Abstract
Under natural conditions, plants are often exposed to both biotic (pathogens, wounding, insects) and abiotic stresses (drought, salinity, heat, high or low temperature, UV light, heavy metals, ozone) simultaneously. Among the various abiotic stresses, drought along with salinity and alkalinity confers osmotic stress and causes major yield losses, with water scarcity (drought) contributing to maximum losses. On perceiving stress, plants respond by activating signal transduction cascades that interact with other pathways (phytohormones) for an optimal response for survival. Hormones also control the response to environmental factors, but do so by influencing each other at a biosynthesis or signaling level rather than by discrete pathways. This coordination leads to a network of signal transduction that integrates various inputs leading to a comprehensive output resulting in a physiological adaptation to stress. The points of hormones interacting with one another are where crosstalk occurs, which helps in switching the response from one pathway to another. Published literature provide comprehensive information on the response of plants to drought and the role of hormones in regulating the response to drought from experiments directly imposing drought stress (dehydration stress-withholding water) or osmotic stress (turgor loss due to extracellular solutes) and experiments with mutants and others involving the functions of hormones and other signals. Changes in gene expression induced by drought overlap with gene expression regulated by hormones. This chapter presents the signal transduction pathways of hormones under drought stress and how they cross talk with each other in regulating the drought stress response in plants.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
1 Introduction
A number of environmental stresses (abiotic—drought, salinity, high and low temperature—and biotic) affect plant growth and productivity. Under stress, both hormonal and redox processes are imbalanced. Plants alter their gene and protein expression in response to signal cascades that are transduced when plants perceive stress (Munns and Tester 2008; Mittler et al. 2011; Munné-Bosch et al. 2013), which leads to a change in metabolic and physiological responses that help plants survive under stressful situations. Phytohormones, that under optimal growth conditions play a critical role in plant growth and development, also play a central role in integrating signal transduction occurring under stressful conditions. Phytohormones help in linking and reprogramming the stress-adaptive signaling cascades (Ma et al. 2006; Golldack et al. 2014).
The growth regulators abscisic acid (ABA) and ethylene (ET) play a vital role in signaling drought stress and conferring drought tolerance. Jasmonic acid (JA) and salicylic acid (SA), known for their role in biotic stress signaling and tolerance, also play a role in abiotic stress signaling and tolerance. In addition, the growth regulators cytokinins (CKs), auxin (AUX), gibberellic acid (GA), brassinosteroids (BRs), and strigolactones (SLs) play a role in abiotic stress tolerance (Zhao and Schaller 2004; Cheng et al. 2013; Wu et al. 2007; Cela et al. 2011; Jayakannan et al. 2015; Magome et al. 2008; Wu et al. 2014a, b; He et al. 2005; Divi et al. 2010). Most of the time, these phytohormones are involved in crosstalk with other phytohormones and other signaling cascades.
Among the abiotic stress, drought stress negatively affects crop growth and productivity (Anjum et al. 2017). Plants exposed to drought stress adapt a drought-escape, avoidance or tolerance mechanism to overcome the stress (Hussain et al. 2018). Under drought escape, plants maintain a short life cycle or adapt developmental plasticity. Under drought avoidance, plants increase their water uptake and decrease water loss such that they avoid physiological drought. However, under drought tolerance, cells tolerate drought by regulating mechanisms such as osmo-protection, antioxidative capacity, and tolerance. Plants maintain a balance among the different mechanisms.
Drought tolerance is a complex trait that operates at morphological, physiological and molecular levels (Tanveer et al. 2018). Traits such as earliness; stomata shape, size and structure; leaf number, orientation, and rolling; the presence of a cuticle; wax on leaf and stem; growth habit; and rooting pattern contribute to morphological characters associated with drought resistance and tolerance. Traits such as photosynthetic rate, transpiration rate, osmotic adjustment, and stomatal closure contribute to physiological characters. Regulation of these traits at the molecular level by regulating gene expression and protein synthesis contribute to molecular characteristics.
Functional genomic approaches (gene expression analysis) have aided in understanding the molecular mechanism of stress tolerance. A number of genes are regulated under stress conditions and can be grouped broadly in two categories based on function. One group involves the regulation of genes encoding proteins involved in cellular homeostasis and stress protection such as osmoprotectants, water channels, antioxidative enzymes, metabolic enzymes, and lipid-transfer proteins. The other group involves genes that code for kinases, transcription factors (TFs) and proteins or products that mediate stress signal transduction and result in the expression of stress-responsive genes. Among them are also genes that are associated with signaling pathway(s) of various phytohormones. Auxins, GA, CKs, ABA, ET, SA, JA, BR, and SLs are the major hormones produced by plants. Although all play a role in the stress response, the hormones ABA, SA, JA, and ET play a major role in the plant response to biotic and abiotic stresses (Bari and Jones 2009; Nakashima and Yamaguchi-Shinozaki 2013). On sensing stress (abiotic or biotic stress), several signaling pathways are initiated in plant cells. Some lead to the induction and alteration of intercellular levels of Ca2+, reactive oxygen species (ROS), and inositol phosphate and activation of the kinase cascade.
2 Abscisic Acid (ABA)
Abscisic acid plays major role in the plant response to osmotic stress induced by cold, high salinity and drought. It is an endogenous messenger of the plant’s water status. Plant hormone, ABA is typically synthesized in response to stress due to enhanced expression of its biosynthetic genes (Swamy and Smith 1999; Zhu 2002). Treating plants with ABA mimics exposure to stress. Abscisic acid plays a critical role in response to various stress signals. It triggers reprogramming of the transcriptome and stomatal closure to control transpirational water loss (Christmann et al. 2007; Cutler et al. 2010; Raghavendra et al. 2010).
Signaling under stress involves various proteins leading to regulation of stress-responsive gene expression. Under stress, signaling pathways occurring under stress (osmotic or drought stress) can be broadly classified as ABA-dependent- or independent. TFs that bind to ABA-responsive element (ABRE) cis-elements play a major role in ABA-dependent gene expression and those that bind to the dehydration-responsive element/C-repeat (DRE/CRT) cis element are involved in ABA-independent gene expression in response to drought stress (Fujita et al. 2011; Qin et al. 2011).
Abscisic acid signaling has been extensively studied, and various components have been identified. The proteins PYRABACTIN RESISTANCE/PYR1-LIKE/REGULATORY COMPONENTS OF ABA RECEPTORS (PYR/PYL/RCARs) function as soluble ABA receptors, as demonstrated by chemical genetic and biochemical approaches. Besides their identification in Arabidopsis, they have been identified in rice (Oryza sativa), maize (Zea mays), sorghum (Sorghum bicolor), soybean (Glycine max), grapevine (Vitis vinifera), citrus (Citrus sinensis), and tomato (Solanum lycopersicum) (Klingler et al. 2010; Sun et al. 2011; Boneh et al. 2012; Kim et al. 2011; Romero et al. 2012). GPCR-type G protein 1 (GTG1)/GTG2 are membrane proteins with homology to G-protein coupled receptors (GPCRs). ChlH (or GENOMES UNCOUPLED 5 [GUN5]) and GTG1/GTG2 may be ABA receptors. However, neither ChlH/GUN5 nor GTG1/GTG2 can bind the biologically active ABA isomer (Shen et al. 2006; Pandey et al. 2009).
Forward genetic screening using mutants resistant to the ABA agonist pyrabactin and a search for biochemical interacting partners of ABA insensitive 1 (ABI1) and ABI2 led to the identification of PYR1 and RCAR1 among the 14 genes that code for PYR/PYL/RCARs (Ma et al. 2009; Nishimura et al. 2009). On activation, the receptor interacts with partners such as type 2C protein phosphatase (PP2C) and sucrose nonfermenting 1-related protein kinase 2 (SnRK2) complex (Umezawa et al. 2009, 2010). In the absence of ABA, PP2C binds to SnRK2 and mediates its dephosphorylation. Binding of ABA to its receptor (PYR/PYL/RCARs) fits well into the active site of PP2C enzyme, thereby inhibiting the phosphatase activity of PP2C. This situation results in phosphorylated SnRK2s, which can activate relevant TFs, and in turn leads to activation of an ABA-induced transcriptional cascade (Kline et al. 2010). Therefore, an increase in endogenous ABA due to environmental and/or developmental cues leads to sequestration of PP2C and ABA-induced release or activation of SnRK2.6. Autophosphorylation of SnRK2s then phosphorylates downstream proteins such as ABA-responsive element binding proteins/ABA-responsive element binding factor/basic-leucine zipper (AREB/ABF/bZIP) proteins and anion channels (Cutler et al. 2010; Klingler et al. 2010; Umezawa et al. 2010; Seiler et al. 2014). SnRK2s can be further regulated by a positive regulator, ARK (B3-MAPKKKs), and a negative regulator, casein kinase 2 (CK2) (Saruhashi et al. 2015; Meggio and Pinna 2003; Vilela et al. 2015).
The Arabidopsis genome encodes 112 phosphatases, of which 76 code for PP2Cs and at least 6 are involved in ABA signaling with well-characterized ABI1/2 and homolog of ABI1 (HAB1). The mutants abi1 and abi2 display ABA hypersensitivity, insensitive phenotypes and reduced seedling growth, seed dormancy, drought tolerance, and stomatal regulation. Other members of PP2Cs include ABA-hypersensitive germination 1 (AHG1), AHG3/AtPP2CA from Arabidopsis, and OsPP108 from rice (Leung et al. 1994, 1997; Meyer et al. 1994; Saez et al. 2004; Singh et al. 2015).
The protein kinase SnRK2 family is a group of plant-specific serine/threonine kinases that participate in cellular responses to drought and dehydration (Hrabak et al. 2003; Saruhashi et al. 2015). Depending on the affinity toward ABA, the SnRK2 family is divided into three subgroups. Subgroup I does not respond to ABA, subgroup II includes weak respondents, and subgroup III includes active respondents of ABA that are key players of ABA-dependent gene expression (Hrabak et al. 2003; Boudsocq et al. 2007). Arabidopsis has 10 SnRK2 members (SnRK2.1-2.10); ABA activates five SnRK2s (SnRK-2.2, -2.3, -2.6, -2.7, -2.8). Mutation in three SnRKs (snrk2.2/2.3/2.6) blocks all main ABA responses (Fujii and Zhu 2009; Fujita et al. 2009; Waadt et al. 2015). In addition, all SnRK2s are involved in ABA and stress signaling except SnRK2.9, which is activated by osmotic stress (Boudsocq et al. 2007; Furihata et al. 2006; Yoshida et al. 2006). ABA-activated protein kinase (AAPK), the ortholog of Arabidopsis open stomata 1 (OST1)/SnRK2.6, was the first protein kinase identified (from Vicia faba).
SnRK2 kinases phosphorylate the TFs ABFs/AREBs and ABI5, both in vitro and in vivo, involved in ABA responsive gene expression (Kobayashi et al. 2005; Furihata et al. 2006; Sirichandra et al. 2010; Nakashima et al. 2009). In addition, SnRK2 (OST1/SNRK2.6) phosphorylates plasma membrane proteins anion channel slow anion channel-associated 1 (SLAC1), potassium channel protein KAT1 and NADPH oxidase AtrbohF involved in regulating stomatal aperture (Geiger et al. 2009; Sato et al. 2009; Sirichandra et al. 2009). Phosphoproteomic and mutation study approach has identified ascorbate peroxidase, Ca2+/H+ antiporter regulator protein, G-protein beta subunit-like protein, glyoxysomal malate dehydrogenase, manganese superoxide dismutase, triose phosphate isomerase and others as potential SnRK2 targets (He and Li 2008; Umezawa et al. 2013).
TFs that play a significant role in ABA-regulated gene expression include ABFs/AREBs, ABI5, myeloblastosis (MYB), myelocytomatosis (MYC), NAM: no apical meristem (NAC), Arabidopsis transcription activation factor (ATAF), cup-shaped cotyledon (CUC), and ethylene response factor (ERF). ABFs/AREBs are regulated by SnRK2-mediated phosphorylation (Fujita et al. 2011; Nakashima et al. 2012; Rushton et al. 2012). ABFs/AREBs and ABI5 encode proteins belonging to the bZIP family regulate ABA and stress responses by binding to ABRE in promoters of target genes (Choi et al. 2000; Uno et al. 2000; Lopez-Molina et al. 2001). AREB1/ABF2, AREB2/ABF4, ABF3 and ABRE binding protein 9 (ABP9) are involved in signaling drought stress (Riechmann et al. 2000; Yoshida et al. 2010). MYC and MYB, belonging to the basic helix loop helix (bHLH) subfamily, also regulate ABA signaling by regulating stress-inducible genes. AtMYB60, AtMYB44, AtMYB15, and AtMYC2 mediate drought stress signaling (Abe et al. 1997, 2003, Jaradat et al. 2013). In addition, NAC (AtNAC) and ERF (AtERF7)-type TFs are involved in regulating ABA signal transduction under drought stress (Song et al. 2005; Zhang and Gan 2012).
3 Ethylene (ET)
This simple two-carbon molecule plays a major role in regulating biotic and abiotic stress signaling (Morgan and Drew 1997; van Loon et al. 2006). Biosynthesis of ET is simple, consisting of three steps. Methionine is used as precursor and is converted to S-adenosyl methionine (SAM), which is converted to ET by the action of ACC synthase (ACS) and ACC oxidase (ACO). ACS is regulated by drought stress, thereby regulating ET levels under drought stress.
Endoplasmic reticulum membrane-localized proteins perceive ET, are negative regulators of ET signaling, and play a role as ET receptors. Arabidopsis has five ET receptors: ET response 1 (ETR1) and ET response sensor 1 (ERS1), belonging to subfamily I, and ETR2, ERS2, and ET insensitive 4 (EIN4), belonging to subfamily II (Chen et al. 2005; Lacey and Binder 2014). Similarly, rice has five receptors: OsERS1 and OsERS2, belonging to subfamily I, and OsETR2, OsETR3, and OsETR4, belonging to subfamily II (Watanabe et al. 2004; Yau et al. 2004). Constitutive triple response 1 (CTR1), also a membrane protein and central transducer, is a negative regulator of ET signaling and acts downstream of the receptor, which is a Raf-like Ser/Thr protein kinase. Downstream of this is ETI2, also localized to the endoplasmic reticulum membrane that activates EIN3 and EIN3-like 1 (EIL1), which function as TFs inducing the expression of ERF1 and inducing or repressing that of many ET response genes (Kendrick and Chang 2008; Stepanova and Alonso 2009).
Therefore, in the absence of ET, CTR1 kinase activity is induced, which phosphorylates EIN2 and prevents its localization to the nucleus (Kieber et al. 1993; Bisson and Groth 2010; Ju et al. 2012). In addition, two F-box proteins—ETI2-targeting protein 1 (ETP1) and ETP2—reduce levels of EIN2 protein (Qiao et al. 2009). EIN2 is localized to the nucleus on its dephosphorylation and cleavage of its C-terminus, in the presence of ET, and it regulates activation of EIN3/EIL1 leading to the ET response (Ju et al. 2012). Similar to EIN2, two F-box proteins—ETI3 binding F-box protein 1 (EBF1) and EBF2—that are downregulated by ET, reduce EIN3/EIL1 protein levels in the absence of ET. Among the ET signal transduction pathway, ERFs are key players of abiotic-stress tolerance induced by drought stress. ERFs are also induced by various other abiotic stresses. ERFs belong to the APETALA2/ERF TF family. The expression of ERFs increases under drought stress, and many ERFs bind to DREs and regulate tolerance to abiotic stress.
ERF induces the expression of P5CS, germin-like protein 9, osmotin 34, similar to RCD one 5 (SRO5), responsive to dessication 29B (RD29B), early response to dehydration (ERD7) and RD20, leading to drought tolerance (Cheng et al. 2013). In addition, OsDERF1 directly binds promoters of the ERF repressors OsERF3 and OsAP2-39 that suppress ET synthesis and regulate drought tolerance (Wan et al. 2011; Zhang et al. 2013). Although most ERFs are transcriptional activators, two (ERF8 and ERF9) are transcriptional repressors. ERF8 is an inhibitor of cell division and leaf growth and thereby regulates the drought stress response (Thao et al. 2015; Dubois et al. 2013, 2018).
4 Jasmonic Acid (JA)
The JAs collectively include JA and its conjugates methyl jasmonate (MeJA) and jasmonyl-isoleucine (JA-Ile) (Ghasemi et al. 2014). They are lipid-derived oxylipins, synthesized from linolenic acid via the octadecanoid pathway as a result of oxidation by lipoxygenases (Feussner and Wasternack 2002).
Jasmonic acids are well known for their role in developmental processes, secondary metabolite synthesis and the plant defense response against pathogens and wounding (McConn et al. 1997; Reymond and Farmer 1998; Wasternack and Hause 2002; Lorenzo and Solano 2005; Schommer et al. 2008). Despite reports of the role of JA in the abiotic stress response, its role in drought stress is little known (Maksymiec et al. 2005; Brossa et al. 2011; Dong et al. 2013; Qiu et al. 2014; Zhao et al. 2013; Clarke et al. 2009). Jasmonic acid basically imparts drought tolerance by modulating stomatal closure and minimizing transpiration water loss. In addition, MeJA increases root hydraulic conductivity and helps plants uptake more water under drought stress (Tanaka et al. 2005; Munemasa et al. 2007; Daszkowska-Golec and Szarejko 2013; Sánchez-Romera et al. 2014). In addition, JAs play an important role in signaling the drought-induced antioxidant response by enhancing the expression and activity of the antioxidant enzymes superoxide dismutase, peroxidase, and catalase (Nafie et al. 2011; Anjum et al. 2011). However, JA biosynthesis, crosstalk and signal transduction is more or less similar between biotic and abiotic stress, with unique aspects being identified for abiotic stress response.
An F-box protein coronatine insensitive 1 (COI1), jasmonate ZIM domain (JAZ) proteins, multi-component E3 ubiquitin ligase-Skp/Cullin/F-box complex (SCFCOI1) and 26S proteasome are key players in JA signaling (Thines et al. 2007; Deshaies 1999; Turner et al. 2002). JA-Ile functions as a ligand and promotes the assembly of COI1 and JAZ proteins (Thines et al. 2007). JAZ proteins are repressors or negative regulators of JA signaling that are targeted for degradation by the SCFCOI1-dependent 26S proteasome pathway. In addition, JAZ proteins interact with co-repressor Topless (TPL) and TPL-related proteins (TPRs) via an adaptor protein, novel interactor of JAZ (NINJA), in JA signaling (Pauwels et al. 2010). Hence, JA-mediated destruction of JAZ transcription repressors leads to the activation of downstream genes (Staswick 2008; Thines et al. 2007; Pauwels and Goossens 2011). JAZ proteins target and regulate TFs belonging to bHLH factors (AtMYC2, OsBHLH1, RERJ1, MYC3, MYC4, Glabra3-GL3, enhancer of glabra 3 1 [EGL1] and transparent testa [TT8]). A few are regulated under drought stress (RERJ1, OsbHLH148), and their overexpression results in enhanced drought tolerance (Kiribuchi et al. 2005; Seo et al. 2011). JAZ proteins interact with the Apetala 2 group of TFs—target of eat 1 (TOE1) and TOE2—and repress transcription (Zhai et al. 2015). An intermediate of JA biosynthesis, 12-OPDA, also plays a role in JA signaling and has a major role in drought response (Savchenko et al. 2014).
5 Salicylic Acid (SA)
Similar to JA, the phytohormone SA plays an important role in response to biotic stresses, pathogenesis, plant growth and development, although antagonizing gene induction by JA. In addition, it participates in signaling abiotic stress responses (drought, salinity, high and low temperature, ozone, UV light and heavy metals) (Rivas-San Vicente and Plasencia 2011; Hara et al. 2012). However, its utility depends on its concentration: low concentration enhancing antioxidant capacity and high concentration inducing oxidative stress and leading to cell death (Hara et al. 2012).
The synthesis of endogenous SA levels is increased in plants exposed to drought stress, and plants susceptible to drought show reduced SA level. SA probably protects plants under stress by regulating the induction of SA-inducible PR genes (Munné-Bosch and Penuelas 2003; Sawada et al. 2006; Miura et al. 2013).
In plants, SA is synthesized in plastids via two distinct pathways: the isochorismate (IC) pathway, the major pathway, and the phenylalanine ammonia-lyase (PAL) pathway. Both pathways begin with chorismic acid, an end product of the shikimate pathway (Wildermuth et al. 2001; Catinot et al. 2008). IC synthase (ICS), responsible for converting chorismic acid to IC, is regulated by biotic stress and also drought stress (Nawrath and Métraux 1999; Hunter et al. 2013). Mutants (adr1, myb96-1d, siz1, acd6, and cpr5) that accumulated endogenous SA showed both SA-dependent disease resistance and drought tolerance (Seo and Park 2010; Miura et al. 2013).
Well-known systemic acquired resistance is induced by SA and leads to an immune response against pathogens via transcriptional reprogramming (Durrant and Dong 2004). Under drought stress, plants are protected against oxidative stress induced by drought stress by the induction of stress proteins such as glutathione S-transferases, ascorbate peroxidase (APX), and 2-cysteine peroxiredoxin by enhanced SA levels (Kang et al. 2012). Exogenous application of SA and high endogenous SA level promote stomatal closure during water deficit to conserve water, which leads to reduced photosynthesis likely because of ROS induced by SA (Senaratna et al. 2000; Korkmaz et al. 2007).
Jasmonic acid binds to effector proteins such as catalase, APX, methyl SA esterase, and carbonic anhydrase (Sanchez-Casas and Klessig 1994; Du and Klessig 1997; Slaymaker et al. 2002; Forouhar et al. 2005). However, mutant studies predicted that non-expressor of PR genes 1 (NPR1) was an SA receptor candidate (Delaney et al. 1995; Cao et al. 1997). NPR1 functions as a positive regulator of the SA-mediated defense response. In addition, NPR3 and NPR4, paralogs of NPR1, are SA receptors (Fu et al. 2012). They have a direct role in defense gene expression and affect disease resistance (Fu et al. 2012; Wu et al. 2012). They interact with cullin 3 (CUL3) ubiquitin E3 ligase and recruit NPR1 for proteasome-mediated degradation dependent on SA. Studies of mutants of the mitochondrial succinate dehydrogenase (SDH) pathway, disrupted in stress response 1 (dsr1) and SDH assembly factor 2 (sdhaf2), demonstrated that SA directly contributes to stress signaling by increasing mitochondrial H2O2 production.
6 Brassinosteroids (BRs)
Brassinosteroids are a plant-specific steroid group of plant hormones known for their role in growth, development, reproduction, and stress response (Sharma et al. 2015; Vardhini and Anjum 2015; Tang et al. 2016; Wei and Li 2016; Xia et al. 2009, 2014). Brassinolide (BL) is synthesized from campesterol via a series of reductions, hydroxylations, epimerizations, and oxidations, whereas the mevalonic acid-dependent triterpenoid pathway is used for synthesis of other major BRs (Fujioka et al. 1998; Fujioka and Yokota 2003; Chung and Choe 2013). BRs actively participate in drought stress response and tolerance, as demonstrated by enhanced drought of plants overexpressing the BR biosynthetic gene encoding cytochrome p450 (Tiwari et al. 2017). Brassinosteroids also help reduce the photoinhibition that commonly occurs under abiotic stress conditions (Ahammed et al. 2015)
The BRs are recognized by the BRASSINOSTEROID INSENSITIVE 1 (BRI1) cell-surface leucine-rich repeat kinase group of receptor proteins. BRI further interacts with co-receptor BRI-associated receptor kinase 1 (BAK1) and initiates a series of phosphorylation and dephosphorylation events resulting in the regulation of gene expression (Belkhadir and Jaillais 2015; Nakamura et al. 2017). BR-mediated signaling is transduced by the bHLH group of TFs such as CESTA and TEOSINTE BRANCHED 1, CYCLOIDEA, PCF1 (TCP) (Poppenberger et al. 2011).
Similarly, the TF BRASSINAZOLE RESISTANT 1 (BZR1), induced by BRs, plays a role in maintaining cell cycle progression even under stress (Hacham et al. 2011). In contrast, BRASSINOSTEROIDS AT VASCULAR AND ORGANIZING CENTER (BRAVO), an R2R3 MYB transcription factor, inhibits stem cell proliferation. In the root quiescent center, interaction with BRI1-EMS SUPRESSOR 1 (BES1) represses the activity of BRAVO (Vilarrasa-Blasi et al. 2014). In addition, BRs remodel the cell wall under abiotic stress by inducing genes responsible for cell wall remodeling: pectin lyase-like proteins, expansins, and xyloglucan endotransglucosylase/hydrolases (Rao and Dixon 2017). In addition, BRI1 receptor induces the expression of pectin methylesterases under stress, thereby resisting the loss of cell wall and maintaining the integrity of the cell wall via interaction of BAK1 and RECEPTOR-LIKE PROTEIN (RPL44) (Wolf et al. 2014). These mechanisms help plants in stress adaptation and increase longevity.
7 Hormonal Crosstalk
7.1 ABA Crosstalk
In response to environmental stress (drought), ABA regulates growth and development via crosstalk with other plant hormones. Abscisic acid interacts antagonistically with most plant hormones. ABA and auxin work in opposing directions in regulating growth and development. Both of these hormones control cell division, seed dormancy and germination, primary root growth, seedling growth, etc. Crosstalk between auxin and ABA in regulating growth occurs via regulation of auxin or ABA response pathways. Auxin activates the ABA response and or ABA biosynthesis. Under osmotic stress, ABA increases basipetal transport of auxin via AUX1 (an auxin influx transporter) and PIN2 (an auxin efflux transporter) (Sun and Li 2014; Wang et al. 2011; Belin et al. 2009; Liu et al. 2013; Xu et al. 2013). Similarly, ABA and CK crosstalk with each other. ABA regulates CK by regulating CK oxidase that degrades CK. Under stress, CK via cytokinin receptor kinases (AHK2 and AHK3) negatively regulates ABA, ABA signaling and stress gene expression (Tran et al. 2007; Jeon et al. 2010). ABA also acts antagonistically with ET in regulating stomatal closure. ET inhibits ABA signaling and thereby delays stomatal closure. Similarly, ABA inhibits ET biosynthesis by regulating ERF1 and long hypocotyl 5 (HY5), thereby repressing ACS5 (ethylene biosynthesis gene). The TF HY5 is a key player in the crosstalk between ABA and ET (Harrison 2012; Tanaka et al. 2005; Li et al. 2011). However, the crosstalk between ABA and JA is complex. Reduction of ABA level upregulates JA. Multiple components of ABA and JA–ET signaling pathways antagonistically interact in regulating stress-responsive gene expression, with MYC2 playing a central role or being a major hub in the crosstalk (Anderson et al. 2004; Chen et al. 2011; Fernández-Calvo et al. 2011; Sun and Li 2014).
7.2 ET Crosstalk
The ERF key regulatory proteins of ET signal transduction are also the hub of the crosstalk between ET and ABA, JA, SA, BR, and redox signaling. Under abiotic stress, both ABA and JA regulate ERFs. However, we have few reports on the crosstalk under drought stress. JA positively regulates the induction of ERFs [ERF6, JERF1, JERF3, Tsi1, OPBP1, and GmERF3 (Sewelam et al. 2013; Wu et al. 2007, 2008; Wang et al. 2004; Park et al. 2001; Zhang et al. 2009a, b)], but ABA negatively regulates the induction of few ERFs (ERF1/6) (Cheng et al. 2013; Sewelam et al. 2013). In contrast, ABA induces other ERFs (CsERF, GmERF3, LchERF, JERF3, TSRF1, TaERF1 and JERF1) (Ma et al. 2014; Zhang et al. 2009a, b; Wu et al. 2007, 2008, 2014a, b; Quan et al. 2010; Xu et al. 2007). Overexpression of TSRF1 results in enhanced drought tolerance (Quan et al. 2010; Cheng et al. 2013). The negative regulator AtERF7 inhibits ABA-induced gene expression, thereby decreasing drought stress tolerance (Song et al. 2005).
7.3 JA Crosstalk
The JA crosstalk with ABA at MYC2 is involved in drought stress signaling and activates genes such as RD22 and RD26, which are also upregulated under drought stress (Abe et al. 2003; Fujita et al. 2004, 2006; Harb et al. 2010). JA and GA also crosstalk, which is mediated by direct interaction between DELLA and JAZ proteins, thereby competing for the JAZ–MYC2 interaction that activates JA-responsive genes (Boter et al. 2004; Hou et al. 2010). Expression of the MYC2 target RGL3, which encodes DELLA, is induced by JA signaling (Wild et al. 2012). MYC2 is released when JA degrades JAZ. DELLA is also the hub of crosstalk between GA and ABA under abiotic stress. In addition, there is crosstalk between JA and ET: both activate Arabidopsis AtERF1, which imparts drought tolerance (Cheng et al. 2013).
7.4 SA Crosstalk
SA interacts with other phytohormones, and depending on the hormone, has a synergistic or antagonistic relation under optimal and stressful conditions. SA-induced ABA improves osmotic adaptation and growth under normal, salt and other abiotic stress (Szepesi et al. 2009; Szalai et al. 2011). Mitogen-activated protein kinases are key players of signaling components where antagonistic interaction between SA and JA occurs (Khan et al. 2012a, b). In addition, NPR1, the master regulator of SA-mediated defense, is a critical component of the epibassinolide-mediated increase in abiotic stress tolerance (heat and salt) (Divi et al. 2010).
7.5 BR Crosstalk
BR and ABA crosstalk via ABI3/viviparous1 (ABI3/VP1) and related to ABI3/VP1 (RAV1) and induce BRI expression (Saini et al. 2015). Maintenance of cell wall integrity is via interaction of BR with other hormones (Wolf et al. 2014). The long-distance effect of BR is via crosstalk with multiple hormones (Vriet et al. 2013; Gudesblat and Russinova 2011). BRs antagonistically cross-interact with ABA, ET, SA, auxin, GA and polyamines (Vardhini and Anjum 2015). Analysis of det-2 and bri-1 BR mutants demonstrated that BIN2 negatively regulates BR signaling in the presence of ABA signaling, which is via ABI1/2 (PP2Cs) that function downstream of BRI1 and upstream of BIN2 and regulate BR signaling (Zhang et al. 2009a, b). ABI1/2 dephosphorylate BIN2, and ABA inhibits BIN2 phosphorylation by BES1, thereby reducing BR signaling (Wang et al. 2018). BIN2 also interacts with ABI5 and phosphorylates it and mediates ABA signaling (Hu and Yu 2014). Both ABA and BR induce the expression of BRASSINOSTEROID-SIGNALING KINASE 5 (BSK5), a key player in ABA signaling. Similar crosstalk between ABA and BR occurs with a TF, BZR1 (Yang et al. 2016). BR and ET crosstalk via H2O2 and regulate stress tolerance (Zhu et al. 2016). BR signaling interacts with SA signaling via the TF WRKY70, which negatively regulates SA biosynthesis. NPR1, regulating SA signaling, interacts with BIN2 and BZR1 and regulates stress tolerance (Divi et al. 2010; Li et al. 2013).
References
Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
Ahammed GJ, Li X, Xia X-J, Shi K, Zhou Y-H, Yu J-Q (2015) Enhanced photosynthetic capacity and antioxidant potential mediate brassinosteriod-induced phenanthrene stress tolerance in tomato. Environ Pollut 201:58–66
Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479
Anjum SA, Xie X, Wang L, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032
Anjum SA, Ashraf U, Zohaib A, Tanveer M, Naeem M, Ali I, Nazir U (2017) Growth and development responses of crop plants under drought stress: a review. Zemdirbyste 104:267–276
Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Belin C, Megies C, Hauserová E, Lopez-Molina L (2009) Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell 21:2253–2268
Belkhadir Y, Jaillais Y (2015) The molecular circuitry of brassinosteroid signaling. New Phytol 206:522–540
Bisson MM, Groth G (2010) New insight in ethylene signaling: autokinase activity of ETR1 modulates the interaction of receptors and EIN2. Mol Plant 3:882–889
Boneh U, Biton I, Zheng C, Schwartz A, Ben-Ari G (2012) Characterization of potential ABA receptors in Vitis vinifera. Plant Cell Rep 31:311–321
Boter M, Ruíz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591
Boudsocq M, Droillard M-J, Barbier-Brygoo H, Laurière C (2007) Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol Biol 63:491–503
Brossa R, López-Carbonell M, Jubany-Marí T, Alegre L (2011) Interplay between abscisic acid and jasmonic acid and its role in water-oxidative stress in wild-type, ABA-deficient, JA-deficient, and ascorbate-deficient Arabidopsis plants. J Plant Growth Regul 30:322–333
Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63
Catinot J, Buchala A, Abou-Mansour E, Métraux J-P (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett 582:473–478
Cela J, Chang C, Munné-Bosch S (2011) Accumulation of γ-rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52:1389–1400
Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot (Lond) 95:901–915
Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352
Cheng M-C, Liao P-M, Kuo W-W, Lin T-P (2013) The Arabidopsis ETHYLENE-RESPONSE-FACTOR1 regulates abiotic-stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582
Choi H-i, Hong J-h, Ha J-o, Kang J-y, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730
Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signaling of water shortage. Plant J 52:167–174
Chung Y, Choe S (2013) The regulation of brassinosteroid biosynthesis in Arabidopsis. Crit Rev Plant Sci 32:396–410
Clarke SM, Cristescu SM, Miersch O, Harren FJ, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679
Daszkowska-Golec A, Szarejko I (2013) Open or close the gate–stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138
Delaney T, Friedrich L, Ryals J (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92:6602–6606
Deshaies R (1999) SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15
Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151
Dong W, Wang M, Xu F, Quan T, Peng K, Xiao L, Xia G (2013) Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of ABA signalling and ROS scavenging. Plant Physiol 161:1217–1218
Du H, Klessig DF (1997) Identification of a soluble, high-affinity salicylic acid-binding protein in tobacco. Plant Physiol 113:1319–1327
Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, De Bodt S, Bossche RV, De Milde L, Yoshizumi T, Matsui M (2013) The ETHYLENE RESPONSE FACTOR 6 acts as central regulator of leaf growth under water limiting conditions in Arabidopsis thaliana. Plant Physiol 5:e70289
Dubois M, Van den Broeck L, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23:311–323
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715
Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297
Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102:1773–1778
Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486(7402):228
Fujii H, Zhu J-K (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385
Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164
Fujioka S, Noguchi T, Yokota T, Takatsuto S, Yoshida S (1998) Brassinosteroids in Arabidopsis thaliana. Phytochemistry 48:595–599
Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LSP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876
Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, et al (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132. https://doi.org/10.1093/pcp/pcp147
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442
Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993
Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430
Ghasemi PA, Sajjadi SE, Parang K (2014) A review (research and patents) on jasmonic acid and its derivatives. Arch Pharm 347:229–239
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151
Gudesblat GE, Russinova E (2011) Plants grow on brassinosteroids. Curr Opin Plant Biol 14:530–537
Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848
Hara M, Furukawa J, Sato A, Mizoguchi T, Miura K (2012) Abiotic stress and role of salicylic acid in plants. In: Abiotic stress responses in plants. Springer, pp 235–251
Harb A, Krishnan A, Ambavaram MM, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271
Harrison MA (2012) Cross-talk between phytohormone signaling pathways under both optimal and stressful environmental conditions. In: Phytohormones and abiotic stress tolerance in plants. Springer, pp 49–76
He H, Li J (2008) Proteomic analysis of phosphoproteins regulated by abscisic acid in rice leaves. Biochem Biophys Res Commun 371:883–888
He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916
Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884–894
Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680
Hunter LJ, Westwood JH, Heath G, Macaulay K, Smith AG, MacFarlane SA, Palukaitis P, Carr JP (2013) Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLoS ONE 8:e66530
Hussain M, Farooq S, Hasan W, Ul-Allah S, Tanveer M, Farooq M, Nawaz A (2018) Drought stress in sunflower: Physiological effects and its management through breeding and agronomic alternatives. Agric Water Manag 201:152–166
Jaradat MR, Feurtado JA, Huang D, Lu Y, Cutler AJ (2013) Multiple roles of the transcription factor AtMYBR1/AtMYB44 in ABA signaling, stress responses, and leaf senescence. BMC Plant Biol 13:192
Jayakannan M, Bose J, Babourina O, Shabala S, Massart A, Poschenrieder C, Rengel Z (2015) The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J Exp Bot 66:1865–1875
Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku SJ, Cho C, Lee DJ, Lee EJ, Strnad M (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386
Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J, Garrett WM, Kessenbrock M, Groth G, Tucker ML (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci USA 109:19486–19491
Kang G, Li G, Xu W, Peng X, Han Q, Zhu Y, Guo T (2012) Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J Proteome Res 11:6066–6079
Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11:479–485
Khan MIR, Syeed S, Nazar R, and Anjum NA (2012a) An insight into the roleofsalicylicacidandjasmonicacidinsaltstresstolerance. In: Khan NA, Nazar R, Iqbal N, Anjum NA (eds) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin, pp 277–300. https://doi.org/10.1007/978-3-642-25829-9_12
Khan NA, Nazar R, Iqbal N, Anjum NA (2012b) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin. https://doi.org/10.1007/978-3-642-25829-9
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72:427–441
Kim H, Hwang H, Hong J-W, Lee Y-N, Ahn IP, Yoon IS, Yoo S-D, Lee S, Lee SC, Kim B-G (2011) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63:1013–1024
Kiribuchi K, Jikumaru Y, Kaku H, Minami E, Hasegawa M, Kodama O, Seto H, Okada K, Nojiri H, Yamane H (2005) Involvement of the basic helix-loop-helix transcription factor RERJ1 in wounding and drought stress responses in rice plants. Biosci Biotechnol Biochem 69:1042–1044
Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci USA 107:15986–15991
Klingler JP, Batelli G, Zhu JK (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J Exp Bot 61:3199–3210
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44:939–949
Korkmaz A, Uzunlu M, Demirkiran AR (2007) Treatment with acetyl salicylic acid protects muskmelon seedlings against drought stress. Acta Physiol Plant 29:503–508
Lacey RF, Binder BM (2014) How plants sense ethylene gas—the ethylene receptors. J Inorg Biochem 133:58–62
Leung J, Bouvier-Durand M, Morris P-C, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264(5164):1448–1452
Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771
Li Z, Zhang L, Yu Y, Quan R, Zhang Z, Zhang H, Huang R (2011) The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J 68:88–99
Li J, Besseau S, Törönen P, Sipari N, Kollist H, Holm L, Palva ET (2013) Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytol 200:457–472
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang H-Q, Luan S, Li J, He Z-H (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA 110:15485–15490
Lopez-Molina L, Mongrand S, Chua N-H (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98:4782–4787
Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540
Ma S, Gong Q, Bohnert HJ (2006) Dissecting salt stress pathways. J Exp Bot 57:1097–1107
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068
Ma Y, Zhang L, Zhang J, Chen J, Wu T, Zhu S, Yan S, Zhao X, Zhong G (2014) Expressing a Citrus ortholog of Arabidopsis ERF1 enhanced cold-tolerance in tobacco. Sci Hortic 174:65–76
Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56:613–626
Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346
McConn M, Creelman RA, Bell E, Mullet JE (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA 94:5473–5477
Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349–368
Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264(5164):1452–1455
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309
Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 73:91–104
Morgan PW, Drew MC (1997) Ethylene and plant responses to stress. Physiol Plant 100:620–630
Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y (2007) The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol 143:1398–1407
Munné-Bosch S, Penuelas J (2003) Photo-and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217:758–766
Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Nafie E, Hathout T, Mokadem A, Shyma A (2011) Jasmonic acid elicits oxidative defense and detoxification systems in Cucumis melo L. cells. Braz J Plant Physiol 23:161–174
Nakamura A, Tochio N, Fujioka S, Ito S, Kigawa T, Shimada Y, Matsuoka M, Yoshida S, Kinoshita T, Asami T (2017) Molecular actions of two synthetic brassinosteroids, iso-carbaBL and 6-deoxoBL, which cause altered physiological activities between Arabidopsis and rice. PLoS ONE 12:e0174015
Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970
Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2. 2, SRK2E/SnRK2. 6/OST1 and SRK2I/SnRK2. 3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta (BBA)-Gene Regul Mech 1819:97–103
Nawrath C, Métraux J-P (1999) Salicylic acid induction–deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404
Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326(5958):1373–1379
Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148
Park JM, Park C-J, Lee S-B, Ham B-K, Shin R, Paek K-H (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2–type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046
Pauwels L, Barbero GF, Geerinck J, Tilleman S, Gurnewald W, Perez AC, Chico JM, Bossche RV, Sewell J, Gil E, Garcia-Casado G, Wltters E, Inze D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signaling. Nature 464:788–791
Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100
Poppenberger B, Rozhon W, Khan M, Husar S, Adam G, Luschnig C, Fujioka S, Sieberer T (2011) CESTA, a positive regulator of brassinosteroid biosynthesis. EMBO J 30:1149–1161
Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev 23:512–521
Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582
Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208
Quan R, Hu S, Zhang Z, Zhang H, Zhang Z, Huang R (2010) Overexpression of an ERF transcription factor TSRF1 improves rice drought tolerance. Plant Biotechnol J 8:476–488
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401
Rao X, Dixon RA (2017) Brassinosteroid mediated cell wall remodeling in grasses under abiotic stress. Front Plant Sci 8:806
Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe O, Samaha R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110
Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338
Romero P, Lafuente MT, Rodrigo MJ (2012) The Citrus ABA signalosome: identification and transcriptional regulation during sweet orange fruit ripening and leaf dehydration. J Exp Bot 63:4931–4945
Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11
Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signaling. Plant J 37:354–369
Saini S, Sharma I, Pati PK (2015) Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Front Plant Sci 6:950
Sanchez-Casas P, Klessig DF (1994) A salicylic acid-binding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species. Plant Physiol 106:1675–1679
Sánchez-Romera B, Ruiz-Lozano JM, Li G, Luu DT, Martínez-Ballesta Mdel C, Carvajal M, Zamarreño AM, García-Mina JM, Maurel C, Aroca R (2014) Enhancement of root hydraulic conductivity by methyl jasmonate and the role of calcium and abscisic acid in this process. Plant Cell Environ 37:995–1008
Saruhashi M, Ghosh TK, Arai K, Ishizaki Y, Hagiwara K, Komatsu K, Shiwa Y, Izumikawa K, Yoshikawa H, Umezawa T (2015) Plant Raf-like kinase integrates abscisic acid and hyperosmotic stress signaling upstream of SNF1-related protein kinase 2. Proc Natl Acad Sci USA 112:E6388–E6396
Sato A, Sato Y, Fukao Y, Fujiwara M, Umezawa T, Shinozaki K, Hibi T, Taniguchi M, Miyake H, Goto DB (2009) Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2. 6 protein kinase. Biochem J 424:439–448
Savchenko T, Kolla V, Wang C-Q, Nasafi Z, Hicks D, Phadungchob B, Chehab W, Brandizzi F, Froehlich J, Dehesh K (2014) Functional convergence of oxylipin and ABA pathways controls stomatal closure in response to drought. Plant Physiol 164:1151–1160
Sawada H, Shim I-S, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis—modulation by salt stress in rice seedlings. Plant Sci 171:263–270
Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6(9):e230
Seiler C, Harshavardhan VT, Reddy PS, Hensel G, Kumlehn J, Eschen-Lippold L, Rajesh K, Korzun V, Wobus U, Lee J (2014) Abscisic acid flux alterations result in differential ABA signalling responses and impact assimilation efficiency in barley under terminal drought stress. Plant Physiol 164:1677–1696
Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161
Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483
Seo J, Joo J, Kim M, Kim Y, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD (2011) OsbHlH148, a basic helix-loop-helix protein, interacts with OsJaZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907–921
Sewelam N, Kazan K, Thomas-Hall SR, Kidd BN, Manners JM, Schenk PM (2013) Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis. PLoS ONE 8:e70289
Sharma I, Bhardwaj R, Pati PK (2015) Exogenous application of 28-homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety Pusa Basmati-1. J Plant Growth Regul 34:509–518
Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C, Zhu S-Y (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823
Singh A, Jha SK, Bagri J, Pandey GK (2015) ABA inducible rice protein phosphatase 2C confers ABA insensitivity and abiotic stress tolerance in Arabidopsis. PLoS ONE 10:e0125168
Sirichandra C, Davanture M, Turk BE, Zivy M, Valot B, Leung J, Merlot S (2010) The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS ONE 5:e13935
Sirichandra C, Gu D, Hu H, Davanture M, Lee S, Djaoui M, et al (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986. https://doi.org/10.1016/j.febslet.2009.08.033
Slaymaker DH, Navarre DA, Clark D, del Pozo O, Martin GB, Klessig DF (2002) The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci USA 99:11640–11645
Song C-P, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu J-K (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396
Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71
Stepanova AN, Alonso JM (2009) Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol 12:548–555
Sun J, Li C (2014) Cross talk of signaling pathways between ABA and other phytohormones. In: Abscisic acid: metabolism, transport and signalling. Springer, pp 243–253
Sun L, Wang Y-P, Chen P, Ren J, Ji K, Li Q, Li P, Dai S-J, Leng P (2011) Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. J Exp Bot 62:5659–5669
Swamy PM, Smith BN (1999) Role of abscisic acid in plant stress tolerance. Curr Sci 76:1220–1227
Szalai G, Pál M, Janda T (2011) Abscisic acid may alter the salicylic acid-related abiotic stress response in maize. J Agron Crop Sci 197:368–377
Szepesi Á, Csiszár J, Gémes K, Horváth E, Horváth F, Simon ML, Tari I (2009) Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. J Plant Physiol 166:914–925
Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343
Tang J, Han Z, Chai J (2016) Q&A: what are brassinosteroids and how do they act in plants? BMC Biol 14(1):113
Tanveer M, Shahzad B, Sharma A, Khan EA (2018) 24-Epibrassinolide application in plants: An implication for improving drought stress tolerance in plants. Plant Physiol Biochem 135:295–303
Thao NP, Khan MIR, Thu NBA, Hoang XLT, Asgher M, Khan NA, Tran L-SP (2015) Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiol 169:73–84
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF COI1 complex during jasmonate signaling. Nature 448(7154):661
Tiwari S, Lata C, Singh Chauhan P, Prasad V, Prasad M (2017) A functional genomic perspective on drought signaling and its crosstalk with phytohormone-mediated signaling pathways in plants. Curr Genomics 18:469–482
Tran LSP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628
Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(suppl 1):S153–S164
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106:17588–17593
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839
Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y, Peck SC, Shinozaki K (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci Signal 6(270):rs8
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637
van Loon LC, Geraats BP, Linthorst HJ (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191
Vardhini BV, Anjum NA (2015) Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Front Environ Sci 2:67
Vilarrasa-Blasi J, González-García M-P, Frigola D, Fàbregas N, Alexiou KG, López-Bigas N, Rivas S, Jauneau A, Lohmann JU, Benfey PN (2014) Regulation of plant stem cell quiescence by a brassinosteroid signaling module. Dev Cell 30:36–47
Vilela B, Nájar E, Lumbreras V, Leung J, Pagès M (2015) Casein kinase 2 negatively regulates abscisic acid-activated SnRK2s in the core abscisic acid-signaling module. Mol Plant 8:709–721
Vriet C, Russinova E, Reuzeau C (2013) From squalene to brassinolide: the steroid metabolic and signaling pathways across the plant kingdom. Mol Plant 6:1738–1757
Waadt R, Manalansan B, Rauniyar N, Munemasa S, Booker MA, Brandt B, Waadt C, Nusinow DA, Kay SA, Kunz H-H (2015) Identification of open stomata1-interacting proteins reveals interactions with sucrose non-fermenting1-related protein Kinases2 and with Type 2A protein phosphatases that function in abscisic acid responses. Plant Physiol 169:760–779
Wan L, Zhang J, Zhang H, Zhang Z, Quan R, Zhou S, Huang R (2011) Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS ONE 6(9):e25216
Wang H, Huang Z, Chen Q, Zhang Z, Zhang H, Wu Y, Huang D, Huang R (2004) Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Mol Biol 55:183–192
Wang L, Hua D, He J, Duan Y, Chen Z, Hong X, Gong Z (2011) Auxin Response Factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet 7(7):e1002172
Wang H, Tang J, Liu J, Hu J, Liu J, Chen Y, Cai Z, Wang X (2018) Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol Plant 11:315–325
Wasternack C, Hause B (2002) Jasmonates and octadecanoids: signals in plant stress responses and development. Prog Nucleic Acid Res Mol Biol 72:165–221
Watanabe H, Saigusa M, Hase S, Hayakawa T, Satoh S (2004) Cloning of a cDNA encoding an ETR2-like protein (Os-ERL1) from deep water rice (Oryza sativa L.) and increase in its mRNA level by submergence, ethylene, and gibberellin treatments. J Exp Bot 55:1145–1148
Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant 9:86–100
Wild M, Davière J-M, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24:3307–3319
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414(6863):562
Wolf S, Van Der Does D, Ladwig F, Sticht C, Kolbeck A, Schürholz A-K, Augustin S, Keinath N, Rausch T, Greiner S (2014) A receptor-like protein mediates the response to pectin modification by activating brassinosteroid signaling. Proc Natl Acad Sci USA 111:15261–15266
Wu L, Chen X, Ren H, Zhang Z, Zhang H, Wang J, Wang X-C, Huang R (2007) ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta 226:815–825
Wu L, Zhang Z, Zhang H, Wang X-C, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963
Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647
Wu D, Ji J, Wang G, Guan C, Jin C (2014a) LchERF, a novel ethylene-responsive transcription factor from Lycium chinense, confers salt tolerance in transgenic tobacco. Plant Cell Rep 33:2033–2045
Wu X, He J, Chen J, Yang S, Zha D (2014b) Alleviation of exogenous 6-benzyladenine on two genotypes of eggplant (Solanum melongena Mill.) growth under salt stress. Protoplasma 251:169–176
Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814
Xia X, Gao CJ, Song LX, Zhou Y, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37:2036–2050
Xu Z-S, Xia L-Q, Chen M, Cheng X-G, Zhang R-Y, Li L-C, Zhao Y-X, Lu Y, Ni Z-Y, Liu L (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732
Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, Zhang J (2013) Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. New Phytol 197:139–150
Yang X, Bai Y, Shang J, Xin R, Tang W (2016) The antagonistic regulation of abscisic acid-inhibited root growth by brassinosteroids is partially mediated via direct suppression of ABSCISIC ACID INSENSITIVE 5 expressions by BRASSINAZOLE RESISTANT 1. Plant Cell Environ 39:1994–2003
Yau CP, Wang L, Yu M, Zee SY, Yip WK (2004) Differential expression of three genes encoding an ethylene receptor in rice during development, and in response to indole-3-acetic acid and silver ions. J Exp Bot 55:547–556
Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006) ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685
Zhai Q, Zhang X, Wu F, Feng H, Deng L, Xu L, Zhang M, Wang Q, Li C (2015) Transcriptional mechanism of jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27:2814–2828
Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158:961–969
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009a) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796
Zhang S, Cai Z, Wang X (2009b) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc Natl Acad Sci USA 106:4543–4548
Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 237:1443–1451
Zhao XC, Schaller GE (2004) Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett 562:189–192
Zhao ML, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY (2013) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zhu T, Deng X, Zhou X, Zhu L, Zou L, Li P, Zhang D, Lin H (2016) Ethylene and hydrogen peroxide are involved in brassinosteroid-induced salt tolerance in tomato. Sci Rep 6:35392
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Govind, G., Harshavardhan, V.T., Hong, CY. (2020). Phytohormone Signaling in Response to Drought. In: Hasanuzzaman, M., Tanveer, M. (eds) Salt and Drought Stress Tolerance in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-030-40277-8_12
Download citation
DOI: https://doi.org/10.1007/978-3-030-40277-8_12
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-40276-1
Online ISBN: 978-3-030-40277-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)