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Drought Stress Tolerance in Plants
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This entry is adapted from the peer-reviewed paper 10.3390/ijms22179108

Drought stress (DS) negatively affects plant morphological, physiological, and biochemical processes, which decrease photosynthesis, impair cell elongation and division, and reduce cell turgor pressure. Drought stress also inhibits nutrient uptake and affects gene expression, yield, and quality of crop plants. Metabolites play an essential role in plant growth and development.

crop improvement drought stress drought tolerance genetic engineering metabolomics primary metabolites secondary metabolites

1. Introduction

Drought stress (DS) negatively affects plant morphological, physiological, and biochemical processes, which decrease photosynthesis [1], impair cell elongation and division [2], and reduce cell turgor pressure [3]. Drought stress also inhibits nutrient uptake and affects gene expression, yield, and quality of crop plants [4][5]. Metabolites play an essential role in plant growth and development. Under stress conditions, metabolites are involved in cell signaling, energy storage, membrane formation and scaffolding, and whole-plant resource allocation [6]. Various abiotic stresses, including drought, disturb plant metabolism through metabolic enzyme inhibition, substrate shortage, excess demand for specific compounds, or a combination of these and many other factors. Thus, the metabolic network must be reconfigured to maintain essential metabolism, and acclimate by adopting a new steady-state in light of the prevailing stress conditions [7]. The induction of primary or secondary metabolites under drought stress can regulate the turgidity and stiffness of cells and tissues, redox homoeostasis, ion transport, and enzyme activity [8][9]. These metabolites play an important role in connecting plant genotypes and phenotypes [10][11].

Metabolomics is an effective tool for garnering comprehensive information on metabolite profiling and metabolic network analysis. It also imparts knowledge about identified and unidentified metabolites. Several reports have contributed to the recent understanding of metabolite regulation in many plant species in response to different environmental stresses, including drought, salt, heat, cold, and light stress [7][12][13]. Metabolite profiling approaches have been widely used to characterize the molecular responses to DS in plants and evaluate metabolite levels in a particular metabolite class or pathway [14][15]. It includes various analytical approaches for identifying different classes of metabolites through gas chromatography-mass spectrometry (GC-MS), liquid chromatography-mass spectrometry (LC-MS), nuclear magnetic resonance (NMR), high-performance liquid chromatography (HPLC), and capillary electrophoresis-mass spectrometry (CE-MS) in various plant species under DS [16][17][18] (Table 1).

Table 1. Key metabolites involved in various plant species under drought stress.

Table
Plant Species Methods of Analysis Tissue Key Metabolites Involved in Drought Tolerance References
Monocots        
Avena sativa GC Leaves Lipids: Monoacylglycerols (MAGs), diacylglycerols (DAGs), and triacylglycerols (TAGs) and free fatty acids (FFAs) [19]
FA: Palmitic acid, linolenic acid
Brachypodium distachyon GC/MS Leaves CH: Glucose, glycerol, mannobiose, maltose, sucrose, galactose [20]
AA: Norvaline
Hordeum vulgare HPLC-DAD-MSn Leaves SM: Flavone glycosides, chlorogenic acids, caffeoyl-hexose, sinapoyl-hexoses, feruloyl-hexose, hydroxycinnamic acids [21]
H. vulgare GC-MS Awns, kernels CH: Galactinol, mannitol [22]
OM: Isocitric acid, α-ketoglutaric acid
H. vulgare GC-MS Grain CH: Raffinose, mannitol, myoinositol, putrescine, [23]
AA: Pyroglutamic acid
H. vulgare GC-MS-EI Fifth leaf, palea AA: Proline, glutamine, threonine, glycine, aspartate, serine, aromatic amino acids [24]
Oryza sativa GC/EI-TOF-MS Leaves AA: Glutamate, arginine, proline [25]
PA: Spermidine, putrescine, spermine
OM: GABA
O. sativa GC/MS Leaf blades AA: Serine, asparagine, threonine [26]
Triticum aestivum GC-TOF-MS Shoots CH: Sucrose, mannose, fructose [13]
AA: Proline
OM: Malic acid
T. aestivum GC/MS Flag leaves AA: Glutamine, methionine, lysine, asparagines, serine [27]
T. aestivum GC-MS Roots, leaves AA: Valine, tryptophan [28]
OM: Malic acid, fumaric acid, citric acid,
Seven Triticeae species GC-MS Roots, leaves CH: Sucrose, trehalose, mannitol, maltose [29]
AA: Proline, glutamate, alanine, glycine, asparagines, methionine, threonine, phenylalanine, homocysteine, serine, valine, tyrosine
OM: Succinate, citrate, aspartate, gluconate, glutathione
Zea mays GC/MS Leaf blades AA: Glycine, myoinositol [30]
Z. mays 1H-NMR Leaves AA: Alanine [31]
Lipids: Triacylglyceride
OM: Malate, glutamate, formate
Dicots        
African eggplant GC-MS Leaves CH: Fructose, sucrose [32]
AA: Proline, glutamate
OM: Tricarboxylic cycle metabolite
Arachis hypogaea GC-MS Nodules CH: Trehalose [33]
AA: Proline
OM: GABA
A. hypogaea GC-MS Leaves, roots CH: Glucose D-ribose, D-mannitol, D-xylopyranose, xylonic acid, α-D-glucopyranose, 2-deoxyribose, L-manopyranose, myo-inositol, galactosoxime, D-fructose, D-turanose, malic acid, succinic acid, 2 butenedoic acids, 2-deoxyribose, myo-inositol [34]
FA: Stearic acid, pentadecanoic acid, 8,11-octadecadienoic acid, palmitic acid, pentadecanoic acid
Craterostigma
plantagineum		 HPLC Leaves PAs: Putrescine, spermine, spermidine [35]
Cicer arietinum UPLC-HRMS Leaves AA: l-proline, l-arginine, l-histidine, l-isoleucine, tryptophan [36]
OM: Allantoin
Glycine max 1H-NMR, 1H-1H TOCSY Leaves, nodules CH: Myoinositol, pinitol [37]
AA: Glutamine
OM: GABA, allantoin
G. max NMR Leaves, roots CH: Sucrose [38]
AA: Alanine
OM: Succinate, citrate, acetate
G. max GC-MS Leaves SM: 5-methoxytryptamine, 4-hydroxycinnamic acid, ferulic acid, salicylic acid [39]
OM: Fluorine
Lentils GC/EI-TOF-MS Cotyledons, radicles, shoots PAs: Putrescine, cadaverine [40]
CH: Erythronic acid
OM: Isocitric acid, nicotinic acid
Nicotiana tabacum GC/MS, LC/MS Leaves, roots CH: Mannitol, trehalose, myoinositol, galactinol [40]
OM: GABA
Nigella sativa GC Seeds(10 black cumin genotypes) FA: Stearic acid, palmitic acid, oleic acid, linoleic acid, linolenic acid, myristic acid, arachidic acid [41]
Portulaca oleracea GC Leaves FA: Palmitic acid, linolenic acid, linoleic acid, oleic acid, stearic acid, arachidic acid, behenic acid [42]
Vigna unguiculata GC-TOF Seeds CH: Galactinol [43]
AA: Proline
SM: Quercetin
V. unguiculata GC-TOF Leaves CH: Rhamnose, raffinose [44]
Vitis vinifera SPME-GC-MS Leaves SM: Quercetin-3-O-glucoside, kaempferol-3-O-glucoside [45]
OM: Citric acid, 2-methyl-butanal phenylacetaldehyde

AA, amino acid; CH: carbohydrate; EI, electrospray ionization; FA, fatty acid; GABA, γ-aminobutyric acid; GC-MS, gas chromatography-mass spectrometry; HPLC-DAD-MS, high-performance liquid chromatography coupled with diode-array detection and multiple-stage mass spectrometry; LC-MS, liquid chromatography-mass spectrometry; 1H-NMR, nuclear magnetic resonance; OM, other metabolites; PAs, Polyamines; SM, secondary metabolites; SPME-GC-MS, solid phase micro extraction-gas chromatography mass spectrometry; TOCSY, total correlation spectroscopy; TOF, time-of-flight; UPLC-HRMS, ultra-performance liquid chromatography-high-resolution mass spectrometry.

2. Metabolomics and Its Application in Drought Tolerance of Plants

Environmental stresses, such as drought, salinity, and high temperatures, can trigger hyper-accumulation of a vast array of metabolites in plants [46][47]. Plant secondary metabolites (SMs) are derivatives of primary metabolites (PMs) produced by plants to fight a variety of unfavorable physiological changes induced due to stressors [48][49]. Drought is one of the most significant environmental stresses on agricultural production worldwide [50]. In plants, DS adaptation is a complicated biological process that involves dynamic trends in metabolite composition and gene expression [51]. Plant tolerance to DS is typically determined by their ability to maintain an appropriate level of primary and secondary metabolic processes and defense responses [47]. Metabolomic analysis can investigate and recognize key differences between DS-tolerant and DS-sensitive plant species/genotypes and connect links between genotypic and phenotypic changes in plants during DS [52]. Two main methods (non-targeted and targeted) are used to understand metabolic reprogramming in plants under abiotic stress [53][54][55]. Non-targeted metabolomics provides an overview of the most abundant metabolites in plants under various environmental stresses. Targeted metabolomics detects, estimates, and analyzes known metabolites in plants under various environmental stresses [56][57]. Therefore, metabolomics studies can reveal the important role for metabolic reprogramming, including regulation and accumulation of PM and SM levels in plants under DS and biotechnological applications for DS management of agricultural crop plants [58][59].

Drought stress directly affects plant metabolism, resulting in profound changes in biosynthesis and transport of PMs and SMs [60][61]. Primary metabolites are important for the proper development of plant cells and directly implicated in plant growth processes, photosynthesis, and respiration [47][62]. They include sugars, polyols, amino acids (AAs), and lipids that allow plants to acclimatize and recover from DS [63] ( Figure 1 ; Table 1 ).

Ijms 22 09108 g001 550
Figure 1. A schematic representation of metabolic response to drought stress. Primary metabolites (PMs) and secondary metabolites (SMs) are reprogrammed in plant cells to maintain osmotic balance and activate various primary and secondary metabolic pathways (green and orange circles, respectively) to survive under DS. Metabolites with an important role in DS are highlighted in bold, and their responses are depicted with green arrow (increased level), red arrow (decreased level), and green and red arrows (increased/decreased levels). ACP, acyl carrier protein; 4 CL, 4-coumarate-CoA ligase; AcCoA, acetyl-CoA; CAD, cinnamyl alcohol dehydrogenase; CCoAR, cinnamoyl-CoA reductase; CHI, chalcone isomerase; CHS, chalcone synthase; DMAPP, dimethylallyl diphosphate; DTs, diterpene synthase; DXP, 1-deoxy-D-xylulose-5-phosphate; DXS, 1-deoxy-D-xylulose 5-phosphate synthase; FAT A/B, fatty acyl-ACP thioesterase A/B; F3H, flavanone 3-hydroxylase, F3’H, flavonoid 3‘-hydroxylase; F6P, fructose 6-phosphate; FDP, farnesyl diphosphate; FDPS, farnesyl diphosphate synthase; FLS, flavonol synthase; G3P, glyceraldehyde 3-phosphate; G6P, glucose 6-phosphate; GDP, geranyl diphosphate; GDPS, geranyl diphosphate synthase; GGDP, geranyl geranyl diphosphate; GGDPS, geranyl geranyl diphosphate synthase; HDR, 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase; HMBPP, 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate; IDI, isopentenyl diphosphate isomerase; IPP, isopentenyl diphosphate; MtID, mannitol-1-phosphate dehydrogenase; MEP, 2-C-methyl-D-erythritol-4-phosphate; MTs, monoterpene synthase; PAE, palmitoyl-ACP elongase; PA, pyruvic acid; PAL, phenylalanine ammonia-lyase; PEP, phosphoenolpyruvate; PER, peroxidase; SAD, stearoyl-ACP desaturase; SQTs, sesquiterpene synthase; TCA, tricarboxylic acid; TCMO, trans-cinnamate 4-monooxygenase. Figure adapted from images created with BioRender.comto draw the proposed model (https://app.biorender.com/biorender-templates (accessed on 18 June 2021)).

Lipids are cellular macromolecules with structural, energy storage, and signalling roles in plant biological systems [64]. Lipids act as signaling mediators [65][66] to mitigate the negative impacts of environmental stressors [67][68]. Plant lipids principally include glycerolipids (e.g., phospholipids, galactolipids, sphingolipids, triacylglycerols) and extracellular lipids (e.g., suberin, cutin, and waxes). Sanchez-Martin et al. [19] profiled different classes of lipids, including polar lipids (PLs), monoacylglycerols (MAGs), diacylglycerols (DAGs), and triacylglycerols (TAGs) and free fatty acids (FFAs) in drought-tolerant (cv. Patones) and drought-sensitive (cv. Flega) oat cultivars differing in their response to drought stress. Saturated FAs, particularly palmitic acid in the DAG and TAG fractions, increased in drought-sensitive cv. Flega. In contrast, drought-tolerant cv. Patones was characterized by the early induction of signaling-related fatty acids and lipids, such as linolenic acid and DAGs [19]. Moradi et al. [69] examined lipid profiling in drought-tolerant and drought-sensitive thyme plants under prolonged drought stress and found that lipid components decreased in sensitive plants but increased in tolerant plants. They proposed that combining lipid profiling with physiological parameters represented a promising tool for investigating the mechanisms of plant response to DS at the non-polar metabolome level [69]. The composition of lipid components changes under DS. The lipid contents in A . thaliana leaves decreased progressively in response to DS. However, the lipid content of highly dehydrated leaves quickly increased after rehydration [70].

Drought elevated the levels of major lipid components, indicating enhanced lipid biosynthesis and/or reduced lipid degradation [69]. Stress-induced changes in the lipid profile cause membrane lipid remodeling and activation of plant defense mechanisms against biotic and abiotic stresses, including drought [71][72].

3. Metabolomic and Molecular Responses to Drought

Metabolic regulation is the key mechanism implicated in the safeguarding of cell osmotic potential during abiotic stress. The metabolite profiling approach has been widely used to characterize molecular responses of plants under abiotic stress [73]. Apart from its importance for cell function, water is an important component of plants due to its undeviating involvement in metabolite transportation and essential nutrients to various plant parts. Inaccessibility of sufficient water or higher transpiration rates enhances DS and changes metabolite production [74]. Drought tolerance strategies of plants comprise numerous biological mechanisms at the cell, organ, and whole-plant levels when stimulated at different phases of plant growth. Drought stress affects plants at several levels, including the molecular level [75], increasing the accumulation of drought-related proteins and metabolites [76]. Several molecular pathway cascades, including perception of water deficiency, activation of signaling network, and transcriptional, metabolic, and regulatory element responses improve plant resistance to DS [77]. Molecular mechanisms of the drought response are strongly governed by regulatory elements, such as transcription factors (TFs) and protein kinases. Transcription factor families, such as MYB, NAC, bZIP, AP2/ERF, and AREB/ABF, regulate stomatal movement and the expression of drought-responsive genes upstream or downstream of a metabolic pathway [78][79].

The molecular response to drought stress is a multi-genic trait controlled by many genes. Several genes related to DS at the transcriptional level have been investigated in microarray and real-time polymerase chain reaction (RT-PCR) studies [73][75][76][77][78][79][80][81][82]. Functional validation revealed that these genes protect against dehydration stress through stress perception, signal transduction, and transcriptional regulatory networks responses to drought tolerance [83][84]. Therefore, understanding molecular responses to drought tolerance can provide insights for enhancing drought tolerance in sensitive plant species. Significant efforts have been made to explore the molecular mechanisms used by plants to cope with DS. Plants respond to DS by reprogramming their transcriptional, proteomic, and metabolic pathways to protect cells from stress-mediated damage [84][85][86]. Primary metabolites, such as glucose, sucrose, and trehalose, function as signal molecules to regulate gene expression involved in plant growth and the stress response [87]. Drought stress elevates ROS production in diverse cellular compartments, particularly chloroplasts and mitochondria, which is controlled by an adaptable and cooperative antioxidant system that balances intracellular ROS levels and sets the redox status of plant cells [88].

4. Genetic Engineering of Metabolic Genes to Improve Drought Tolerance in Plants

The genetic engineering approach is widely used to enhance plant tolerance to various environmental stresses, including drought, by engineering candidate genes for crop improvement [61][89][90][91]. Drought stress can seriously impact plant growth, photosynthesis, water relations, yield, pigment content, and membrane integrity [92]. Plants have evolved various interconnected signaling networks to regulate drought-responsive genes to produce various classes of proteins, including transcription factors, enzymes, molecular chaperones, and other functional proteins, for drought tolerance [93]. Developing drought-tolerant plants using the genetic engineering approach requires identifying key genetic determinants underlying DS tolerance in plants and introducing metabolic genes into crops for expression. Drought-responsive genes are involved in signaling cascades, transcriptional regulation (e.g., transcription factors and protein kinase/phosphatase), and functional proteins that protect cell membranes [94]. Other proteins, such as antioxidants, osmotin, late embryogenesis abundant proteins, and proteins associated with the uptake and transport of water and ions, such as aquaporins and sugar transporters, also respond to DS. Drought tolerance is a complex trait involving the activation of signaling mechanisms and differentially expressed molecular responses [95].

Numerous drought-responsive genes have been isolated from various sources, including plants; their characterization for enhancing drought tolerance by developing transgenic plants with increased level of metabolites shown in Table 2 . The schematic representation of the proposed model for the application of metabolic genes involved in drought tolerance in plants is shown in Figure 2 . It shows the specific responses of metabolic genes under DS in transgenic plants. It also depicts the accumulation of various key metabolites such as glycine betaine, proline, polyamines, trehalose, mannitol, lipids, flavonoids, and other important metabolites in transgenic plants under DS. The accumulation of these metabolites leads to various cellular responses, such as ROS detoxification, modulation of antioxidant activities, increased relative water contents (RWC), decreased electrolytic leakage (EL) and malondialdehyde (MDA) contents, and structural adaptation of membranes, resulting in morphological changes that improve growth and drought tolerance in plants ( Figure 2 ). Targeted metabolites can be enhanced by overexpression of single or multiple genes that produce either direct desired molecule/metabolites or enzymes implicated in the production of the targeted metabolites. The upregulation of these genes resulted in biosynthesis of the metabolite responsible for osmolyte synthesis [96]. The C1A cysteine protease (CysProt) family is one the most abundant proteins, also known as papain-like CysProt). The upregulation of C1A CysProt genes is important for protein breakdown during stress responses by reorganizing metabolism, remodeling cell protein compounds, degrading damaged or unnecessary proteins, and remobilizing nutrients [56][97][98]. Gomez-Sanchez et al. [99] reported that drought stimulated the entire C1A CysProt family and upregulates HvPap-1 and HvPap - 19 genes in H . vulgare leaves. Transgenic Arabidopsis overexpressing the T. aestivum cysteine protease ( TaCP ) gene showed enhanced drought tolerance and cysteine protease (CP) activity under water-stressed conditions compared to wild-type (WT) plants [100].

Table 2. Application of metabolic genes for generating transgenic crops with improved drought tolerance.

Table
Gene Locus ID Source Transgenic Plants Metabolite Accumulation Stress Tolerance References
Arginine decarboxylase (AtADC) BT000682 Arabidopsis thaliana A. thaliana Increased putrescine Drought [101]
Arginine decarboxylase (DsADC) AJ251819 Datura stramonium Oryza sativa Increased putrescine and spermidine Drought [102]
Arginine decarboxylase (PtADC) HQ008237 Poncirus trifoliata A. thaliana Enhanced putrescine High osmoticum, dehydration, long-term drought, cold [103]
Betaine aldehyde dehydrogenase (AnBADH) KJ841914 Ammopiptanthus nanus A. thaliana Increased glycine betaine Drought, salt [104]
Chalcone synthase (NtCHS) LOC107801774 Nicotiana tabacum N. tabacum Increased flavanoids (rutin, quercetin, naringenin) Drought [105]
Choline monooxygenase (BvCMO) AB221007 Beta vulgaris N. tabacum Increased glycine betaine Drought, salt [106]
Choline oxidase (AgcodA) AY589052 Arthrobacter globiformis Solanum tuberosum Increased glycine betaine Water stress [107]
Choline oxidase (codA) AY304485 A. globiformis S. tuberosum Increased glycine betaine Drought, salt, oxidative [108]
Cysteine protease (TaCP) AY841792 Triticum aestivum A. thaliana Increased Cysteine protease activity Drought [100]
Dehydrin (OesDHN) KR349290 Olea europaea A. thaliana Increased proline Drought [109]
Dehydrin (TdDhn-5) AY619566 T. durum A. thaliana Increased proline Drought, salt [110]
Dehydrin (ShDHN) AK319970 Solanum habrochaites Solanum lycopersicum Increased proline Drought, salt, osmotic stress [111]
Dehydrin (PmLEAs) XM_016796383 Prunus mume N. tabacum Increased proline Drought, cold [112]
Flavanone 3-hydroxylase(RsF3H) JQ043380 Reaumuria soongorica R. soongorica Increased flavonoids and anthocyanin Drought, UV-B radiation [113]
Mannitol dehydrogenase (CaMTD) LOC101510334 Cicer arietinum C. arietinum Increased flavonoids Drought [114]
Mannitol-1-phosphate dehydrogenase (EcmtlD) EFF7369098 Escherichia coli T. aestivum Increased mannitol Drought [115]
Ornithine δ-aminotransferase (Atδ-OAT) NM_123987 A. thaliana O. sativa Increased proline Drought [116]
Ornithine δ-aminotransferase (OsOAT) LOC Os03g44150 O. sativa O. sativa Increased proline Drought [117]
Spermidine synthase (CfSPDS) BD142348 Cucurbita ficifolia A. thaliana Increased spermidine synthase activity and spermidine content Drought, chilling, freezing, salinity, hyperosmosis [118]
Trehalose-6-phosphate synthase (EcTPS; otsA) and Trehalose-6-phosphate
phosphatase (EcTPP; otsB)		 NC_000913 E. coli O. sativa Increased trehalose Drought, salt, cold [119]
Trehalose-6-phosphate synthase1 (OsTPS1) HM050424 O. sativa O. sativa Increased trehalose and proline Drought, salt, and cold [120]
Trehalose-6-phosphatesynthase1 (ScTPS1) and trehalose-6-phosphate synthase2 (ScTPS2) NC_001134 Saccharomyces cerevisiae N. tabacum Enhanced trehalose Drought [121]
Wax synthase/acyl-CoA:diacylglycerol acyltransferase (AtWSD1) AT5G37300 A. thaliana A. thaliana and Camelina sativa Increased deposition of epicuticular wax crystals and leaf and stem wax loading Drought [122]
WRI4-like gene (CeWRI4) MW039149 Cyperus esculentus A. thaliana Increased cuticular wax biosynthesis and deposition Drought [123]
Δ1-pyrroline-5-carboxylate synthetase (VaP5CS) VIRPYRR Vigna aconitifolia N. tabacum Increased proline Drought [124]
Δ1-pyrroline-5-carboxylate synthetase genes (OsP5CS) D49714 O. sativa P. hybrida Increased proline Drought [125]
Ijms 22 09108 g002 550
Figure 2. Schematic model displaying drought-induced expression of metabolic genes in transgenic plants. The proposed model depicts drought stress (DS)-mediated (yellow circle) reduction in root and shoot biomass, decrease chlorophyll content, increased reactive oxygen species (ROS) and flower and pod abortion, reducing yield and production (shown in purple oval). Plant DS response and adaptation involve various pathways for signal perception, transduction, transcriptional regulation depicted in olive green ovals, and expression of various metabolic genes shown in aqua color rectangle. Drought-induced expression of metabolic genes, such as Δ1-pyrroline-5-carboxylate synthetase (P5CS), trehalose-6-phosphate synthase1 (TPS1), dehydrin (DHN), cysteine protease (CP), flavanone 3-hydroxylase (F3H), arginine decarboxylase gene (ADC), choline monooxygenase (CMO), betaine aldehyde dehydrogenase (BADH), and spermidine synthase (SPDS), mannitol dehydrogenase (MTD), wax synthase/acyl-CoA:diacylglycerol acyltransferase (WSD) resulted in the accumulation of primary and secondary metabolites. This leads to the accumulation of several osmoprotectants and defensive compounds and ROS detoxification inside cells. Modulation of antioxidants prevents cell damage and maintains homeostasis. SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GPX, guaiacol peroxidase; PAL, phenylalanine ammonia-lyase; GRX, glutaredoxins; MeJA, methyl jasmonate; GB, glycine betain; SA, salicylic acid depicted in orange color rectangles. Morphological changes occurs in plants are shown in light green color rectangles. Plant growth and tolerance are shown in light green color in rectangle. Figure adapted from images created with BioRender.com to draw the proposed model (https://app.biorender.com/biorender-templates (accessed on 18 June 2021)).

Flavonoids are important SMs that play significant roles in maintaining the cellular redox balance of plant cells. Chalcone synthase (CHS) is the key enzyme in the flavonoid biosynthesis pathway and is modulated under DS. Transgenic N. tabacum plants overexpressing the NtCHS gene showed enhanced drought tolerance and oxidative stress responses under DS, relative to control plants [105]. Transgenic Brassica napus overexpressing the BR biosynthesis gene AtDWARF4 from Arabidopsis had improved drought tolerance [126]. Overexpressing Gossypium hirsutum Gh4CL7 gene enhanced drought stress tolerance in Arabidopsis [127]. Drought tolerance is conferred in N. tabacum plants through the overexpression of sweet potato cinnamate 4-hydroxylase ( IbC4H ), promoting phenolic compound accumulation and increasing the expression of stress-responsive genes [128]. The role of metabolic gene expression for providing drought tolerance in plants is summarized in Table 2 . Overall, we conclude that induction of metabolite biosynthesis provides a defensive level of drought protection and enhances growth tolerance in drought-stressed plants.

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