic stress becomes highly problematic in the open field, where stresses can easily coexist. Improving the tomato’s ability to withstand common abiotic stresses is economically more advantageous and sustainable than the use of non-renewable chemical input or the implementation of new agronomic measures. It is, therefore, necessary to develop resilient, high-yielding cultivars with greater tolerance to a variety of abiotic challenges [7,8]. Classic tomato breeding has increased yield (and its specific components), quality-related traits, and resistance to some abiotic as well as biotic stress considerably. The application of high throughput and multidisciplinary methodologies currently provides new tools to develop stress tolerance for crop species with high genetic complexity and large ecological interactions like tomato [9].
It has long been established that recombinant DNA technology is a suitable approach for breeding tomato cultivars. Developments in tomato genomics have largely favored the identification of various genes, gene families, and metabolic pathways that are responsible for providing the required modified adaptation to the plants to stressful environments. Their study and modification can result in improved yield attributes under sub-optimal environmental conditions [10,11,12]. In addition to being the foundation of novel cultivars, genetically modified plants can also be useful for studying and characterizing how gene networks for abiotic stress tolerance interact and perform under a variety of conditions [13]. In this article, we present and discuss various genes, proteins, and other molecular compounds that are directly and/or indirectly linked to improved tolerance to abiotic stress, focusing on biomimetic strategies. Broadly speaking, a biomimetic technological approach is one that follows and improves models provided by nature. Although it is debated whether “biomimetics” should be distinguished from “biomimicry” (interventions that are only inspired by vs. those strictly following nature), we discuss the principles of the mechanisms of stress response in tomato, as well as various possible interventions, under the conceptual framework that the study of nature’s models provides inspiration to their modifications and improvements. To address public concerns, the concepts of cisgenesis and intragenesis have been developed as a more acceptable strategy to alter the genetic material of a plant. Nonetheless, it is not easy to strictly define the extent of the sequence variability of a gene or, more generally, a DNA stretch that can be considered within or outside the gene pool of a crop species. This is further complicated considering that cisgenesis and intragenesis allow the use of sequences from not only the crop of interest but also related species capable of sexual hybridization. To stimulate a discussion, in this review, we would like to put forward that modifications of the metabolism of an organism through DNA recombinant technology should be evaluated considering not only the sequence of interest but also the functional modification that will be achieved. To this purpose, we refer to the term biomimetic biotechnological approaches (BBA) to identify the improvement, but not the redesign or (non-native) reconstruction, of systems and pathways that are already present within a plant species and active in an organ or tissue, irrespective of the taxonomical source of the DNA employed. Biomimetics is often coupled with aterials science, mechanical engineering, and nanotechnology and, along with biomimicry, is associated with more biodiverse agricultural systems. Therefore, the concept of BBA in plants may facilitate the dialogue as well as the cultural exchange between scientists, stakeholders, and citizens.

2. Abiotic Stress Resistance at the Physiological Level

Abiotic stress causes a range of changes in morphological, physio-biochemical, and molecular processes in plants [14]. Extreme heat, salt, oxidative stress, and drought are frequently linked and can cause cellular damage either alone or in a combined fashion. The abiotic stresses provide extremely complex stimuli with a wide range of concurrent but distinct characteristics. Each of them has the potential to provide the plant cell with a totally distinct set of environmental cues [15]. On the whole, abiotic stress leads to changes in osmotic balance and ion distribution, which in turn affect both individual cells and the entire plant. Ion and water homeostasis change, causing cellular disturbance, growth arrest, and even death in the most severe cases [16]. Although plant response is one multifaceted and holistic adjustment to the environment, three interrelated activities can be distinguished as crucial for abiotic stress tolerance. The first activity is to stop or lessen the damage, the second one is to restore homeostatic conditions in the new challenging environment, and the third is to restore plant growth (i.e., recovery stage) [17]. Resistance or tolerance must, therefore, assume some flexibility in the metabolic processes that enable plants to survive in harsh conditions (Figure 1). The development in the understanding of plant response to abiotic stress at various levels helps explain these complicated cellular reactions. On a time scale, during abiotic stress, in theory, three phases can be discerned: (1) the phase of alarm; (2) the period of defense; and (3) the phase of collapse [18]. However, an alternative stage should also be considered, the regeneration stage [19]. This is highly crucial and allows the retrieval of various physiological functions of the plant [20].
The stress response is integrated, incorporating several pathways, certain cellular sections, and tissues, and it relies on a battery of signaling molecules to synchronize the response of a specific variation at the organismal level. In response to abiotic stresses, various pathways are activated concurrently (Figure 2). Molecular and genetic investigations have shown that these pathways are highly complex, owing to the diversity of information involved. As plants respond to challenges physiologically, molecularly, and cellularly, it is not a surprise that the transcription of several dissimilar resistance/tolerance genes is also altered [21].

3. Biotechnological Tools to Develop Tolerant Plants against Abiotic Stress

Biotechnological tools include several methods used for plants to develop tolerance to abiotic stress. The genetic transformation of tomato relies highly on the tissue culture technique [22]. Recent advances in the field of plant genetic transformation have enabled the identification of genes that are responsible for tolerance to different environmental stresses [23,24]. Further advancement in understanding the genomics of wild relatives of tomatoes and other Solanaceae has facilitated their exploitation in various breeding programs aiming to introgress genes responsible for abiotic stress resistance in cultivars.

3.1. Genetic Transformation Methods in Tomato

Multiple transformation techniques have been utilized to deliver foreign DNA sequences into an ample range of plant species [25]. The combination of recombinant DNA technologies, genetic transformation, and plant tissue culture are at the core of the production of transgenic plants in a variety of crops [26,27,28,29,30,31,32,33,34,35,36]. In tomato, the first genetic transformation protocol was developed in the 1980s [37], and still today, Agrobacterium-mediated techniques are widely employed for many tomato cultivars [38]. Transformation mediated by the Agrobacterium is a complex process. Briefly, the efficiency of gene delivery into tomato plants depends on various factors, such as the pre-culture of the explants, culture media, culture density, virulence and strain of Agrobacterium, phytohormones, type of explants, vectors, size of DNA insert, and genotype of the recipient plant [39,40]. Table 1 presents a short selection of research efforts devoted to improving the process of tomato genetic transformation. Genetic transformation can also be obtained using A. rizogenes [41]. However, some detrimental phenotypes can be observed in tomato plants, such as shortened internodes, reduced seed setting, and wrinkled leaves. A. rizogenes–mediated transformation can be utilized for the in vitro production of compounds in tomato with biopharmaceutical properties. Besides indirect genetic transformations, direct methods like particle bombardment have also been reported for tomato [42]. This method was optimized by altering factors such as the quality and quantity of DNA, concentration of osmoticum in the tissue culture media, firing separation, and period of particle bombardment to which tomato explants are exposed [43].
Besides the addition of a new DNA sequence or (untargeted) mutation of the tomato genome, recent advances in recombinant DNA technology and reverse genetic approaches, such as antisense technology, RNA interference (RNAi), and genome editing by CRISPR-CAS9, have revolutionized functional genomics in plants. These approaches have been utilized in tomato cultivars to delay their ripening during abiotic stress, such as extreme temperature, by silencing the gene vis 1 [54,55].
Overall, the genetic transformation of tomato is a mature and well-established technique that is employed by numerous laboratories around the world. Although improvements in regeneration and transformation efficiency are always welcome, the production of genetically modified tomatoes should not be considered a limiting factor for biotechnological approaches since efficient and repeatable transformation and regeneration protocols are widely available.

3.2. Transformation Approaches Using rDNA Technologies (Genetic Engineering)

Climate change is predicted to increase the occurrence of abiotic stress, further hampering the ability of plants to yield [56]. Traditional plant breeding has limitations for creating a substantial level of tolerance against abiotic stress because it is time-consuming and often requires a complex breeding scheme to insert multiple sources of variability from wild relatives to a cultivated variety. Recombinant DNA (rDNA) technology–based tools have been traditionally considered alternatives to change the genetic constitution of plants. Different rDNA technologies have been employed to modify the tomato genome so that it can adapt to abiotic stress. These modifications include the exploitation of regulatory genes highly expressed during stress and coding for enzymes whose biochemical or enzymatic activity is useful to counteract abiotic stress [57]. Various examples are reported in Table 2.
Genetic modifications based on sequences that encode compounds involved in stress adaptation are given below.

3.2.1. Mannitol

Mannitol is an important polyol (sugar alcohol) produced from fructose metabolism and serves as a scavenger of free radicals and osmoregulation. The enzyme involved in fructose metabolism to obtain mannitol is mannitol-1-phosphate dehydrogenase, and the corresponding gene encoding this enzyme is mt1D [89,90]. In tomato, the constitutive expression of a bacterial mt1D gene driven by the CaMV 35S promoter provides improved tolerance against chilling, drought, and saline stress [72].

3.2.2. Glycine Betaine

It is an organic compound derived from the amino acid glycine, whose accumulation in plants may occur following abiotic stress. In plants, this compound is considered an organic osmolyte, ensuring, for instance, the regulation and preservation of the thylakoid membrane and, thus, sustaining the photosynthetic efficiency under stress [91]. Various studies have used biotechnological tools, such as the overexpressing of this compound, to facilitate an increased response of plants to abiotic stress tolerance. For example, the expression of the bacterial choline oxidase A (coda) in tomato targeted to the chloroplasts with a transit peptide resulted in an accumulation of glycine betaine in a relatively low (0.09 to 0.30 µmol·g−1 FW) but significant (up to 86% in chloroplasts compared to unstressed control plants) amount, sufficient to enhance tolerance to chilling at various phenological stages, as indicated by an increased yield in stress conditions of the transgenic plants [88].

3.2.3. Glutathione

Glutathione, an important antioxidant performing multiple functions in plants, is synthesized from amino acids (i.e., L-glutamate, cysteine, and glycine). The whole process requires two ATP molecules and is catalyzed by two glutamate enzymes—cysteine ligase (GCL) and glutathione synthetase (GSS). This tripeptide provides protection at cellular and tissue levels in response to various reactive oxygen species (ROS), such as peroxides, superoxides, and hydroxyl radicals [92]. Glutathione has an important role during induced stress. The constitutive expression in tomato of a Se-independent glutathione peroxidase (GPx5) from Mus musculus resulted in an increased tolerance to mechanical stress [93]. Similarly, the concurrent constitutive expression of two glyoxalase (GlyI and GlyII) from Brassica juncea in tomato showed a reduced growth depression and membrane damage (as indicated by the level of lipid peroxidation and hydrogen peroxide production in leaves) following long-term exposure (3 months) to salinity (up to 800 mM NaCl) [94].

3.2.4. Osmotin

Osmotin is a 26 kDa protein, a member of the PR-5 family, which also includes zeamatin and thaumatin. It accumulates in plants as a defense mechanism against abiotic stress because of its prominent role in osmoregulation [95]. It has been reported that tomatoes constitutively expressing an osmotin gene from Nicotiana tabacum have higher levels of proline, increased chlorophyll contents, and higher water contents (under stress). These features were considered crucial in helping tomato withstand salt stress (150 mM NaCl for 10 days) [87]. The osmotin from N. tabacum was also used to increase pathogen resistance in transgenic barley, while it did not have a significant impact on insect-borne virus infections (by aphids and leafhoppers) [96]

3.2.5. Polyamines

Polyamine (PA) is a term used to indicate the wide class of organic molecules having multiple (more than two) amino acid groups. In plants, naturally occurring, low molecular–weight polyamines are associated with embryogenesis, organogenesis, anthesis, fruit development, ripening, and leaf senescence, but there is also evidence of their role in stress response [95]. The most common and abundant PAs in plants are putrescine (a diamine) and its derivatives spermidine and spermine [97]. Tomato transformed to constitutively express the arginine decarboxylase gene from Poncirus trifoliata (PtADC), indirectly involved in the biosynthesis of putrescine, showed increased levels of free PAs and improved tolerance to leaf dehydration and drought stress [98]. Tomato genetically transformed to constitutively overexpress the tomato SlSAMS1 gene accumulated PAs and hydrogen peroxide and had an improved alkali stress tolerance. This gene is a member of the S-adenosylmethionine synthetase (SAMS) family, and it is stress-inducible. These genes catalyze the formation of SAM, which is also a precursor to PAs [99].

3.2.6. Trehalose

Trehalose is a highly soluble disaccharide made of glucose subunits, and it is present in a wide range of organisms, including prokaryotes, algae, mosses, fungi, protozoa, and mammals. Trehalose appears to be able to play a special function as a stress metabolite protecting the integrity of the cell against environmental stress and nutrient limitations [100]. Traditionally, trehalose has been of little importance for angisoperms, where another non-reducing saccharide, sucrose, has a predominant role in carbon storage and transport. Nonetheless, the discovery of gene families encoding trehalose phosphate synthases (TPSs) and trehalose phosphatases, along with their subsequent functional characterization, indicated that trehalose acts mainly as an osmoprotectant and as a signal molecule involved in stress response. Recombinant DNA technologies have made it possible to modify genes governing trehalose metabolism in tomato. For example, the constitutive expression of Saccaromyces cerevisiae ScTPS1 improved tolerance against drought or salt. Nonetheless, transgenic plants had phenotypic abnormalities and alterations in carbohydrate biosynthesis [101].

3.2.7. Biosynthesis of Ethylene

Ethylene is a well-known plant hormone whose commercial derivatives are also used to induce post-harvest tomato ripening. Because of its applied importance, there are several studies on genetically modified tomato cultivars with altered ethylene pathways in relation to fruit maturation. Ethylene production is typically increased in stressful environmental conditions. Several works have demonstrated that one of the positive effects of plant growth–promoting rhizobacteria (PGPR) is lowering the ethylene level under stress by cleaving and deaminating aminocyclopropane-1-carboxylic acid (ACC), the precursor of ethylene, by ACC-deaminases [102]. Tomato cultivars expressing a bacterial ACC deaminase under constitutive and inducible promoters were more tolerant to flooding [103].

3.2.8. Aquaporins

Aquaporins (AQPs) are trans-membrane proteins that allow the movement of water and small solutes between and within cells. Numerous studies have reported the potential roles of aquaporins in relation to abiotic stress in plants, water use efficiency (WUE), and solute transport in plants [104,105]. In tomato, over forty members of the AQP gene family have been linked to abiotic stress and plant development, mainly because of their expression pattern [106]. The overexpression of genes regulating the formation and functioning of aquaporins, such as SlTIP;2, in tomato increased the tolerance to abiotic stress. Interestingly, transgenic plants were more productive and had higher biomass than untransformed controls in normal and drought conditions [107]. An AQP from apple (MdPIP1;3) was also used to increase fruit growth rate and size mainly thanks to bigger cells, also increasing tolerance to drought stress [86]. Similarly, the overexpression of SlPIP2;1 conferred to tomato’s higher hydraulic conductivity and tolerance against drought stress [108,109].

3.2.9. Heat Shock Proteins

A set of relatively conserved, ubiquitous proteins, referred to as heat shock proteins, are synthesized by virtually all organisms, including plants, in response to various environmental stresses. These proteins often serve as intracellular chaperones and, for the establishment of protein-protein interaction, are involved in protein folding, assembly, translocation, degradation, and transport [110]. Different genes encoding HSPs (e.g., HsfA1, HsfA2, HsfB1, LeHSP 17.6) have been identified and delivered to tomato to facilitate the production of HSPs, with the common aim of helping plants better adapt to stress [111,112]. Moreover, the overexpression in tomato of LeHSP21.5 diminished tunicamycin-induced ER stress [85]. Tunicamycin is an antibiotic that inhibits protein N-glycosylation, hence, inducing misfolded glycoproteins, and it is experimentally used to induce the unfolded protein response in living organisms. Furthermore, other plant chaperonins have been employed to increase the stress resistance in tomato [113]. For example, the overexpression of the tomato SlDnaJ20 relieved ROS accumulation by ensuring high levels of SOD and APX activities and was associated with higher fresh weights of six-week-old plants under heat stress [114].

3.2.10. Antioxidants

Many antioxidants have been reported in plants that act as buffers to regulate the redox potential of cells. Among antioxidant enzymes, the most exploited in plant biotechnology are probably glutaredoxins, catalases, ascorbate peroxidases (APX), and superoxide dismutases (SOD). Just to give a few examples of applications, a catalase gene (katE) from E. coli, introduced in the chloroplast genome of tomato under the RBCS promoter, increased catalase activity and better protected plants from oxidative stress induced by high light intensity, drought, or low temperature, compared to the untransformed control [76]. An ascorbate peroxidase from tomato (LetAPX) was expressed in Arabidopsis and conferred resistance to cold (4 °C for up to 24 h) [115]. Genetically modified tomato cultivars expressing the A. thaliana Fe-SOD gene promoted the increased performance and stability of the photosynthetic apparatus under UV stress [58].

3.2.11. Ion Transport Proteins

Cation and anion transporters comprise a large class of transmembrane proteins vital for any organism, serving the purpose of moving ions and other small molecules within and between cells. These proteins are fundamental for ion homeostasis and are involved in salt stress resistance because they participate in sodium and chloride uptake, translocation, and cellular compartmentalization [116]. Numerous investigations have reported that genes like HAL1 and HAL5, encoding ion transport proteins in S. cerevisiae, when delivered to tomato using recombinant DNA technology, increased the tolerance of toward salinity [117]. Similarly, the A. thaliana AtNHX1 gene inserted in the tomato genome resulted in improved salinity tolerance [118]. In both cases, a positive effect was associated with an improved K/Na ratio under saline conditions. The importance of K homeostasis in the tolerance to NaCl stress was also demonstrated by overexpressing the endosomal LeNHX2 ion transporter [70,113].

4. Genome Editing for Ameliorating Abiotic Stresses in Tomato

New research tools and techniques are now available for creating abiotic stress-tolerant crop cultivars. The development of resistance to abiotic stress in crops through conventional breeding methods (e.g., crossing between two contrasting parental plants) has some drawbacks, such as the complex genetic base of the phenotypic features related to abiotic stress adaptation, and significant achievements have not been obtained [119,120]. Genetic engineering approaches based on the insertion of a transgene are restricted in certain areas of the world. Thus, to supply to the world’s rising population, there is great hope in genome editing tools, which are expected to revolutionize the world’s agriculture [121]. In tomato, genome editing has been performed for different genes, and resistance to abiotic stress has been obtained. For instance, the alteration of HyPRP1 (hybrid proline-rich protein 1) using CRISPR/CAS9 has resulted in salinity stress tolerance in mutagenized tomato lines [122]. Similarly, cold stress tolerance in tomatoes was obtained by mutation through CRISPR/CAS9 in the C-repeat binding factor 1 (CBF1) gene of tomato. The tomatoes with the cbf1 mutation were more vulnerable to stress and had increased electrolyte leakage [123]. To establish its function in tomato drought tolerance, the CRISPR/Cas9 method was recently utilized to create mutated strains for the tomato gene NPR1 (non-expresser of pathogenesis-related gene 1) [124]. S1NPR1 is essential for managing drought stress, and a variety of SlNPR1 variations may be created through genome editing to give tomato and other crops broad-spectrum drought tolerance.

5. Conclusions

Abiotic stress negatively influences the growth and yield of crops by disrupting their morpho-physio-biochemical and molecular activities. However, plants have evolved multiple counter-mechanisms. Advances in rDNA technology have made increasing the resistance to various abiotic stresses possible [77]. These recombinant DNA technologies are highly time-efficient compared to classic breeding and widely applicable to multiple plant species [38]. Despite the scientific and technological efficacy of biotechnological approaches, briefly presented in this review, there will always be constraints that can hamper the widespread diffusion of biotech tomatoes with abiotic stress tolerance. In different countries, this germplasm is subjected to a series of strict safety regulations, even when compared to genotypes derived from random mutagenesis programs. Currently, there is a strong debate on the possible legal distinction between plants obtained through classic genetic transformation (i.e., based on the transgene insertion) and plants developed using gene-editing approaches, such as CRISPR-CAS9. A strong argument that limits this distinction is that, in the EU (where GMOs are extensively regulated) any “organism in which the genetic material (DNA) has been altered in a way that does not occur naturally by mating or natural recombination”—and coherently, also plants obtained by site-directed mutagenesis—“are subject to the obligations laid down by the GMO Directive” (European Court of Justice ruling of case C-528/16, 2018; https://curia.europa.eu, accessed on the 1 December 2022). Transgenic plants are the most common GMOs but not the only possible GMOs. In the EU, GMOs can be eventually marketed only after a scientific assessment of the risks to health and the environment. Under the current legal framework, any molecular biology technique that induces DNA variations with a mechanism that does not occur in nature will generate a GMO. We would like to conclude that, rather than focusing on the technique that alters the DNA or the source of the genetic material, a less stringent legal framework and a less complex and onerous authorization procedure can be perhaps granted for organisms modified using BBA because this approach can better achieve the development of modified varieties within the functional range potentially obtainable by conventional methods or classic mutagenesis.

Author Contributions

Conceptualization, G.K.R., P.K. and G.C.; methodology, G.K.R., D.M.K., S.M.C., S.C., R.K. and I.M.; Tables and Figures, R.K., S.M.C., S.C., B.K. and I.M.; writing—original draft preparation, G.K.R. and P.K.; writing—review and editing, P.K., R.R.K., C.R., T.K.B., Y.R. and G.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Khapte, P.S.; Kumar, P.; Saxena, A.; Singh, A. Performance evaluation and character association studies in arid region greenhouse tomato hybrids. Indian J. Hortic. 2018, 75, 457–462. [Google Scholar] [CrossRef]
  2. FAOSTAT. 2020. Available online: http://faostat3.fao.org/home/E (accessed on 12 September 2022).
  3. Singh, H.; Kumar, P.; Chaudhari, S.; Edelstein, M. Tomato grafting: A global perspective. HortScience 2017, 52, 1328–1336. [Google Scholar] [CrossRef] [Green Version]
  4. Chaudhry, Z.; Rashid, H. An improved Agrobacterium-mediated transformation in tomato using hygromycin as a selective agent. Afr. J. Biotechnol. 2010, 9, 1882–1891. [Google Scholar]
  5. Sanwal, S.K.; Mann, A.; Kumar, A.; Kesh, H.; Kaur, G.; Rai, A.K.; Kumar, R.; Sharma, P.C.; Kumar, A.; Bahadur, A.; et al. Salt Tolerant Eggplant Rootstocks Modulate Sodium Partitioning in Tomato Scion and Improve Performance under Saline Conditions. Agriculture 2022, 12, 183. [Google Scholar] [CrossRef]
  6. Behera, T.K.; Krishna, R.; Ansari, W.A.; Aamir, M.; Kumar, P.; Kashyap, S.P.; Pandey, S.; Kole, C. Approaches Involved in the Vegetable Crops Salt Stress Tolerance Improvement: Present Status and Way Ahead. Front. Plant Sci. 2022, 12, 787292. [Google Scholar] [CrossRef] [PubMed]
  7. Colla, G.; Kumar, P.; Cardarelli, M.; Rouphael, Y. Grafting an effective tool for abiotic stress alleviation in vegetables. In Horticulture for Food and Environment Security; Chadha, K.L., Singh, A.K., Singh, S.K., Dhillon, W.S., Eds.; West Ville Pub. House: New Delhi, India, 2013; pp. 15–28. [Google Scholar]
  8. Rouphael, Y.; Venema, J.H.; Edelstein, M.; Savvas, D.; Colla, G.; Ntatsi, G.; Kumar, P.; Schwarz, D. Grafting as a tool for tolerance of abiotic stress. In Vegetable Grafting: Principles and Practices; Colla, G., Perez-Alfocea, F., Schwarz, D., Eds.; CAB International: Wallingford, UK, 2017; pp. 171–215. [Google Scholar]
  9. Lin, K.H.; Lo, H.F.; Lee, S.P.; Kuo, C.G.; Chen, J.T. RAPD markers for the identification of yield traits in tomatoes under heat stress via bulk segregant analysis. Heredity 2006, 143, 142–154. [Google Scholar] [CrossRef]
  10. Ranjan, A.; Ichihashi, Y.; Sinha, N.R. The tomato genome: Implications for plant breeding, genomics and evolution. Genome Biol. 2012, 13, 167. [Google Scholar] [CrossRef]
  11. Chen, Q.; Lai, H. Gene delivery into plant cells for recombinant protein production. BioMed Res. Int. 2015, 2015, 932161. [Google Scholar] [CrossRef] [Green Version]
  12. Low, L.; Yang, S.; Kok, D.A.; Ong-Abdullah, J.; Tan, N.; Lai, K. Transgenic Plants: Gene Constructs, Vector and Transformation Method. In New Visions in Plant Science; IntechOpen: London, UK, 2018; pp. 41–61. [Google Scholar] [CrossRef]
  13. Kissoudis, C.; Chowdhury, R.; van Heusden, S.; van de Wiel, C.; Finkers, R.; Visser, R.G.F.; Bai, Y.; van der Linden, G. Combined biotic and abiotic stress resistance in tomato. Euphytica 2015, 202, 317–332. [Google Scholar] [CrossRef] [Green Version]
  14. Kumar, P.; Rouphael, Y.; Cardarelli, M.; Colla, G. Vegetable grafting as a tool to improve drought resistance and water use efficiency. Front. Plant Sci. 2017, 8, 1130. [Google Scholar] [CrossRef]
  15. Nicky, J.A.; Urwin, P.E. The interaction of plant biotic and abiotic stresses: From genes to the field. J. Exp. Bot. 2012, 63, 3523–3543. [Google Scholar] [CrossRef] [Green Version]
  16. Miller, M.A.; Zachary, J.F. Mechanisms and Morphology of Cellular Injury, Adaptation, and Death. Pathol. Basis Vet. Dis. 2017, 2017, 2–43.e19. [Google Scholar] [CrossRef]
  17. Zhu, J.K. Plant salt tolerance. Trends Plant Sci. 2001, 6, 66–71. [Google Scholar] [CrossRef] [PubMed]
  18. Rehem, B.C.; Bertolde, Z.F.; de Almeida, A.F. Regulation of gene expression in response to abiotic stress in plants. In Cell Metabolism—Cell Homeostasis and Stress Response; Bubulya, P., Ed.; IntechOpen: London, UK, 2012. [Google Scholar] [CrossRef] [Green Version]
  19. Lichtenthaler, H.K. (Ed.) In vivo chlorophyll fluorescence as a tool for stress detection in plants. In Applications of Chlorophyll Fluorescence; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1988; pp. 129–142. [Google Scholar]
  20. Yamaguchi-Shinozaki, K.; Shinozaki, K. DREB regulons in abiotic-stress-responsive gene expression in plants. In Molecular Breeding of Forage and Turf; Yamada, T., Spangenberg, G., Eds.; Springer: New York, NY, USA, 2009; pp. 15–28. [Google Scholar] [CrossRef]
  21. Hoang, X.L.T.; Nhi, D.N.H.; Thu, N.B.A.; Thao, N.P.; Tran, L.P. Transcription Factors and Their Roles in Signal Transduction in Plants under Abiotic Stresses. Curr. Genom. 2017, 18, 483–497. [Google Scholar] [CrossRef]
  22. Ishida, Y.; Hiei, Y.; Komari, T. Tissue culture protocols for gene transfer and editing in maize (Zea mays L.). Plant Biotechnol. 2020, 37, 121–128. [Google Scholar] [CrossRef]
  23. Gerszberg, A.; Hnatuszko-Konka, K. Tomato tolerance to abiotic stress: A review of most often engineered target sequences. Plant Growth Regul. 2017, 83, 175–198. [Google Scholar] [CrossRef] [Green Version]
  24. Parmar, N.; Singh, K.H.; Sharma, D.; Singh, L.; Kumar, P.; Nanjundan, J.; Khan, Y.J.; Chauhan, D.K.; Thakur, A.K. Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: A comprehensive review. 3Biotech 2017, 7, 239. [Google Scholar] [CrossRef]
  25. Hnatuszko-Konka, K.; Kowalczk, T.; Gerszberg, A.; Wiktorek-Smagur, A.; Kononowicz, A.K. Phaseolus vulgaris—Recalcitrant potential. Biotechnol. Adv. 2014, 32, 1205–1215. [Google Scholar] [CrossRef]
  26. Yang, N.S.; Christou, P. (Eds.) Particle Bombardment Technology for Gene Transfer; Oxford University Press: New York, NY, USA, 1994; pp. 143–165. [Google Scholar]
  27. Mathews, H.; Wagoner, W.; Cohen, C.; Kellogg, J.; Bestwick, R. Efficient genetic transformation of red raspberry, Rubus ideaus L. Plant Cell Rep. 1995, 14, 471–476. [Google Scholar] [CrossRef]
  28. Hilder, V.A.; Boulter, D. Genetic engineering of crop plants for insect resistance—A critical review. Crop Prot. 1999, 18, 177–191. [Google Scholar] [CrossRef]
  29. Gosal, S.S.; Gosal, S.K. Genetic transformation and production of transgenic plants. In Plant Biotechnology—Recent Advances; Trivedi, P.C., Ed.; Panima Publishers: New Delhi, India, 2000; pp. 29–40. [Google Scholar]
  30. Chahal, G.S.; Gosal, S.S. Principles and Procedures of Plant Breeding: Biotechnological and Conventional Approaches; Narosa Publishing House: New Delhi, India, 2002. [Google Scholar]
  31. Altman, A. From plant tissue culture to biotechnology: Scientific revolutions, abiotic stress and new advances in crop improvement. Theor. Appl. Genet. 2003, 129, 1639-16. [Google Scholar]
  32. Grewal, D.K.; Gill, R.; Gosal, S.S. Genetic engineering of Oryza sativa by particle bombardment. Biol. Plant 2006, 50, 311–314. [Google Scholar] [CrossRef]
  33. Kerr, A. GM crops—A minireview. Australas. Plant Pathol. 2011, 40, 449–452. [Google Scholar] [CrossRef]
  34. Kamthan, A.; Chaudhuri, A.; Kamthan, M.; Datta, A. Genetically modified (GM) crops: Milestones and new advances in crop improvement. Theor. Appl. Genet. 2016, 129, 1639–1655. [Google Scholar] [CrossRef] [PubMed]
  35. Arora, L.; Narula, A. Gene editing and crop improvement using CRISPR-Cas9 system. Biol. Plant 2017, 50, 311–314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Tanuja, P.; Kumar, A.L. Transgenic fruit crops—A review. Int. J. Curr. Microbiol. Appl. Sci. 2017, 6, 2030–2037. [Google Scholar] [CrossRef] [Green Version]
  37. McCormick, S.; Niedermeyer, J.; Fry, J.; Barnason, A.; Horsch, R.; Fraley, R. Leaf disc transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens. Plant Cell Rep. 1986, 2, 81–84. [Google Scholar] [CrossRef]
  38. Gerszberg, A.; Hnatuszko-Konka, K.; Kowalczyk, T.; Kononowicz, A.K.K. Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell Tissue Organ Cult. 2015, 120, 881–902. [Google Scholar] [CrossRef] [Green Version]
  39. Shah, S.H.; Ali, S.; Jan, S.A.; Din, A.U.; Ali, G.M. Piercing and incubation method of in planta transformation producing stable transgenic plants by overexpressing DREB1A gene in tomato (Solanum lycopersicum Mill.). Plant Cell Tissue Organ Cult. 2015, 120, 1139–1157. [Google Scholar] [CrossRef]
  40. Sun, S.X.P.; Xing, X.J.; Xu, X.Y.; Cheng, J.; Zheng, S.W.; Xing, G.M. Agrobacterium-mediated transformation of tomato (Lycopersicon esculentum L. cv. Hezuo908) with improved efficiency. Biotechnol. Biotechnol. Equip. 2015, 29, 861–868. [Google Scholar] [CrossRef]
  41. Chetty, V.J.; Ceballos, N.; Garcia, D.; Narvaez-Vasquez, J.; Lopez, W.; Orozco-Cardenas, M.L. Evaluation of four Agrobacterium tumefaciens strains for the genetic transformation of tomato (Solanum lycopersicum L.) cultivar Micro-Tom. Plant Cell Rep. 2013, 32, 239–247. [Google Scholar] [CrossRef] [PubMed]
  42. Cueno, M.C.; Hibi, Y.; Karamatsu, K.; Yasutomi, Y.; Imai, K.; Laurena, A.C.; Okamoto, T. Preferential expression and immunogenicity of HIV-1 Tatfusion protein expressed in tomato plant. Transg. Res. 2010, 19, 889–895. [Google Scholar] [CrossRef] [PubMed]
  43. Ruma, D.; Dhaliwal, M.S.; Kaur, A.; Gosal, S.S. Transformation of tomato using biolistic gun for transient expression β glucuronidase gene. Indian J. Biotechnol. 2009, 8, 363–369. [Google Scholar]
  44. Hasan, M.; Khan, A.J.; Khan, S.S.; Shah, A.H.; Khan, A.R.; Mirza, B. Transformation of tomato (Lycopesricon esculentum Mill.) with Arabidopsis early flowering gene APETALI (API) through Agrobacterium infiltration of ripened fruits. Pak. J. Bot. 2008, 1, 161–173. [Google Scholar]
  45. Guo, M.; Zhang, Y.L.; Meng, Z.J.; Jiang, J. Optimization of factors affecting Agrobacterium-mediated transformation of MicroTom tomatoes. Genet. Mol. Res. 2012, 1, 661–671. [Google Scholar] [CrossRef]
  46. Moghaieb, R.E.; Saneoka, H.; Fujita, K. Shoot regeneration from GUS-transformed tomato (Lycopersicon esculentum) hairy root. Cell. Mol. Biol. 2004, 9, 439–449. [Google Scholar]
  47. Abu-El-Heba, G.A.; Hussein, G.M.; Abdalla, N.A. A rapid and efficient tomato regeneration and transformation system. Agric. For. Res. 2008, 58, 103–110. [Google Scholar]
  48. Fuentes, A.D.; Ramos, P.L.; Sanchez, Y.; Callard, D.; Ferreira, A.; Tiel, K.; Cobas, K.; Rodriguez, R.; Borroto, C.; Doreste, V.; et al. A transformation procedure for recalcitrant tomato by addressing transgenic plant-recovery limiting factors. Biotechnol. J. 2008, 3, 1088–1093. [Google Scholar] [CrossRef]
  49. Sharma, M.K.; Solanke, A.U.; Jani, D.; Singh, Y.; Sharma, A.K. Asimple and efficient Agrobacterium-mediated procedure for transformation of tomato. J. Biosci. 2009, 3, 423–433. [Google Scholar] [CrossRef]
  50. Janani, C.; Girija, S.; Ranjitha Kumari, B.D. In vitro culture and Agrobacterium-mediated transformation in high altitude tomato (Lycopersicon esculentum Mill.) cultivar Shalimar. Int. J. Pharm. Teach. Pract. 2013, 4, 483–488. [Google Scholar]
  51. Cruz-Mendıvil, A.; Rivera-Lopez, J.; German-Baez, L.J.; Lopez-Meyer, M.; Hernandez-Verdugo, S.; Lopez-Valenzuela, J.A.; Reyes-Moreno, C.; Valdez-Ortiz, A. A simple and efficient protocol for plant regeneration and genetic transformation of tomato cv. Micro-Tom from leaf explants. HortScience 2011, 46, 1655–1660. [Google Scholar] [CrossRef] [Green Version]
  52. Kaur, P.; Bansal, K.C. Efficient production of transgenic tomatoes via Agrobacterium-mediated transformation. Biol. Plant. 2010, 54, 344–348. [Google Scholar] [CrossRef]
  53. El-Siddig, M.A.; El-Hussein, A.A.; Saker, M.M. Agrobacterium-mediated transformation of tomato plants expressing defensin gene. Int. J. Agric. Res. 2011, 4, 323–334. [Google Scholar] [CrossRef] [Green Version]
  54. Metwali, E.M.R.; Soliman, H.I.A.; Fuller, M.P.; Almaghrabi, O.A. Improving fruit quality in tomato (Lycoper sicum esculentum Mill) under heat stress by silencing the vis 1 gene using small interfering RNA technology. Plant Cell Tissue Organ Cult. 2015, 121, 153–166. [Google Scholar] [CrossRef]
  55. Wang, T.; Wen, L.W.; Zhu, H.L. Effectively organ-specific virus induced gene silencing in tomato plant. J. Nat. Sci. 2015, 1, 34. [Google Scholar]
  56. Mishra, K.B.; Ianacone, R.; Petrozza, A.; Mishra, A.; Armentano, N.; La Vecchia, G.; Trtilek, M.; Cellini, F.; Nedbal, L. Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Sci. 2012, 182, 79–86. [Google Scholar] [CrossRef]
  57. Vincour, B.; Altman, A. Recent advances in engineering plant tolerance to abiotic stress: Achievements and limitations. Curr. Opin. Biotechnol. 2005, 16, 123–132. [Google Scholar] [CrossRef]
  58. Baranova, E.N.; Serenko, E.K.; Balachnina, T.I.; Kosobruhov, A.A.; Kurenina, L.V.; Gulevich, A.A.; Maisuryan, A.N. Activity of the photosynthetic apparatus and antioxidant enzymes in leaves of transgenic Solanum lycopersicum and Nicotiana tabacum plants, with FeSOD1 gene. Russ. Agric. Sci. 2010, 36, 242–249. [Google Scholar] [CrossRef]
  59. Alvarez-Gomez, T.B.; Ramirez-Trujillo, J.A.; Ramirez-Yanez, M.; Suarez-Rodriguez, R. Overexpression of SIERF3b and SIERF5 in transgenic tomato alters fruit size, number of seeds and promotes early flowering, tolerance to abiotic stress and resistance to Botrytis cinereal infection. Ann. Appl. Biol. 2021, 179, 382–394. [Google Scholar] [CrossRef]
  60. Dominguez, T.; Hernandez, L.M.; Pennycooke, J.C.; Jimenez, P.; Martınez-Rivas, J.M.; Sanz, C.; Stockinger, E.J.; Sanchez-Serrano, J.; Sanmartin, M. Increasing v-3 desaturase expression in tomato results in altered aroma profile and enhanced resistance to cold stress. Plant Physiol. 2010, 153, 655–665. [Google Scholar] [CrossRef] [Green Version]
  61. Gong, B.; Wang, X.; Wei, M.; Yang, F.; Li, Y.; Shi, Q. Overexpression of S-adenosylmethionine synthetase1 enhances tomato callus tolerance to alkali stress through polyamine and hydrogen peroxide cross-linked networks. Plant Cell Tissue Organ Cult. 2015, 124, 377–391. [Google Scholar] [CrossRef]
  62. Yang, D.Y.; Li, M.; Ma, N.N.; Yang, X.H.; Meng, Q.W. Tomato SlGGP-LIKE gene participates in plant responses to chilling stress and pathogenic infection. Plant Physiol. Biochem. 2017, 112, 218–226. [Google Scholar] [CrossRef] [PubMed]
  63. Zhu, M.; Meng, X.; Cai, J.; Li, G.; Dong, T.; Li, Z. Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biol. 2018, 10, 83. [Google Scholar] [CrossRef] [Green Version]
  64. Yuling Bai, Y.B.; Sri Sunarti, S.S.; Christos Kissoudis, C.K.; Richard, G.F.; Visser, C.G.; van der Linden, C. The Role of Tomato WRKY Genes in Plant Responses to Combined Abiotic and Biotic Stresses. Plant Sci. 2018, 9, 801. [Google Scholar] [CrossRef] [Green Version]
  65. Zhang, L.; Wu, M.; Teng, Y.; Jia, S.; Yu, D.; Wei, T.; Chen, C.; Song, W. Overexpression of the Glutathione Peroxidase 5 (RcGPX5) Gene from Rhodiola crenulata Increases Drought Tolerance in Salvia miltiorrhiza. Plant Sci. 2019, 9, 1950. [Google Scholar] [CrossRef] [PubMed]
  66. Fernando Novillo, F.N.; Joaquın Medina, J.M.; Julio Salinas, J.S. Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulation. Proc. Natl. Acad. Sci. USA 2007, 104, 21002–21007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Hu, D.G.; Wang, S.H.; Luo, H.; Ma, Q.J.; Yao, Y.X.; You, C.X.; Hao, Y.J. Overexpression of MdVHA-B, a V-ATPase gene from apple, confers tolerance to drought in transgenic tomato. Sci. Hortic. 2012, 145, 94–101. [Google Scholar] [CrossRef]
  68. Hu, D.G.; Ma, Q.J.; Sun, C.H.; Sun, M.H.; You, C.X.; Hao, Y.J. Overexpression of MdSOS2L1, a CIPK protein kinase, increases the antioxidant metabolites to enhance salt tolerance in apple and tomato. Physiol. Plant 2015, 156, 201–214. [Google Scholar] [CrossRef]
  69. Rahman, M.A.; Wu, W.; Yan, Y.; Shamsul, A. Bhuiyan Overexpression of TERF1 in sugarcane improves tolerance to drought stress. Crop Pasture Sci. 2021, 72, 268–279. [Google Scholar] [CrossRef]
  70. Huertas, R.; Rubio, L.; Cagnac, O.; Garcia-Schanchez, M.J.; De Dios Alche, J.; Venema, K.; Fernandez, J.A.; Rodriguez-Rosales, M.P. The K+/H+ antiporter LeNHX2 increases salt tolerance by improving K+ homeostasis in transgenic tomato. Plant Cell Environ. 2013, 36, 2135–2149. [Google Scholar] [CrossRef]
  71. Li, Z.; Palmer, W.M.; Antony, P.; Wang, M.R.; Rainsford, F.; Jin, Y.; Patrick, J.W.; Yang, Y.; Ruan, Y.-L. High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J. Exp. Bot. 2011, 63, 1155–1166. [Google Scholar] [CrossRef] [PubMed]
  72. Khare, N.; Goyary, D.; Kumar Singh, N.; Shah, P.; Rathore, M.; Anandhan, S.; Sharma, D.; Arif, M.; Ahmed, Z. Transgenic tomato cv. Pusa uphar expressing a bacterial mannitol-1-phosphate dehydrogenase gene confers abiotic stress tolerance. Plant Cell Tissue Organ Cult. 2010, 103, 267–277. [Google Scholar] [CrossRef]
  73. Liu, X.; Yang, J.H.; Li, B.; Yang, X.M.; Meng, Q.W. Antisense expression of tomato chloroplast omega-3 fatty acid desaturase gene (LeFAD7) enhances the tomato high-temperature tolerance through reductions of trienoic fatty acids and alterations of physiological parameters. Photosyntheyhica 2010, 1, 59–66. [Google Scholar] [CrossRef]
  74. Lyu, J.I.; Min, S.R.; Lee, J.H.; Lim, Y.H.; Kim, J.K.; Bae, C.H.; Liu, J.R. Overexpression of a trehalose-6-phosphate synthase/phosphatise fusion gene enhances tolerance and photosynthesis during drought and salt stress without growth aberrations in tomato. Plant Cell Tissue Organ Cult. 2013, 112, 257–262. [Google Scholar] [CrossRef]
  75. Miura, K.; Shiba, H.; Ohta, M.; Seung Kang, W.; Sato, A.; Yuasa, T.; Iwaya-Inoue, M.; Kamada, H.; Ezura, H. SlICE1 encoding a MYC-type transcription factor controls cold tolerance intomato, Solanum lycopersicum. Plant Biotechnol. 2012, 29, 253–260. [Google Scholar] [CrossRef]
  76. Mohamed, E.A.; Iwaki, T.; Munir, I.; Tamoi, M.; Shigeoka, S.; Wadano, A. Overexpression of bacterial catalase in tomato leaf chloroplasts enhances photo-oxidative stress tolerance. Plant Cell Environ. 2003, 26, 2037–2046. [Google Scholar] [CrossRef]
  77. Muñoz-Mayor, M.F.; Pineda, B.; Garcia-Abellan, J.O.; Antón, T.; GarciaSogo, B.; Sanchez-Bel, P.; Flores, F.B.; Atarés, A.; Angosto, T.; Pintor-Toro, J.A.; et al. Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. J. Plant Physiol. 2012, 169, 459–468. [Google Scholar] [CrossRef] [PubMed]
  78. Park, E.J.; Jenknic, Z.; Chen, T.H.H. Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol. 2006, 6, 706–714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Rai, A.C.; Singh, M.; Shah, K. Engineering drought tolerant tomato plants over-expressing BcZAT12 gene encoding a C2H2 zinc finger transcription factor. Phytochemistry 2013, 85, 44–50. [Google Scholar] [CrossRef]
  80. Seong, E.S.; Cho, H.S.; Choi, D.; Joung, Y.H.; Lim, C.K.; Hur, J.H.; Wang, M.H. Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress. Biochem. Biophys. Res. Commun. 2007, 363, 983–988. [Google Scholar] [CrossRef]
  81. Shah, K.; Singh, M.; Rai, A.C. Effect of heat-shock induced oxidative stress is suppressed in BcZAT12 expressing drought tolerant tomato. Phytochemistry 2013, 95, 109–117. [Google Scholar] [CrossRef] [PubMed]
  82. Wang, B.Q.; Zhang, Q.F.; Liu, J.H.; Li, G.H. Overexpression of PtADC confers enhanced dehydratation and drought tolerance in transgenic tobacco and tomato: Effect on ROS elimination. Biochem. Biophys. Res. Commun. 2011, 413, 10–16. [Google Scholar] [CrossRef] [PubMed]
  83. Wang, H.S.; Yu, C.; Tang, X.F.; Zhu, Z.J.; Ma, N.N.; Meng, Q.W. Atomato endoplasmic reticulum (ER)-type omega-3 fatty acidd esaturase (LeFAD3) functions in early seedling tolerance to salinity stress. Plant Cell Rep. 2014, 33, 131–142. [Google Scholar] [CrossRef] [PubMed]
  84. Yarra, R.; He, S.J.; Abbagani, S.; Ma, B.; Bulle, M.; Zhang, W.K. Overexpression of wheat Na+/H+ antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tissue Organ Cult. 2012, 111, 49–57. [Google Scholar] [CrossRef]
  85. Saha, B.C.; Racine, F.M. Effects of pH and corn steep liquor variability on manitol production by Lactobaccilus. NRRL B-3693. Appl. Microb. Biotechnol. 2010, 87, 553–560. [Google Scholar] [CrossRef]
  86. Dai, Q.M.; Mu, W.; Zhang, T. Recent advances in the applications and biotechnological production of manitol. J. Func. Foods 2017, 36, 404–409. [Google Scholar] [CrossRef]
  87. Chen, T.H.H.; Murata, N. Glycine betaine protects plants against abiotic stress: Mechanisms and biotechnological applications. Plant Cell Environ. 2010, 34, 1–20. [Google Scholar] [CrossRef]
  88. Park, E.J.; Jeknić, Z.; Sakamoto, A.; DeNoma, J.; Yuwansiri, R.; Murata, N.; Chen, T.H.H. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J. 2004, 40, 474–487. [Google Scholar] [CrossRef]
  89. Hossain, M.A.; Piyatida, P.; Teixeira da Silva, J.A.; Fujita, M. Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 2012, 872875. [Google Scholar] [CrossRef] [Green Version]
  90. Herbette, S.; Tourvieille de Labrouheb, D.; Drevet, J.R.; Roeckel-Drevet, P. Transgenic tomatoes showing higher glutathione peroxydase antioxidant activity are more resistant to an abiotic stress but more susceptible to biotic stresses. Plant Sci. 2011, 180, 548–553. [Google Scholar] [CrossRef]
  91. Alvarez-Viveros, M.F.; Inostroza-Blancheteau, C.; Timmermann, T.; González, M.; Arce-Johnson, P. Overexpression of GlyI and GlyII genes in transgenic tomato (Solanum lycopersicum Mill.) plants confers salt tolerance by decreasing oxidative stress. Mol. Biol. Rep. 2013, 4, 3281–3290. [Google Scholar] [CrossRef]
  92. Ram, C.; Danish, S.; Kesawat, M.S.; Panwar, B.S.; Verma, M.; Arya, A.; Yadav, S.; Sharma, V. Genome-wide comprehensive characterization and expression analysis of TLP gene family revealed its responses to hormonal and abiotic stresses in watermelon (Citrullus lanatus). Gene 2022, 844, 146818. [Google Scholar] [CrossRef] [PubMed]
  93. Goel, D.; Singh, A.K.; Yadav, V.; Babbar, S.B.; Bansal, K.C. Overexpression of osmotin gene confers tolerance to salt and drought stresses in transgenic tomato (Solanum lycopersicum L.). Protoplasma 2010, 245, 133–141. [Google Scholar] [CrossRef]
  94. Viktorova, J.; Klcova, B.; Rehorova, K.; Vlcko, T.; Stankova, L.; Jelenova, N.; Cejnar, P.; Kundu, J.K.; Ohnoutkova, L.; Macek, T. Recombinant expression of osmotin in barley improves stress resistance. PLoS ONE 2019, 14, e0212718. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Minocha, R.; Majumdar, R.; Minocha, S.C. Polyamines and abiotic stress in plants: A complex relationship. Front. Plant Sci. 2014, 5, 175. [Google Scholar] [CrossRef] [PubMed]
  96. Alćazar, R.; Altabella, T.; Marco, F.; Bortolotti, C.; Reymond, M.; Koncz, C.; Carrasco, P.; Tiburcio, A.F. Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta 2010, 231, 1237–1249. [Google Scholar] [CrossRef]
  97. Kumar, R.R.; Sharma, S.K.; Rai Gyanendra, K.; Sing, K.; Choudhury, M.; Dhawan, G.; Singh, G.P.; Goswami, S.; Pathak, H.; Rai, R.D. Exogenous application of putrescine at pre anthesis enchances the thermotolerance of wheat (Triticum aestivum L.). Indian J. Biochem. Biophys. 2014, 51, 396–406. [Google Scholar]
  98. Arguelles, J.C. Physiological roles of trehalose in bacteria and yeasts: A comparative analysis. Arch. Microbiol. 2000, 174, 217–224. [Google Scholar]
  99. Cortina, C.; Culianez-Macia, F.A. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci. 2005, 169, 75–82. [Google Scholar] [CrossRef]
  100. Gururani, M.A.; Tapan Mohanta, K.; Bae, H. Current understanding of the interplay between phytohormones and photosynthesis under environmental stress. Int. J. Mol. Sci. 2015, 16, 19055–19085. [Google Scholar] [CrossRef] [Green Version]
  101. Grichko, V.P.; Glick, B.R. Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlledby the 35S, rolD or PRB-1b promoter. Plant Physiol. Biochem. 2001, 39, 19–25. [Google Scholar] [CrossRef]
  102. Bienert, G.P.; Bienert, M.D.; Jahn, T.P.; Boutry, M.; Chaumont, F. Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J. 2011, 66, 306–317. [Google Scholar] [CrossRef] [PubMed]
  103. Raturi, G.; Kumawat, S.; Mandlik, R.; Duhan, D.; Thakral, V.; Sudhakaran, S.; Ram, C.; Sonah, H.; Deshmukh, R. Deciphering the role of aquaporins under different abiotic stress conditions in watermelon (Citrullus lanatus). J. Plant Growth Regul. 2022; preprint. [Google Scholar] [CrossRef]
  104. Reuscher, S.; Akiyama1, M.; Mori1, C.; Aoki, K.; Shibata, D.; Shiratake, K. Genome-wide identification and expression analysis of aquaporins in tomato. PLoS ONE 2013, 8, e79052. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Sade, N.; Vinocur, B.J.; Diber, A.; Shatil, A.; Ronen, G.; Nissan, H.; Wallach, R.; Karchi, H.; Moshelion, M. Improving plant stress tolerance and yield production: Is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion. New Phytol. 2009, 181, 651–661. [Google Scholar] [CrossRef] [PubMed]
  106. Wang, L.; Li, Q.T.; Lei, Q.; Feng, C.; Zheng, X.; Zhou, F.; Li, L.; Liu, X.; Wang, Z.; Kong, J. Ectopically expressing MdPIP1;3, an aquaporin gene, increased fruit size and enhanced drought tolerance of transgenic tomatoes. BMC Plant Biol. 2017, 17, 246. [Google Scholar] [CrossRef] [Green Version]
  107. Li, R.; Wang, J.; Li, S.; Zhang, L.; Qi, C.; Weeda, S.; Zhao, B.; Ren, S.; Guo, Y.D. Plasma membrane intrinsic proteins SlPIP2; 1, SlPIP2; 7 and SlPIP2; 5 conferring enhanced drought stress tolerance in tomato. Sci. Rep. 2016, 6, 31814. [Google Scholar] [CrossRef]
  108. Ouziad, F.; Wilde, P.; Schmelzer, E.; Hildebrandt, U.; Bothe, H. Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ. Exp. Bot. 2006, 57, 177–186. [Google Scholar] [CrossRef] [Green Version]
  109. Al-Whaibi, H.M. Plant heat-shock proteins: A mini review. J. King Saud. Univ.-Sci. 2011, 23, 139–150. [Google Scholar] [CrossRef] [Green Version]
  110. Sabehat, A.; Weiss, D.; Lurie, S. The correlation between heatshock protein accumulation and persistence and chilling in tomato fruit. Plant Physiol. 1996, 110, 531–537. [Google Scholar] [CrossRef] [Green Version]
  111. Kadyrzhanova, D.K.; Vlachonasios, K.E.; Ververidis, P.; Dilley, D.R. Molecular cloning of a novel heat induced/chilling tolerance related cDNA1 in tomato fruit by use of mRNA differential display. Plant Mol. Biol. 1998, 36, 885–895. [Google Scholar] [CrossRef]
  112. Zhao, C.; Mariko, M.; Sun, A.; Yi, S.; Li, M.; Liu, J. Constitutive expression of an endoplasmic reticulum small heat shock protein alleviates endoplasmic reticulum stress in transgenic tomato. J. Plant Physiol. 2007, 164, 835–841. [Google Scholar] [CrossRef] [PubMed]
  113. Zhang, X.H.; Li, B.; Hu, Y.G.; Chen, L.; Min, D.H. The wheat E subunit of V-Type H+-ATPase is involved in the plant response to osmotic stress. Int. J. Mol. Sci. 2014, 15, 16196–16210. [Google Scholar] [CrossRef] [Green Version]
  114. Wang, G.; Cai, G.; Xu, N.; Zhang, L.; Sun, X.; Guan, J.; Meng, Q. Novel DnaJ Protein Facilitates Thermotolerance of Transgenic Tomatoes. Int. J. Mol. Sci. 2019, 20, 367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  115. Duan, M.; Feng, H.L.; Wang, L.Y.; Li, D.; Meng, Q.W. Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J. Plant Physiol. 2012, 169, 867–877. [Google Scholar] [CrossRef] [PubMed]
  116. Gamper, N.; Shapiro, M. Regulation of ion transport proteins by membrane phosphoinositides. Nat. Rev. Neurosci. 2007, 8, 921–934. [Google Scholar] [CrossRef] [PubMed]
  117. Gisbert, C.; Rus, A.M.; Boların, C.M.; Lopez-Coronado, J.M.; Arrillaga, I.; Montesinos, C.; Caro, M.; Serrano, R.; Moreno, V. The yeast HAL1 gene improves salt tolerance of transgenic tomato. Plant Physiol. 2000, 123, 393–402. [Google Scholar] [CrossRef]
  118. Leidi, E.O.; Barragan, V.; Rubio, L.; El-Hamdaoui, A.; Ruiz, T.M.; Cubero, B.; Fernandez, J.A.; Bressan, R.A.; Hasegawa, P.H.; Quintero, F.J.; et al. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J. 2010, 61, 495–506. [Google Scholar] [CrossRef] [Green Version]
  119. Lenaerts, B.; Collard, B.C.Y.; Demont, M. Review: Improving global food security through accelerated plant breeding. Plant Sci. 2019, 287, 110207. [Google Scholar] [CrossRef]
  120. Ahmar, S.; Gill, R.A.; Jung, K.H.; Faheem, A.; Qasim, M.U.; Mubeen, M.; Zhou, W. Conventional and Molecular Techniques from Simple Breeding to Speed Breeding in Crop Plants: Recent Advances and Future Outlook. Int. J. Mol. Sci. 2020, 21, 2590. [Google Scholar] [CrossRef] [Green Version]
  121. Kaur, N.; Sharma, S.; Hasanuzzaman, M.; Pati, P.K. Genome Editing: A Promising Approach for Achieving Abiotic Stress Tolerance in Plants. Int. J. Genom. 2022, 2022, 5547231. [Google Scholar] [CrossRef] [PubMed]
  122. Tran, M.T.; Doan, D.T.H.; Kim, J.; Song, Y.J.; Sung, Y.W.; Das, S.; Kim, E.J.; Son, G.H.; Kim, S.H.; Van Vu, T.; et al. CRISPR/Cas9-based precise excision of SlHyPRP1 domain (s) to obtain salt stress-tolerant tomato. Plant Cell Rep. 2021, 40, 999–1011. [Google Scholar] [CrossRef] [PubMed]
  123. Li, R.; Zhang, L.; Wang, L.; Chen, L.; Zhao, R.; Sheng, J.; Shen, L. Reduction of tomato-plant chilling tolerance by CRISPR–Cas9-mediated SlCBF1 mutagenesis. J. Agric. Food Chem. 2018, 66, 9042–9051. [Google Scholar] [CrossRef] [PubMed]
  124. Li, R.; Liu, C.; Zhao, R.; Wang, L.; Chen, L.; Yu, W.; Zhang, S.; Shen, J.; Shen, L. CRISPR/Cas9-mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol. 2019, 19, 38. [Google Scholar] [CrossRef]
Plants 12 00086 g001 550
Figure 1. A schematic illustration of the effects of abiotic stress at the cellular level. The tolerance of tomato in a challenging environment requires several modifications to its cellular activities, which are based on stress-induced gene expression, translational reprogramming, and metabolic adaptation, often based on homeostatic mechanisms.
Figure 1. A schematic illustration of the effects of abiotic stress at the cellular level. The tolerance of tomato in a challenging environment requires several modifications to its cellular activities, which are based on stress-induced gene expression, translational reprogramming, and metabolic adaptation, often based on homeostatic mechanisms.
Plants 12 00086 g001
Plants 12 00086 g002 550
Figure 2. Abiotic stress at the physiological level is mediated by the signal transduction pathway. The first stage of a signal transduction pathway is signal perception, which is followed by the formation of secondary messengers (e.g., calcium, phosphoinositides, and reactive oxygen species (ROS)). Second, messengers promote the downstream signaling cascades that lead to the plant response against abiotic stress.
Figure 2. Abiotic stress at the physiological level is mediated by the signal transduction pathway. The first stage of a signal transduction pathway is signal perception, which is followed by the formation of secondary messengers (e.g., calcium, phosphoinositides, and reactive oxygen species (ROS)). Second, messengers promote the downstream signaling cascades that lead to the plant response against abiotic stress.
Plants 12 00086 g002
Table
Table 1. Investigations focused on improving the efficiency of tomato genetic transformation.
Table 1. Investigations focused on improving the efficiency of tomato genetic transformation.
S. lycopersicum CultivarTransformation
Method		Type of ExplantTransformation Frequency (TF)References
Micro-TomIndirectEmbryonic part of the seedling11%[41]
NAIndirectFruits54 to 68.0%[44]
Micro-TomIndirectCotyledons (embryonic part)5.1%[45]
Hezuo 908IndirectHypocotyls and embryonic part40%[40]
Roma and Rio GrandeIndirectHypocotyls and leaf disks24% and 8%, respectively[4]
Momotaro, UC-97, and EdkawiIndirectHypocotyls54 to 67%[46]
Castle RockDirectHypocotyls and part of cotyledons26.5%[47]
Cambell-28IndirectCotyledons21.5%[48]
Pusa Ruby, Sioux, and Arka VikasIndirectCotyledons41.4%, 22%, and 41%, respectively[49]
Hezuo 908IndirectEmbryonic part and Hypocotyl40%[40]
ShalimarIndirectShoot and LeafNA[50]
MicroTomIndirectLeaf19.1%[51]
NAIndirectHypocotyls33 to 59%[41]
Pusa Ruby and DT-93IndirectCotyledonshigher than 37%[52]
SummerIndirectHypocotyls and cotyledons7%[53]
Footnote. NA: not available.
Table
Table 2. A selection of genes that have been utilized to improve tomato cultivars to withstand abiotic stress.
Table 2. A selection of genes that have been utilized to improve tomato cultivars to withstand abiotic stress.
Gene/OriginFunctionExpressionResultsReferences
Fe-SOD/A. thalianaLessens the oxidative stressUpregulationIncreased ability to withstand oxidative stress and improve stability of photosynthetic equipment[58]
SIERF3b & SIERF5Regulates transcription for stress conditionsOverexpressionEnhanced tolerance to abiotic stress and resistance to biotic stress[59]
FAD3/rape FAD7/potatoRegulates the fatty acid unsaturation of membrane lipidsUpregulationBoosted cold resistance; an increase in the 18:3/18:2 ratio in leaves and fruits[60]
SlSAM1/tomatoPromotes the conversion of ATP plus methionine to S-adenosylmethionine, which is necessary for the production of ethylene and PAsUpregulationImproved resistance to saline-alkali stress[61]
SIGGP (LIKE)/tomatoTranscription factorExpressionEnhanced tolerance to abiotic and biotic stress[62]
SIBZIP1/tomatoTF, Defense proteinDownregulationRegulated ABA-mediated pathway to enhance drought tolerance[63]
SLWRKYTF, transcriptional regulationOverexpressionRegulated biotic stress[64]
RcGPX5/SalvimiltiorrhizaGluthatione biosynthesisOverexpressionTolerance to H2O2, drought and oxidative stress[65]
CBF1/A. thalianaTF and regulates transcriptionTranscription/ regulationEnhanced cold tolerance[66]
MdVHA-B/appleMaintains the homeostasis of ionUpregulationImproved drought tolerance[67]
MdSOS2L1/appleSignal-inducing proteins; influence on ion-driving transport mechanismsExcessive expressionIncreased salt tolerance[68]
TERF1/sugarcaneTranscription factor for ethylene response; assimilates ethylene and osmotic stress pathwaysExcessive expressionIncreased tolerance to drought stress, osmotic stress caused by salt[69]
LeNHX2/tomatoTransport of ionsExpression in excessSalt tolerance increase[70]
CWIN (Lin7)/tomatoTakes part in mechanisms related to temperature stressExpresses at normal levelImproved heat resistance in tomato flowers[71]
mt1D/E. coliBiosynthesis of mannitolUpregulationIncreased tolerance to drought, cold, and salinity[72]
LeFAD7/tomatoRole in fatty acid transcriptionAntisense regulationImproved high-temperature tolerance; trienoic fatty acids reduced[73]
TPSP (TPS/TPP fusion gene)/E. coliBiosynthesis of TrehaloseUpregulationSalt and drought resistance improved[74]
SlICE1/tomatoTranscription regulationOverexpressionImproved tolerance to cold[75]
katE/tomatoOxidative stress (catalase)OverexpressionUpgraded resistance to photo-oxidative stress as a result of drought and Fungal stress[76]
tas14/tomatoAccumulates chaperone-like proteins more effectivelyupregulationEnhanced tolerance to drought and salinity without any growth aberrations[77]
Glycine betaineStress saviorSupplementsChilling tolerance increased[78]
ZAT12/B. carinataTranscriptional regulationUpregulationBoosted resistance toward drought[79]
CaKR1/pepperImpact on defense machineryExpression in excessImproved salt tolerance as well as oxidative stress[80]
ZAT12/B. carinataTranscription of C2H2 zinc finger proteinUpregulationEnhanced tolerance to heat[81]
PtADC/P. trifoliataInvolved in PAs synthesisUpregulationIncreased tolerance to water stress[82]
LeFAD3/tomatoTranscription of fatty acid and lipids unsaturationTranscribed in excessAugmented tolerance to salt stress[83]
TaNHX2/wheatTransport of ions; equal-ion managementUpregulationBoosted resistance to salt stress[84]
LeHSP21.5/tomatoHeat shock proteinOverexpressionCombat with tunicamycin-induced stress[85]
MdPIP1; 3/AppleAquaporin protein and used to increase fruit sizeExpressionIncreased drought tolerance[86]
OSMOTIN gene/N. TobacumHas a higher level of prolineConstitutively expressionTolerance to salt stress[87]
CodA/tomatoOrganic osmolyteExpressionEnhanced chilling stress[88]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Rai, G.K.; Kumar, P.; Choudhary, S.M.; Kosser, R.; Khanday, D.M.; Choudhary, S.; Kumar, B.; Magotra, I.; Kumar, R.R.; Ram, C.; et al. Biomimetic Strategies for Developing Abiotic Stress-Tolerant Tomato Cultivars: An Overview. Plants 2023, 12, 86. https://doi.org/10.3390/plants12010086

AMA Style

Rai GK, Kumar P, Choudhary SM, Kosser R, Khanday DM, Choudhary S, Kumar B, Magotra I, Kumar RR, Ram C, et al. Biomimetic Strategies for Developing Abiotic Stress-Tolerant Tomato Cultivars: An Overview. Plants. 2023; 12(1):86. https://doi.org/10.3390/plants12010086

Chicago/Turabian Style

Rai, Gyanendra Kumar, Pradeep Kumar, Sadiya Maryam Choudhary, Rafia Kosser, Danish Mushtaq Khanday, Shallu Choudhary, Bupesh Kumar, Isha Magotra, Ranjit Ranjan Kumar, Chet Ram, and et al. 2023. "Biomimetic Strategies for Developing Abiotic Stress-Tolerant Tomato Cultivars: An Overview" Plants 12, no. 1: 86. https://doi.org/10.3390/plants12010086

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