Defensive Role of Plant Hormones in Advancing Abiotic Stress-Resistant Rice Plants

M. Iqbal R. Khan, Sarika Kumari, Faroza Nazir, Risheek Rahul Khanna, Ravi Gupta, Himanshu Chhillar

Defensive Role of Plant Hormones in Advancing Abiotic Stress-Resistant Rice Plants

M. Iqbal R. Khan1, Sarika Kumari1, Faroza Nazir1, Risheek Rahul Khanna1, Ravi Gupta2, Himanshu Chhillar1

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Consistent climatic perturbations have increased global environmental concerns, especially the impacts of abiotic stresses on crop productivity.Rice is a staple food crop for the majority of the world’s population. Abiotic stresses, including salt, drought, heat, cold and heavy metals, are potential inhibitors of rice growth and yield. Abiotic stresses elicit various acclimation responses that facilitate in stress mitigation.Plant hormones play an important role in mediating the growth and development of rice plants under optimal and stressful environments by activating a multitude of signalling cascades to elicit the rice plant’s adaptive responses. The current review describes the role of plant hormone-mediated abiotic stress tolerance in rice, potential crosstalk between plant hormones involved in rice abiotic stress tolerance and significant advancements in biotechnological initiatives including genetic engineering approach to provide a step forward in making rice resistance to abiotic stress.

abiotic stress; genetic engineering; plant hormone; rice; transcription factor; tolerance

Rapid increases in global population, climate change, and depletion of natural resources are major factors influencing agri-food system and food demand. The global agri-food system should be reformed to reach the sustainable development goals. Rice, a primary crop and staple food for half of the world’s population, is cultivated on nearly 162 million hectares of land with an annual production of about 756 million tonnes globally (FAO, 2022). Sustaining and improving the rice system is crucial to ensure the sustainable development goals, mainly in Asian and African countries, where rice is produced at larger scale. Abiotic stresses are major factors that hamper various morpho-physiological and molecular mechanisms of rice plants, resulting in significant decreases in rice growth and productivity (Mukamuhirwa et al, 2019; Neang et al, 2020). Among different abiotic stresses, drought and salt stresses have been considered as the most deleterious abiotic stresses, causing a significant loss in rice production by altering the ionic and osmotic equilibriums of the cell. The adverse effects of excess salts are the consequences of water deficit that results from decreased osmotic/water potential of soil solution due to high solute concentration in the soil, as well as ion-specific stress due to altered Na+/K+ratio and Na+/Cl−ratio that are inimical to the plants (Roychoudhury et al, 2007). Besides these stresses, heavy-metal (HM) toxicity, caused by the unwanted accumulations of arsenic (As), lead (Pb) and cadmium (Cd), is emerging as a major factor, affecting the yield and performance of the rice plants (Wu et al, 2016; Ahmed et al, 2021). Rice is also extremely sensitive to temperature extremes (Hussain et al, 2019). Among all the cereals, rice is the most sensitive crop to prolonged exposure to cold stress from the germination to the booting stages (Najeeb et al, 2020). On the contrary, high temperatures (HT) in rice have negative effects on spikelet fertility and grain quality at the reproductive stage (especially the flowering stage) (Jagadish et al, 2008). The challenge of sustaining rice productivity to ensure ‘food for all’ has been continuously increasing, and thus efficient and speedy strategies are required to address this global concern. Research in the past has indicated that plant hormone-mediated tolerance mechanisms have the potential to improve rice toleranceunder various abiotic stresses (Wani et al, 2016; Sharma et al, 2017; Wang J et al, 2019; Khan et al, 2021). Plant hormones are chemical messengers that are essential for the coordination of intracellular and extracellular activities to manifest efficient adaption of plants to the changing environments (Peleg and Blumwald, 2011; Wang B et al, 2019). The five classical plant hormone classes are auxin, cytokinin (CK), gibberellin (GA), abscisic acid (ABA) and ethylene (ET), and other recognized plant growth regulators (PGRs) or plant hormones such as jasmonic acid (JA), salicylic acid (SA) and brassinosteroids (BRs) have been discovered and well-studied.

Plant hormones regulate plant adaptive responses by altering stress-responsive genes which culminate in the stress tolerance (Eyidogan et al, 2012; Hoang et al, 2017; Khan et al, 2022). In this review, the essentiality of plant hormones during various abiotic stresses in relation to the regulation of physiological and molecular responses of rice was discussed. Apart from this, potential crosstalk between plant hormones to facilitate the amelioration of abiotic stress-induced alterations in rice was elucidated. Moreover, the implications ofbiotechnological initiatives including genetic engineering approach were highlighted.

Plant hormones-mediated abiotic stress tolerance in rice

Abiotic stresses affect 70% of rice crops (RoyChoudhury et al, 2007). Plant hormones can aid in the acclimation of rice plants to different abiotic stresses such as drought (Zhang et al, 2017; Li J Z et al, 2019; Khan et al, 2021), salt (Misratia et al, 2015), heavy metal (Farooq et al, 2015; Verma et al, 2020), cold (Mega et al, 2015), heat (Sharma et al, 2018) and flooding (Khan et al, 2020). The growing importance of plant hormones in ameliorating abiotic stress tolerance in rice plants is briefly discussed here (Table 1 and Fig. 1).

Auxin in developing abiotic stress tolerance in rice

Auxin is renowned for its capability to control numerous plant growth and development processes (Saini et al, 2013). Alteration in auxin biosynthesis genes and transporters during stress conditions induces rice stress resistance (Table 1 and Fig. 1). Jung et al (2015) revealed a mechanistic link between the rice Aux/IAA gene ()expression and drought stress, showing that expression ofis highly triggered by drought stress and its over-expression increases drought stress resistance. Zhang et al (2012) identified a putative auxin efflux carrier genein rice vascular tissue, which is involved in root and shoot development as well as water regulation in drought- stressed rice plants. Du et al (2013) reported drought- stress induced transcript levels of(auxin receptor) and PIN-formed genes (and) in rice plants, however, suppression of(and) and() homolog in rice genome was reported in drought-stressed rice plants. The exogenous application of indole-3-acetic acid (IAA) rescues the expression levels of auxin receptor genes (and), transcription factors (TFs)/ chromatin-binding protein genes (and), and auxin response factor target gene () in response to drought stress (Sharma et al, 2018). Further, RNA interference (RNAi) rice lines with reducedtranscript levels show root growth inhibition in the presence of auxin (1 µmol/L) as compared with wildtype, suggesting that IAA-inducedexpression could be a promising target for altering the genes associated with salt and drought stresses via employing genetic engineering approaches (Sharma R et al, 2013).

Auxin may play a positive role in salt resistance in rice plants. Saini et al (2021) examined the expression levels of various genes implicated in auxin homeostasis in rice roots under salt stress. The expression levels of,,,and, among other auxin transport genes, are increased in rice roots, indicating that rice possess a greater potential to retain auxin homeostasis under salt stress. Furthermore, Jadamba et al (2020) revealed that over- expression of α-expansin genegreatly improves salt stress tolerance in rice. Increased salt tolerance may be attributed to auxin-triggered cellular differentiation and redox balance, as well as an increased antioxidant defence system in response to salt stress. Furthermore, foliar application of IAA (50 µmol/L) at the flowering stage can enhance the number of spikelets per panicle, seed-setting efficiency, and grain production in rice under salt stress by regulating the antioxidant defence system (Saedipour, 2016).

As, Arsenic; AsA, Ascorbate; APX, Ascorbate peroxidase; Ca, Calcium; CAT, Catalase; Cd, Cadmium; DHAR, Dehydroascorbate reductase; GR, Glutathione reductase; GPX, Glutathione peroxidase; GSH, Glutathione; IAA, Indole-3-aceticacid; MDHAR, Monodehydroascorbate reductase; MDA, Malondialdehyde; Mg, Magnesium; P, Phosphorous; Pb, Plumbum; PEG, Polyethylene glycol;POX, Peroxidase; ROS; Reactive oxygen species; Se, Selenium; SMC, Soil moisture content; SOD, Superoxide dismutase; POD, Peroxidase; RWC, Relative water content.

Fig. 1. Plant hormone involvement in amelioration of abiotic stress in rice.

Green lines with inhibitory heads signify repression mediated by hormonal action. Red lines with inhibitory heads indicate inhibition/repression. Black lines with arrowheads indicate activation/course of signalling. Blue cross indicates failure of inhibition.

Aux/IAA, Auxin/indole-3-acetic acid; ARF, Auxin response factor; ABP1, Auxin-binding protein 1; AFB, Auxin signalling F-box protein; Aux-RE, Auxin response DNA element; ACS, 1-aminocyclopropane-1-carboxylic acid (AC) synthase; ACO, AC oxidase; AOS, Allene oxide synthase; AOC, Allene oxide cyclase; ADP, Adenosine diphosphate; AMP, Adenosine monophosphate; ATP, Adenosine triphosphate; AREB, bZIP transcription factors; As, Arsenic; ABRE, Abscisic acid (ABA) response element; ABI, ABA insensitive; BZR1, Brassinazole resistant 1; BRI1, Brassinosteroid insensitive 1; BAK1, BRI1-associated receptor kinase 1; BES1, BRI1-EMS-suppressor 1; CTR1, Constitutive triple response 1; CYP, Cytochrome P450 monooxygenase; CKX, Cytokinin oxidase/dehydrogenase; Cr, Chromium; CRE1, Cyclic AMP response element 1; Cd, Cadmium; DMAPP, Dimethylallyl pyrophosphate; ER, Endoplasmic reticulum; ETR, Ethylene receptor; EIN, Ethylene-insensitive; ERF, Ethylene response factor; HMBPP, Hydroxymethylbutenyl pyrophosphate; IPT, Isopentenyl transferase; JAZ, Jasmonate-ZIM domain proteins; JAV1, Jasmonate-associated VQ domain protein 1; NCED, 9--epoxycarotenoid dioxygenase; OPDA, 12-oxophytodienoic acid; OPR, OPDA reductase; Pb, Lead; PM, Plasma membrane; PYR/PYL/RCAR, ABA receptors; PP2C, 2C-type protein phosphatase; SnRK2, SNF1-related kinase 2; SCF-COI1, Ubiquitin-ligase complex; TIR1, Transport inhibitor response 1; YUCCA, A flavin monooxygenase gene; ZEP, Zeaxanthin epoxidase.

Auxins play vital roles in plant growth and development under HM stress, with a significant impact on root and shoot growths (Wani et al, 2016). Exogenous treatment of IAA regulates miRNA expression, which often results in improved plant growth under stressful conditions (Sytar et al, 2019). Intercellular auxin transport is mediated by ABC-type transporters including AUX/LAX influx facilitators, and PIN-formed efflux carriers which are used for polar auxin transport under HM stress and participate in IAA distribution, resulting in reduced root elongation (O’Brien and Benková, 2013; Li et al, 2015; Sytar et al, 2019). Further, exogenous treatment of the auxin precursortryptophan (L-TRP) to Cd stressed rice seedlings reversed the detrimental impacts of Cd exposure, with plants showing improved height, yield and the numbers of panicles and tillers as compared with the untreated plants (Farooq et al, 2015). Likewise, application of auxin to arsenic (As) and selenium (Se) stressed rice results in enhanced root and shoot growth and seedling weight along with improved contents of chlorophyll, protein, proline and cysteine as well as a reduction in

Table 2. Representative studies of rice genes targeted at plant hormone for abiotic stress mitigation.

ABA, Abcisic acid; APX, Ascorbate peroxidase; Aux/IAA, Auxin/indole-3-acetic acid; CAT, Catalase;Cr, Chromium; CK, Cytokinin; ET, Ethylene; ERF, Ethylene response factor; GR, Glutathione reductase; GPX, Glutathione peroxidase; GSH, Glutathione; K, Potassium; POX, Peroxidase; ROS, Reactive oxygen species; RNAi, RNA interference; RWC, Relative water content; SOD, Superoxide dismutase; TF, Transcription factor.

DNA damage compared with untreated plants, indicating a positive role of auxin in Cd stress tolerance (Pandey and Gupta, 2015). Moreover, thiourea-mediated reactiveoxygen species (ROS)-metabolite reprogramming restores root system architecture under As stress in rice,which coincides with increased accumulation of amino acids (/-feruloyl putrescine and γ-glutamyl leucine) along with restoration of redox-status and auxin transport towards the root-tip (Ghate et al, 2022).

Auxins are known to be crucial in influencing plant organogenesis and therefore aiding the plants in dealing with HT conditions. Seedlings respond to elevated temperatures by elongating their hypocotyl, which improves the cooling effect of air on the plant, and inhibition of auxin via blocked biosynthesis or mutation pertaining to auxin transport/response, has been shown to limit hypocotyl elongation, imposing greater heat sensitivity (Ahammed et al, 2016). Auxin biosynthesis is predominantly mediated by the TAA1-YUC- dependent route and a growing body of evidence suggests its key role in hypocotyl elongation, as treatment of auxin transport inhibitor 1-naphthylphthalamic acid inhibits hypocotyl elongation, indicating that auxin is crucial for hypocotyl elongation (de Wit et al, 2014). However, under HT conditions, cotyledons serve as the main source of auxins. The observation that YUCgenes are greatly expressed in cotyledons as compared with hypocotyl supports the idea that cotyledon is an active source of auxin (de Wit et al, 2014).

Similar to other stress conditions, exogenous application of auxin to heat-stressed (HS) rice plants has also been proven fruitful in reversing oxidative damage and improving reproductive functioning. For instance, exogenous treatment of IAA to rice improves pollen viability, spikelet fertility and overall yield while lowering membrane damage, lipid peroxidation and ROS generation, under HS conditions (Sharma et al, 2018). IAA application under HS improves the expression of auxin receptors (and) and, another positive regulator of(Sharma et al, 2018). Genes related to the auxin biosynthesis are up-regulated under HS conditions with the highest expression being reported in stress-tolerant rice cultivars, indicating the involvement of enhanced auxin biosynthesis in HS tolerance. Du et al (2013) reported similar auxin-HS interactions where up-regulations of,,andwere observed together with an increase in IAA concentration under HS conditions. Anthranilate synthase (AS) is a key enzyme involved in the tryptophan and auxin biosynthesis pathway, and two genes,andthat encode for AS α-subunit, are also up-regulated by HS (Du et al, 2013). On the other hand,genes are involved in the regulation of plant growth and can inhibitand, however, induced expression ofhas been reported upon exogenous application of auxin (Xu et al, 2017). Additionally, under HS conditions, the expression ofgenes is dependent on a(), which is a basic helix-loop-helix TF involved in the regulation of auxin biosynthesis and accumulation and has been used in designing transgenic plants to facilitate improved abiotic stress tolerance (Franklin et al, 2011; Kudo et al, 2017).

CKs in developing abiotic stress tolerance in rice

CKs are N6-substituted adenine derivatives that play significant roles in plant growth and development. In addition, a growing body of evidence also suggests that a crucial role of CKs in stress tolerance as an altered endogenous concentration of CKs has been reported upon the onset of different abiotic stresses in rice. In particular, HM stress reduces CK production and its transportation from roots to the other organs (Wani et al, 2016; Sytar et al, 2019). However, there are reports indicating the activation of CK signalling under HM toxicity to provide HM stress tolerance (O’Brien and Benková, 2013). The modification of CK biosynthesis either by the over-expression of cytokinin oxidase/ dehydrogenase (CKX) or loss of isopentyl transferase (IPT) genes, involved in CK biosynthesis and degradation,respectively, also confers abiotic stress tolerance (Nishiyama et al, 2011; Ramireddy et al, 2018). An increase in the stress-induced CK concentrations by over-expression of the IPT gene driven by a constitutive or stress-inducible promoter senescence associated receptor kinase (SARK) reduces the detrimental effect of abiotic stress (Guo et al, 2010; Peleg and Blumwald, 2011).

In rice, HS reduces endogenous CKs in young panicles of a heat-sensitive variety by altering CK transport, inhibiting CK biosynthesis, and enhancing CK catabolism by modulating the activities of IPT, cytochrome P450 mono-oxygenase (CYP735A), lonely guy (LOG) and CKX, all of which affect the number of spikelets per panicle. In contrast, the heat-tolerant variety maintains a sustained level of CK in the panicle, resulting in a much higher number of spikelets per panicle as compared with the heat-sensitive variety (Wu et al, 2019). Further, down-regulation of the CK degrading enzyme generesults in increased tiller and grain numbers, delayed senescence and enhanced grain weight while insertional activation ofreverses all of these attributes (Yeh et al, 2015). Furthermore, Chen L et al (2021) noted a heat-tolerant QTL/gene ()at the region of 3 555 000–4 520 000 bp on rice chromosome 8. In this target region, 10 putative genes influencing rice abiotic stress tolerance were also revealed. Based on the qRT-PCR and sequence analysis,andgenes control HS tolerance during the flowering stage in rice and are implicated in long-distance CK translocation from root to shoot, making them potential candidate for improving rice heat tolerance.

GAs in developing abiotic stress tolerance in rice

In the case of salt stress, GAscan modulate seedling growth and grain yield parameter in rice plants. In addition, priming of rice seeds with GA3results in the mitigation of salt stress by regulating theratio of Na+and K+, the contents of proline, H2O2, anthocyanin, chlorophyll and phenolics, as well as antioxidant activities (Chunthaburee et al, 2014). Wen et al (2020)reported that the treatment of GA3(100 µmol/L) increases germination vigor and plant growth in salt-stressed rice plants. Further, Misratia et al (2015) showed that application of GA3(150 mol/L) is effective in enhancing the number of panicles per plant, panicle length, the number of filled grains per panicle, grain yield per plant, grain weight and harvest index in salt-stressed rice plants. Further analyses revealed that biochemical parameters such as soluble sugars, proteins and prolinesare increased along with the accumulations of K+, Mg2+and Ca2+. Additionally, the application of GA3reduces the negative effects of salt stress through minimizing membrane permeability (Liu et al, 2018). Moreover, up-regulation of mono- galactosyldiacylglycerol synthase, digalactosyldiacylglycerol, and phospholipid lipids + sulfoquinovosyl diacylglycerol were also reported after the treatment of GA3, indicating the participation of GA3in the regulation of lipid biosynthesis under salt stress.

In response to cold stress, GAs function as a stress regulator, modulating physiological responses and inducing tolerance traits in rice. For example, treatment with GA3promotes rice seedling emergence and vigor under cold stress (Chen et al, 2005). Furthermore, the application of GA3to rice at the seedling stage improves cold stress tolerance and significantly increases yield traits (Shashibhushan et al, 2021). However, more studies are needed to explore the role of GAs under HM stress. Additionally, substantial studies are needed to comprehend how plants react and modify to GA-mediated HT stress alleviation at the cellular and molecular levels that can help to increase our ability to improve stress resistance in rice crops in the future.

ABA in developing abiotic stress tolerance in rice

ABA is an important plant hormone whose application to plant mimics the effect of abiotic stress condition (Roychoudhury et al, 2013). Drought stress tolerance is mediated by changes in root morphological traits including root development and plasticity, and a growing body of evidence suggests the involvement of ABA in changes in root architecture under stress conditions. For instance, Chen et al (2006) showed that the enhanced viability of ABA-treated roots was observed by the 2,3,5-triphenyl tetrazolium chloride reductase ability, suggesting a role of ABA in maintaining root development that can endure drought tolerance. Foliar application of ABA (100 µmol/L) to rice results in enhanced contents of chlorophyll, reducing sugar, starch, protein and proline contents under drought stress (Ramachandran et al, 2021). Moreover, Activities of antioxidant enzymes are also increased in the ABA- treated rice, suggesting a role of ABA in the maintenance of ROS homeostasis under drought stress.

ABA has also been suggested to play essential roles under HM toxicity, and elevated expression levels of ABA-biosynthetic genes have been observed in rice in response to HM exposure (Wani et al, 2016; Bücker- Neto et al, 2017; Sytar et al, 2019). For instance, enhanced expression levels of four ABA signalling and two ABA biosynthetic genes includingandwere observed in rice seedlings exposed to As stress (Huang et al, 2012). Increased expressionlevels of five ABA signalling and one ABA biosynthesis genes were also observed in rice in response to vanadium toxicity (Lin et al, 2013). Moreover, a higher increase in endogenous ABA was reported in the roots and leaves of Cd-tolerant cultivar as compared with the Cd-sensitive cultivar (Hsu and Kao, 2003). Additionally,exogenous application of fluridone (an ABA biosynthesis inhibitor) to the Cd-tolerant cultivar TNG67 results in reduced ABA content and Cd-tolerance which is reversed when ABA was exogenously administered, further confirming a positive correlation between ABA and HM stress tolerance (Hsu and Kao, 2003). Multiple loss-of-function mutants of ABA receptors, such as,, and,which are insensitive to ABA even at high ABA concentrations, show deficient HM stress amelioration mediated by ABA exogenous application (O’Brienand Benková, 2013). HM stress is always accompanied by oxidative stress and an ABA signalling geneis found to be involved in the alleviation of HM stress-induced oxidative stress in rice. ABA treatment enhances the expression of,resulting in the induction of the antioxidant defence system in rice leaves. In contrast,mutants show higher H2O2accumulation, culminating in increased oxidative stress (Shi et al, 2012).

In addition to these stresses, the involvement of ABA in heat tolerance has also been reported. For instance, ABA-insensitivemutants are highly sensitive to HS, and exogenous application of ABA can reverse the detrimental impacts imposed by HS (Larkindale and Knight, 2002; Ahammed et al, 2016).mutants deficient in ABA biosynthesis (,and) and ABA signalling (and) exhibit deficiency in heat tolerance (Larkindale et al, 2005). ABA biosynthetic genes (,and) are also involved in enhancing ABA levels under HT conditions (Ahammed et al, 2016).,,,andgenes are involved in alleviating different abiotic stress conditions, however, their involvement in HS mitigation still needs to be investigated (Huang et al, 2012; Xu X Z et al, 2018). Heat shock proteins (HSPs) play a crucial role in revitalising the metabolism of HS rice plants, and ABA induces the expression of, a member of the HSP70 family. ABA-inducedexpression is the highest in leaves and sheaths, suggesting its role in facilitating normal leaf functioning, photosynthesis and respiration (Zou et al, 2009). Apart from HSPs, other ABA signalling components have been implicated in HS tolerance in rice. For instance, Chang et al (2017) studied HS transgenic rice designed to co-overexpress a protein kinase involved in ABA signalling () and a bZIP-TF (), and found improved ability of these transgenic lines to combat HT conditions (Table 1). The over-expression of the ABA 8′-hydroxylase1 () gene, which regulates the endogenous level of ABA, results in decreased ABA content, while increasing seed vigor index in cold stressed rice plants (Mega et al, 2015). This study also suggests that ABA homeostasis is an important trait for alleviating cold stress-induced responses in rice plants. Lee et al (1997) reported that exogenously-sourced ABA significantly improves the survival ratio of chilled rice seedlings. Overall, ABA proves to be an efficient plant hormone in facilitating HS amelioration by multifaceted stress-responsive mechanisms.

ET in developing abiotic stress tolerance in rice

The role of ET under abiotic stress conditions has been extensively studied, and evidence gathered thus far suggests that ET plays an efficient role in inducing acclimatizing responses in abiotic-stressed rice plants (Steffens, 2014; Abiri et al, 2017). ET-responsive element-binding proteins and associated TFs have primarily been focused to alleviate the negative effects of drought stress on rice (Khan et al, 2021). Du et al (2014) studied the role of the() gene in modulation of drought tolerance traits in rice plants. The allelic mutants ofshow increased resistance to drought stress by maintaining ET production and energy metabolism in rice plants. The loss of,() in rice results in the accumulation of proline and improves ROS scavenging activity (Zhang et al, 2020). In addition, the interaction and phosphorylation ofby() gene show their potential in the field of genetic engineering. In another experiment, over-expression of() results in a significant enhancement in drought stress tolerance (Zhang et al, 2010)(Table 1). These transgenic rice plants show activated expression levels of stress- responsive genes, as well as increased synthesis of proline by regulating the expression of gene(s) involved in proline biosynthesis such as(), indicatingas a potential candidate that can be targeted to induce tolerance in drought susceptible rice plants.

ET is also suggested to confer HM stress tolerance in plants as increased ET concentration has been reported in plants under HM exposure (Thao et al, 2015; Sytar et al, 2019). In the ET biosynthetic pathway, aminocyclopropane- 1-carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO) are considered as key genes involved in the biosynthesis of ET, and enhanced expression levels of these genes have been reported under HM toxicity (Wani et al, 2016; Bücker-Neto et al, 2017). The phosphorylation-dependent stabilization of ACS2 and ACS6 enzymes by the activity of mitogen-activated protein kinase (MAPK) including MAPK3 and MAPK6 are crucial in enhancing ET biosynthesis under HM stress (Thao et al, 2015). The TF WRKY33 is phosphorylated by MPK6 and regulates the expression levels ofand(Bücker-Neto et al, 2017). Abiri et al (2017) showed up to 5-fold up-regulations of 22 WRKYgenes under Cr6+stress, suggesting a crucial role of these TFs and ET signalling under Cr toxicity. ET is perceived by endoplasmic reticulum localized ET receptors, including ETR1, ETR2 and CTR1, which act as the signal transducer to EIN2 ion transporters, EIN3 TFs, and members of the apetala2/ethylene response factor (AP2/ERF) multi- gene family (Steffens, 2014).isa crucial transducer of the ET response in HM stress, regulating the functions of ABC-transporters involved in the efflux of HM from the cytosol (Bücker-Neto et al, 2017). Cr6+toxicity induces the transcript levels of 21 AP2/ERFresponse factors in rice, suggesting a crucial role for ET signalling under HM toxicity (Trinh et al, 2014). Similarly, Cd induces the expression of ERF proteins in rice (Abiri et al, 2017).

Treatment of ACC (an ET precursor) under HS results in higher expression levels of HSFs, including,,,,,and ET signalling genes such as,,andin rice plants (Wu and Yang, 2019). The activation of HSFs and ET signalling genes confers heat tolerance in rice by reducing cell membrane oxidation, and ion leakage, along with enhanced antioxidant activities (CAT and POX), chlorophyll content and fresh weight. Gautam et al(2022)showed the involvement of ET in the up-regulations of photosynthesis-related genes such asandof PSII in HS rice plants, which further modulates carbohydrate metabolism, antioxidant defence system, and rice growth under HS. Moreover, Tian et al (2011) revealed the role of ET response factor (TERF2) in cold-stressed rice. Physiological analysis indicated that TERF2 reduces the production of reactive oxygen species (ROS) and malondialdehyde (MDA) content as well as electrolyte leakage (EL) in rice under cold stress, thereby maintaining osmotic adjustment and photosynthetic rate. Further gene expression studies revealed that TERF2 can elicit the activation of cold-related genes like,,,,,andin transgenic rice plants under natural or cold stress circumstances, implying that TERF2 may have important regulatory functions and may be useful in improving crop cold adaptability. However, more research is needed to support the differential role of ET biosynthesis and signalling under HS which can aid in enhancing the resistance traits in rice plants.

JA in developing abiotic stress tolerance in rice

JA and methyl jasmonate (MeJA) are simple lipid- derived oxylipins, which are implicated in various physiological and molecular processes associated with plant growth and development, as well as a key frontier in conferring abiotic stress tolerance in plants (Raza et al, 2021). Biosynthetic genes and signalling pathways of JA have been extensively studied for inducing drought-tolerant traits in rice plants (Umesh and Pal, 2018). In rice, up-regulations of genes involved in JA biosynthesis, such as,and, and JA receptor gene,(), were observed under drought stress conditions. Moreover, a reverse trend was noticed for JA-signalling repressor gene,(), which results in higher accumulation of JA in drought-stressed rice plants to positively enhance relative water content (RWC), membrane stability index, and superoxide dismutase (SOD) activity, with lowered lipid peroxidation and H2O2contents (Umesh and Pal, 2018). Similarly, the increased JA concentration along with the enhanced expression of genes involved in JA biosynthesis and signalling such as,,,,,,,,,andwere reported in rice plants under drought stress (Du et al, 2013).

JA acts as a stress regulator in response to salt stress and aids in modulating physiological responses for inducing tolerance traits in rice. For instance, Kang et al (2005) reported JA increases the leaf water potential, photosynthetic rate, and maximum quantum yield efficiency of PSII, as well as K, Ca and Mg contents, while decreasing Na accumulation in salt-stressed rice plants. Furthermore, pre-soaking treatment of MeJA (20 µmol/L) to rice seeds results in increased germination rate, shoot and root dry mass and activity of alpha-amylase under salt stress (Mahmud et al, 2016). However, there is little evidence that elucidates the potential functions of JA-induced responses under salt stress. Therefore, further investigations are needed to enhance a better understanding of JA-mediated salt stress alleviation.

JA is also increased in plants exposed to HM stress, suggesting a crucial role of these compounds in HM stress tolerance (Rucińska-Sobkowiak, 2016; Wani et al, 2016; Per et al, 2018). Exogenous application of MeJA to Cd-stressed rice shows improved activities of SOD, peroxidase (POD), catalase (CAT) and glutathione reductase (GR), resulting in reduced Cd2+uptake, enhanced membrane integrity, and triggered lipoxygenase (LOX) activity mediating JA biosynthesis (Singh and Shah, 2014; Sytar et al, 2019). Similarly, MeJA application to As-stressed rice improves growth, photosynthetic pigment content, and both enzymatic and non-enzymatic antioxidants, while decreasing together electron leakage, lipid peroxidation and As content (Mousavi et al, 2020; Verma et al, 2020). Apart from LOX, allene oxide synthase and 12-oxo- phytodienoic acid reductase catalyze crucial steps in the JA biosynthetic pathway (Per et al, 2018). Exposures to Cu, Cd and mercury (Hg) of rice seedlings enhance the expressions of blast- and wound-inducible first functional MAPK gene () and multiple stress-responsive MAPK gene (), which are also induced by JA, suggesting activation of JA signalling under HM toxicity (Agrawal et al, 2002, 2003). Application of MeJA to As-stressed rice modulates the expression of genes involved in the JA signalling pathway (,and), As uptake and translocation (,,,,and), and As detoxification (,and), and enhances the expressions levels ofand(Mousavi et al, 2020; Verma et al, 2020).

HSdecreases JA content along with the reduced expression ofin rice (Li J J et al, 2019). Du et al (2013) showed the lowering of JA content in rice after exposure to HS, however, this decrease in JA content was not immediate but gradual. Moreover, genes related to JA biosynthesis (,,,,,and) and JA signalling (,,and)are also down-regulated or suppressed upon HS exposure (Du et al, 2013). Further, rice transgenic lines over-expressing thegene, which encodes a chloroplast protein, reduce JA under HS condition by down-regulatinggene (Li J J et al, 2019). In contrast to the studies where a decline in JA has been reported under HS, Umesh and Pal (2018) reported no change in endogenous JA level following HS. However, the application of JA increases endogenous JA content in rice lodicules, which results in a higher opened-spikelet rate under HS conditions (Umesh and Pal, 2018). These results were potentially in two ways, (i) by activating antioxidant systems and HSPs, culminating in improved oxidative stress suppression and lowered programmed cell death (PCD), and (ii) by enhancing the production of osmolytes which stimulate cell expansion and spikelet-opening in rice (Yang et al, 2021). Studies focusing on the impacts of JA and MeJA in HS rice are scarce, which leaves a gap in our understanding of JA responses to HS and may be prioritized considering the tremendous potential of JA in HS mitigation. Further, studies focusing on JA significance in response to cold stress are even more limited and only a handful of reports have been published so far on analyzing the effects of JA on cold stress in rice. Interestingly, results reported so far indicate a positive regulation of cold stress tolerance by JA in rice plants. Du et al (2013) showed that the concentration of endogenous JA along with IAA increases in rice under cold stress. Furthermore, several JA biosynthesis-related genes, such as,,andand JA signalling genes, such asand, are up-regulated in response to cold exposure.

SA in developing abiotic stress tolerance in rice

SA has been well recognized as a signalling molecule that plays a pivotal role in inducing the plant defence system under abiotic stress (Khan et al, 2015a). Treatment of SA via seed priming, hydroponic, and foliar applications is beneficial in modulating acclimation traits including reversal of oxidative stress-mediated cellular damage (Horváth et al, 2007). Recent studies signify the role of SA modulated defence mechanism in mitigating the stress-induced adversities in plants.

SA-mediated drought-tolerant mechanisms have been gaining importance due to their significant role in modulating major metabolic responses in plants (Khan et al, 2015b). Priming of rice seeds with SA (1.0 and 2.5 mmol/L) enhances seedling growth performances such as emergence rate, biomass accumulation, vigor index, plumule, and root length under drought stress (Ali et al, 2021). Moreover, enhanced chlorophyll, carbohydrate, total soluble sugar and protein contents along with decreased MDA levels due to the improved activities of CAT, APX and SOD are also observed in SA primed rice seedlings under drought stress Ali et al 2021). Recently, the pre-treatment of rice seedlings with SA (225 mg/L) results in a notable increase in germination indices, and thus alleviates the inhibitory effects of drought stress (Rafiq et al, 2021). Sohag et al (2020) reported similar results, where exogenous treatments of SA (0.5 and 1.0 mmol/L) significantly promote the seedling germination, chlorophyll content, plant growth, and biomass accumulation in drought-stressed rice plants. In addition, endogenous levels of stress markers (H2O2and MDA) are drastically reduced, possibly due to enhanced activities of antioxidant enzymes such as CAT, GPX and APX in SA-supplemented rice plants. Foliar application of SA (100 mg/L) enhances the stomatal conductance and CO2net assimilation, leaf gaseous-exchange attributes and net photosynthetic rate in drought-stressed rice plants (Farooq et al, 2009a). Moreover, SA treatment is beneficial in maintaining plant-water relations and stimulating the antioxidant system (SOD, CAT and APX) under drought stress. Hosain et al (2020) examined the effect of varying SA concentrations, ranging from 250 to 1000 µmol/L per square, on rice plants under drought stress, of which the best results such as increased yield traits (panicle number per hill, filled grain number per hill, grain weight, straw yield, and harvest index) were observed at 750 µmol/L per square in drought-stressed rice plants. Apart from the foliar application, researchers also investigated the effect of seed priming with SA in drought-stressed rice plants. Seeds primed with 100 mg/L SA counteracted the negative effects of drought stress by increasing the seedling growth traits such as germination rate, vigor index, energy percentage, and biomass accumulation (Shatpathy et al, 2018).

Salt stress induced the up-regulation of SA, which aids in inducing defence responses in plants. The treatment of SA (1 mmol/L) improves germination rate, and agronomic traits including plant height, leaf area index, number of panicles per plant, number of filled grains per plant, and grain weight along with increased carbohydrate and protein contents in salt-stressed rice plants (Jini and Joseph, 2017). Further, elevated concentrations of Ca2+, phosphorous (P), and K+were observed, which may contribute to the alleviation of salt-induced effects on rice plants (Jini and Joseph, 2017). Similar results were also reported in two subsequent studies where SA-priming results in enhanced seedling growth, photosynthetic pigments, gaseous exchange, and chlorophyll fluorescence in salt-stressed rice plants (Sheteiwy et al, 2019). Further decreased accumulations of Na+, ROS and MDA support the SA-mediated tolerance mechanism in rice (Khan et al, 2019).

SA acts as a stress regulator in response to HM stress and aids in modulating physiological responses for inducing tolerance in rice (Jing et al, 2007; Guo et al, 2009). For instance, pretreatment with SA alleviates the Cd-induced inhibition of root growth in rice plants by enhancing the antioxidant defence activities, thus alleviating Cd-induced oxidative damage and enhancing Cd tolerance (Guo et al, 2007). Similarly, SA pre-treatment to Pb-stressed rice results in improved shoot and root lengths, chlorophyll content, and enhanced activities of SOD, CAT and APX, culminating in lowered H2O2content (Jing et al, 2007). Guo et al (2009) conducted a split-root hydroponic experiment wherein half of the rice roots were exposed to Cd, while the other half were pre-treated with SA along with Cd exposure. The study concluded that SA treatment reduces Cd uptake, which may be attributed to SA-mediated regulation of Cd uptake via accelerating cell death in Cd-stressed root portion, enhancement in enzymatic antioxidants (SOD, CAT and POD), GSH, as well as non-protein thiols, and ROS-induced lipid peroxidation.

SA also plays a multidimensional role in HS responses such as regulation of HSPs, antioxidants, and secondary metabolites (Wani et al, 2016). Feng et al (2018) showed that SA spray is efficient in improving seed setting and pollen viability under HS conditions. The involvement of SA in this phenomenon was further confirmed by the application of SA inhibitor (paclobutrazol), which results in lower pollen viability in response to HS. SA aberted HS-induced pollen abortion through inhibiting the tapetum programmed cell death (PCD). This could be related to the up-regulations of thegene, which regulates the differentiation of primary parietal cells into secondary parietal cells, and thegene, which controls the early stages of tapetum development. Moreover, SA is also involved in the prevention of PCD by reducing the ROS accumulation in anthers to improve pollen viability under HS conditions. Further, pre-treatment with SA reverses the harmful impacts of HS in rice plants by improving the spikelet number per panicle, grain yield, and seed-setting rate, promoting the biosynthesis of proline, soluble sugar, and plant hormones including ABA, GA3, BR, IAA, JA, CK and zeatin riboside, and improving the activities of antioxidant enzymes (Zhang et al, 2017). In addition, Akasha et al (2019) also showed that SA treatment is efficient in enhancing the plant biomass as well as improving nitrate reductase and nitrite reductase activities, accumulations of soluble sugars and proteins, along with inorganic solutes including N, P, K and Mg. Furthermore, exogenous SA application is suggested to regulate the transcript ofgene, which plays a crucial role in HS tolerance as evidenced by the increased heat sensitivity ofknock-down mutants (Ahammed et al, 2016).

SA-mediated alleviation of cold stress-induced damages in rice plants has not been explored much as compared with HS. However, few studies indicated the concentration-dependent role of SA in providing cold tolerance in rice. Xu et al (2010) showed that SA treatment enhances SOD activity, chlorophyll pigment and proline contents, resulting in decreased MDA content in cold stressed rice plants. Moreover, Hussain et al (2016) revealed that seed priming with SA (100 mg/L) efficiently ameliorates the adverse effects of chilling stress on rice, which is associated with increased starch metabolism, elevated respiration rate, reduced lipid peroxidation, and strong antioxidative defence system under chilling stress.

BRs in developing abiotic stress tolerance in rice

BRs are steroidal hormones that regulate a wide range of physiological and molecular responses under stress conditions (Nolan et al, 2020). Farooq et al (2009b) showed that seed priming and foliar application at 0.01 µmol/L of 28-homobrassinolide (HBL) and 24- epibrassinolide (EBL) result in substantial improvements of seedling biomass, plant height, intracellular CO2concentration, net photosynthetic rate, leaf water status, and water use efficiency. In addition, accumulations of phenolics, anthocyanin and proline together with increased SOD, APX and CAT activities were also observed, resulting in minimal accumulation of MDA and H2O2under drought stress conditions. Besides, knock-out mutant of a negative regulator of BR signalling gene,(), an orthologue of() and, enhances drought stress tolerance as compared with non-transgenic lines, indicating its role in stress signal-transduction pathways (Koh et al, 2007).

Under HS, EBL (0.001 µmol/L) treatment has been proven efficient in enhancing pollen germination, pollen viability, and seed setting while reducing pollen bursting of rice plants (Thussagunpanit et al, 2013). Thussagunpanit et al (2013) also revealed that this EBL-mediated HS tolerance in rice is due to the improved plant biomass, photosynthetic area, photosynthetic pigments, stomatal conductivity, net CO2assimilation efficiency, RWC, chlorophyll fluorescence, photochemical quenching, soluble sugar content as well as reduced MDA and H2O2contents. In addition, BR also aids in maintaining redox homeostasis by improving non-enzymatic and enzymatic antioxidant defence systems as well as enhancing the ribulose 1,5-bisphosphate carboxylase/oxygenase activity, photosynthetic pigment content, and PSI efficiency in response to HS (Yang et al, 2021). At the cellular level, BRs are perceived by BR signalling receptors, which reverberates in the activation of(Yang et al, 2021), and are involved in the regulation of HSPs (and) including HSP90, which is mediated byandto prevent the deregulation of stress-induced proteins. Further, TFs such as MYB/MYC are involved in HS tolerance in rice, while NAC TFs are implicated in the up-regulation of enzymatic ROS scavengers, which also facilitate HS tolerance in rice (Sharma et al, 2017). Chen J et al(2021) recently reported that BRs can modulate the impact of HT during anthesis on pistil fertilization ability and ameliorate the detrimental impacts of HS on the pistil fertility in rice.

BRs are also in response to HM and cold stresses. Fujii and Saka (2001) reported that rice seedlings treated with brassinolide (20nmol/L) counteract the negative impacts of cold stress by promoting cell elongation, germination, vigor index, and biomass accumulation. Seed priming with EBL (0.01 µmol/L) ameliorates Cr-induced adversities in rice by triggering physio-biochemical attributes such as increased chlorophyll content, mineral uptake, antioxidant enzyme activities, as well as reducing ROS production under Cr stress (Basit et al, 2021). Basit et al (2022) also reported the effect of EBL (0.01 µmol/L) on aluminium (Al)-stressed rice plants, and found that EBL application reduced the adverse impacts of oxidative stress indicators.

Crosstalk between plant hormones induces abiotic stress tolerance in rice

The advancements in deciphering the plant hormone signalling pathways in rice have not only revealed insights into the biosynthetic and signalling components of major plant hormones but also have supported the notion that plant hormones do not act solitarily. The majority of the plant hormone responses to stress cues are accompanied by antagonistic and/or synergistic interactions (Fig. 2). For instance, the overlapping transcriptional responses of different PGRs were observed in microarray analysis (Garg et al, 2012). Interestingly, auxin-responsive genes are also responsive to stress hormones ABA, SA and JA,suggesting a significant overlap in the signalling cascades of these plant hormones under stress conditions. Genes, regulated by IAA/SA and IAA/ABA, show a similar response, implying a synergistic and/or antagonistic interaction among these plant hormones to regulate plant growth and development. CKs are known to act antagonistically to ABA (Pospíšilová, 2003) and therefore mediate the cooling of leaves under HT conditions by triggering the opening of stomata, which results in enhanced transpiration rates (Ahammed et al, 2016). Moreover, intricate crosstalk has been suggested among ET and other plant hormones for regulating flooding stress responses in rice. Adventitious root formation in rice under normal conditions was speculated to be coordinated by the synergistic interaction between auxin and ET (Zhang et al, 2012). However, under flooding stress, auxin-induced adventitious root formation was found to be suppressed by an ET action inhibitor 2,5-norbornadiene, suggesting that auxin-induced adventitious root formation is dependent on ET during submergence (Lorbiecke and Sauter, 1999). On the other hand, the submergence- induced ET accumulation in rice promotes inter-nodal elongation by inhibiting ABA biosynthesis, and activating its catabolism (Azuma et al, 1995; Zhou et al, 2020). Conversely, a synergistic interaction between ET and GA has been observed during flooding stress, where ET under submergence can significantly induce GA biosynthetic genethrough an ET-responsive TF,(Kuroha et al, 2018). ET treatment- induced GA biosynthesis reduces ABA and promotes rice stem elongation in deep water rice by increasing the GA/ABA ratio (Hoffmann-Benning and Kende, 1992). However, an opposite response has been observed in submergence tolerant rice genotype harbouring thegene. In this case, ET inhibits GA-induced plant growth by negatively regulating GA signalling as an energy-keeping strategy for survival during flooding (Fukao and Bailey-Serres, 2008). Moreover, JA is also suggested to act antagonistically to ET in terms of inter-node and elongation in deep-water rice (Minami et al, 2018).

Fig. 2. Plant hormones modulate signaling mechanism in plant system.

Red lines with inhibitory heads indicate inhibition/repression; Black lines with arrowheads indicate activation/course of signalling.

ABA, Abscisic acid; ET, Ethylene; ACC, Aminocyclopropane-1-carboxylic acid; JA, Jasmonic acid;GA, Gibberellic; SA,Salicylic acid.

A coordinated interaction has also been speculated between JA and SA defence signalling in rice where it was observed that 313 genes were up-regulated by SA analog benzothiadiazole, and surprisingly, more than half of these genes were also up-regulated by JA (Tamaoki et al, 2013). Additionally, a study conducted in relation to, which is identified as a root-specific pathogenesis-related protein revealed an antagonist effect of SA on JA/ET signalling whereby JA and ACC induce the expression ofwhile SA is involved in its suppression.is also induced in response to various abiotic stress conditions, and its overexpression results in improved tolerance to drought stress in rice, and both salt and drought stresses in(Hashimoto et al, 2004; Takeuchi et al, 2016). Furthermore, the cumulative foliar applications of IAA, CK and ABA increase the grain yield and yield components of rice under cold stress (Mohabbati et al, 2012).

During drought stress, a probable correlation between JA and ABA has been observed (Kim et al, 2009). JA is induced in drought-stressed rice plants which stimulate the production of ABA, alter spikelet development and lead to grain yield loss. Another study described an antagonist interaction between ABA and JA in the regulation of salt stress-inducible transcripts in rice where salt stress and ABA-induced expression ofis negatively affected by JA(Moons et al, 1997). Further, ABA negatively affects the JA and salt stress-induced transcript accumulation of. Several studies have shown an interaction between plant hormones in rice under HM stress. Genome-wide transcriptome analysis revealed that the transcriptional activationof JA-responsive genes (,and) along with genes of auxin (and), GA (), ET (), ABA (and) and CK () were up-regulated in response to As3+stress in rice seedlings. Thus, the involvement of plant hormones and their relative transcriptional activation proclaimed theirpotential candidature for As3+detoxification in rice plants (Yu et al, 2012). According to Zhao et al (2014), ABA modulates root system growth in rice under Cd stress by regulating the activation of specific genes involved in auxin signalling and allocation, such asand. Furthermore, the cumulative treatment of JA and auxin modulates root system development in rice under Cd and/or As stress (Ronzan et al, 2019).

The application of JA or MeJA (50 µmol/L) enhances the spikelet-opening of rice, as evidenced by a higher spikelet-opening rate under HT stress (Yang et al, 2021). Furthermore, supplementation of zeatin riboside, IAA, GA3, EBL, or ABA at a low concentration (10 µmol/L) has no influence on spikelet-opening rate. The implementation of ABA at a high level (50 µmol/L) or ACC effectively diminishes the spikelet-opening rate. These findings suggest that, among plant hormones, JAs may play a distinct role in ameliorating spikelet-opening damage caused by HT stress during the flowering stage in rice (Yang et al, 2021). Chen J et al (2021) reported a potential antagonistic relationship between BRs and ET. They suggested three major observations: (1) under HT stress during anthesis, a photo-thermo-sensitive genic male sterile (PTSGMS) rice line withhigher BR (24-EBL and 28-HBL) content has lower ACC content in the pistils; (2) levels of 24-EBL and 28-HBL are positively and directly linked with ascorbatecontent and CAT activity in PTSGMS lines, whereas ACC content is negatively correlated; and (3) implementation of 24-EBL or 28-HBL to the panicles of PTSGMS lines significantly reduces ACC levels in the pistils, but treatment with brassinazole (a BR biosynthesis inhibitor) significantly increases it. However, concrete evidence of BRs and ET crosstalk in rice under HT is still lacking.

Cold stress significantly monitors the transcription of genes encoding protein metabolism, adjustment, folding and defence responses in rice seedlings, according to transcriptome analyses (Du et al, 2013). Furthermore, ABA-, auxin- and JA-related genes are highly expressed in rice shoots and roots and are linked to cold stress homeostasis. The massive rises in ABA and JA levels increase plant survival by eliciting rapid responses such as stomatal closure, which prevents water loss. These two hormones may interact with each other to change the expression of a particular set of TFs in shoots (mainly NACs). In roots, auxin may interact with these two hormones to modulate the activation of other TFs, such as WRKY, to foster cold stress resistance in rice. In summary, it can be inferred that plant hormones either act independently or in conjugation with other hormones that may play an essential role in rice plants to cope with abiotic stresses.

Genetic engineering of plant hormones for rice improvement

Genome editing-based directed alteration of desired traits has become an indispensable strategy for improving plant’s performance under abiotic stress conditions. The CRISPR/Cas9 system is one of the emerging tools for the efficient generation of desired mutants (Thurtle-Schmidt and Lo, 2018)(Fig. 3). Abiotic stress tolerance in plants can be improved by targeting two categories of genes including structural and regulatory genes (Zafar et al, 2020). While structural genes encode proteins directly related to enhancement of abiotic stress tolerance, the regulatory genes facilitate alteration in the expression of other genes. Interestingly, several studies centred on the utilization of CRISPR/Cas9 systems in achieving improved abiotic stress amelioration in rice have also been reported. Using CRISPR/Cas9 gene editing system, Zeng et al (2020) targeted,andgenes, responsible for panicle length, grain size, and cold tolerance, respectively, to obtain individual mutants, double mutants in various combinations, as well as triple mutants withmutant rice lines exhibiting improved cold tolerance ability. Moreover, the triple mutants exhibit a high yield as well as improved cold tolerance. CRISPR/Cas9-inducedmutants exhibit a greater number of tillers and more panicle length, compared with wild type, suggesting a correlation between an auxin carrier involved in auxin transport and homeostasis, and grain yield traits under stress conditions (Zeng et al, 2020). Strategies focused on the editing of genes involved in plant hormone biosynthesis or signalling are also efficient in imparting abiotic stress tolerance in rice. For instance, Dong et al (2020) showed that knockout mutants ofgene, which is involved in BR signalling, show increased salt sensitivity while also exhibit reduced plant height. However, over-expression ofresults in considerably improved salt tolerance as well as grain size. Recently, there have been few studies focussing on BR-responsive NAC TFs in inducing abiotic stress tolerance in rice. Mutations ofandgenes confer sensitivity under salt, drought and HS conditions (Sharma et al, 2017; Wang B et al, 2019, 2020). Considering the involvement of NAC in ROS detoxification, use of gene editing to down-regulate the expression of NAC repressors or up-regulate the expression of NAC TFs may aid in imparting abiotic stress tolerance by reducing the damage caused by oxidative stress.

Recently, the functional role of CRISPR/Cas9 generatedmutants was established in improving drought tolerance and yield in rice (Usman et al, 2020). The mutant lines possess enhanced ABA accumulation, antioxidant activity, chlorophyll content, and improved survival rate, whereas stomatal conductance, MDA content and transpiration rates are reduced in response to drought stress. In addition, proteins related to drought response, circadian rhythm, and ROS are also significantly up-regulated in the mutant plants, suggesting a possible role of ABA receptor,,inregulating drought stress- responsive pathways in rice.() is considered as an important component of ABA signalling and regulates dehydration responses (Pei et al, 1998). Interestingly, ricemutant lines carrying CRISPR/Cas9-induced frame- shift mutations exhibit increased sensitivity to ABA along with the improved drought stress responses mediated by stomatal regulation, showing the negative interplay ofin coordinating drought responses in rice (Ogata et al, 2020). In addition,has been suggested as another potential target for inducing drought and salt stress tolerance in rice (Yue et al, 2020). Furthermore,belongs to a highly conserved miRNA in plants and is involved in regulating cold stress responses (Sun et al, 2020). However, anknockout line generated through CRISPR/Cas9 exhibit improved tolerance to salt, dehydration, polyethylene glycol (PEG), and ABA stress while its over-expression lines result in a reduced survival rate under PEG and dehydration stresses, making it an ideal gene-editing target for improving drought and salt stress tolerance in rice. Apart from CRISPR/Cas9 mediated gene editing, RNAi is also increasingly being used to target desired genes in order to decipher their functions in governing plant responses to abiotic stress conditions. For instance, RNAi-mediated suppression of() results in reduced water loss and stomatal conductance, high RWC, increased sensitivity to ABA, improved survival rate, and thereby enhanced tolerance to drought stress (Hu et al, 2017).

Fig. 3. Approaches for improving abiotic stress tolerance in rice by targeted regulation of plant hormone genes.

gRNA, guide RNA; RISC, RNA-induced silencing complex; RNAi, RNA interference; siRNA, Small interfering RNA.

The down-regulation of, a key gene involved in ABA catabolism, improves drought tolerance by enhancing enzymatic antioxidant defence and lowering membrane damage (Cai et al, 2015). Similarly, drought-responsive ERF () RNAi knock-down lines exhibit enhanced drought tolerance as well as increased ABA sensitivity (Guo et al, 2017). RNAi-mediated suppression of an auxin-induciblegene (a CC-type glutaredoxin gene) results in increased sensitivity to several abiotic stresses including salt, osmoticand oxidative stresses (Sharma R et al, 2013).gene may act as a crosstalk point between auxin signalling and abiotic stress tolerance and could be a promising target for imparting tolerance in rice plants. CRISPR/ Cas9 and RNAi are highly efficient technologies that should be applied to abiotic stress conditions to gain a better understanding of the impact of editing and/or silencing of targeted genes pertaining to plant hormone pathways and their reverberation into improved abiotic stress mitigation.

Conclusion and future prospects

Plant hormones play an important role in conferring abiotic stress tolerance and maintaining rice growth and yield. In this review, we provided considerable evidence for the functional attributes of plant hormones in coordinating defence responses and resistance in rice to major abiotic stress along with crosstalks existing between the plant hormones for sustaining growth and development of rice under such conditions. In the coming decades, this collection of knowledge will be useful for modifying hormone biosynthesis pathways in order to create abiotic stress resistant rice plants. Furthermore, a comprehensive approach should be used to uncover additional mechanisms of abiotic stress-induced up-regulation of plant hormone biosynthesis genes, as well as the precise description of hormonal crosstalk in influencing abiotic stress from spatiotemporal responses, genetic plasticity, in order to gain a better comprehension of plant responses to abiotic stress. Further research into genome editing based directed alteration of desired traits under abiotic stress is needed. In particular, analysis of genes encoding for transcription factors might add to our current understanding of this complex relationship.

ACKNOWLEDGEMENTS

M. Iqbal R. Khanis gratefully acknowledging the Science and Engineering Research Board-Department of Science and Technology(Grant No. SRG/2020/001004) and University Grants Commission Start-up Grant (Grant No. F. 30-482/2019) in South Korea. Faroza Nazir acknowledges Department of Biotechnology- Research Associateship (Grant No. DBT-RA/2022/January/N/ 1186) in India.

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http://dx.doi.org/10.1016/j.rsci.2022.08.002

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