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Brassinosteroid Signaling and Complex Interplay of ROS, NADPH Oxidase, and MAPK Mediated Biotic and Abiotic Stress Acclimation in Plants
C H A P T E R
26 Brassinosteroid Signaling and Complex Interplay of ROS, NADPH Oxidase, and MAPK Mediated Biotic and Abiotic Stress Acclimation in Plants Deepesh Bhatt1, , Mayank Sharma2,, Manoj Nath3, Megha D. Bhatt4 and Saurabh Badoni5 1
Department of Biotechnology, Shree Ramkrishna Institute of Computer Education and Applied Sciences, Veer Narmad South Gujarat University, Surat, Gujarat, India 2Martin Luther University of Halle-Wittenberg, Halle, Germany 3 Indian Council of Agricultural Research, New Delhi, Uttar Pradesh, India 4GSFC AgroTech Ltd. Gujarat State Fertilizers & Chemicals Ltd., Vadodara, India 5Plant Breeding Division, International Rice Research Institute, Metro Manila, Philippines
O U T L I N E 26.1 Introduction
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26.6 BR Mediated Defense Signaling
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26.2 Brassinosteroids
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26.3 Brassinosteroid Signaling in Plants
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26.7 BR Mediated ROS Signaling and Its Role in Plant Defense
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26.8 Conclusion
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26.4 Transcription Factors Involved in BR Signaling
409
References
413
26.5 Role of RD26 in BR Signaling
410
Further Reading
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26.1 INTRODUCTION Plants are constantly exposed to multiple biotic and abiotic stresses during their entire life, which include pathogen attacks and insect herbivory, high or low
temperatures stress, drought and salinity stress, etc. Therefore, to survive, plants have evolved a range of intricate signaling mechanisms thus adapting towards these fluctuating environments. Plant growth regulators, also termed as phytohormones, are increasingly
The authors (Deepesh Bhatt and Mayank Sharma) contributed equally to this work.
Plant Signaling Molecules. DOI: https://doi.org/10.1016/B978-0-12-816451-8.00025-3
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© 2019 Elsevier Inc. All rights reserved.
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26. BRASSINOSTEROID SIGNALING IN PLANTS
recognized to play vital roles in plant stress adaptations. Several studies indicated that biological processes in plants are influenced by stressful conditions, which are regulated through different hormonal signaling pathways in plants (Teale et al., 2008). Phytohormones, like salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA), are primary signals that regulate responses to mitigate biotic and abiotic stresses in plants (Lorenzo and Solano, 2005; Mauch-Mani and Mauch, 2005). These stresses, if not properly regulated, may further lead to the generation of a key intermediate termed as reactive oxygen species (ROS). ROS are generated in response to stress as well as to regulate normal metabolic processes as a signaling agent (Mittler et al., 2011; Sewelam et al., 2016). Additionally, respiratory burst oxidase homologs (RBOHs) and NADPH oxidases are also known to be major components of ROS production system in plants (Suzuki et al., 2011; Kadota et al., 2015). Furthermore several other studies also propose that ROS plays a critical role in enhancing stress tolerance by activating mitogenactivated protein kinases (MAPKs), antioxidant enzymes, and other related transcription factors (Gechev et al., 2006). The generation of ROS has been shown to be a key process that is shared among many transcriptional pathways related to stress signaling. Thus at the molecular level, the perception of external stimuli results in the subsequent activation of stress signaling through some intermediate signal molecules. Brassinosteroids are a group of steroidal hormones and play a major role in various developmental pathways and are involved in stress response (Choudhary et al., 2012). Here in this chapter we will mainly emphasize how brassinosteroids are able to influence and regulate concomitant generation of ROS, NADPH oxidase, and MAPK, which act as intermediate components in the signaling cascade to regulate biotic and abiotic stress acclimation in plants.
26.2 BRASSINOSTEROIDS Mitchell and coworkers explored a sixth class of plant hormones named brassinosteroids (BRs) in 1970 (Mitchell et al., 1970). BR was first isolated from the pollen of Brassica napus. BRs are polyhydroxysteroids similar to steroid hormones from animals (Clouse, 2011). Furthermore they play an important role in regulating various aspects of plant growth and development (Wei and Li, 2016). This includes cell division and elongation, tissue morphogenesis, plant defense, seed germination, and reproduction (Krishna, 2003; Ashraf et al., 2010). They also play a direct or indirect role in stress signaling in plants (Bajguz and Hayat, 2009). Approximately 70 different kinds of analogue of BRs have been identified to date from various plant species and tissue samples. Brassinolide has
FIGURE 26.1 Chemical structure of the most active brassinosteroid ‘brassinolide’ C28H48O6 (Image from PubChem) and its phytochemical compounds tree.
been reported as a most active BR identifies hitherto (Grove et al., 1979, Tang et al., 2016) (Fig. 26.1). BRs are continuously biosynthesized, mostly in pollens, immature seeds, roots, and flower (Takatsuto, 1994; Kutschera and Wang, 2012). Excess of BRs can be metabolized by plants via different chemical reactions to render them into inactive form. However, they can be converted into the active form whenever needed to maintain the BR homeostasis (Bishop and Yokota, 2001; Bajguz, 2007). Plant cell consists of various receptors for BRs, which recognize them and stimulate the downstream signaling processes. Characterization of BR-insensitive (bri1) mutants led to the discovery of the first BR receptor in Arabidopsis thaliana (Clouse et al., 1996). BRI1 encodes a leucine-rich repeat-receptor like kinase (LRR-RLK) composing of an intracellular kinase domain and extracellular LRR domain (Li and Chory, 1997). The bri1 mutants were shown to be male sterile with several developmental and tissue deformities. Three BRI1 homologs namely BRL1, BRL2, and BRL3 (BRI1 like 1, 2, and 3) were also reported to recognize BRs in Arabidopsis (Cano-Delgado et al., 2004), though they display a weak phenotype in respective knockout plants when compared with BRI1. A further molecular dissection, by two different scientific groups, contributed in identification of interacting partners of BRI1 named BRI1 associated kinase 1 (BAK1) or somatic embryogenesis receptor-like kinase (SERK3) (Hecht et al., 2001; Nam and Li, 2002). BAK1 interacts with BRI1 to persuade the BR signaling. The SERK family of proteins with five members seems to play an important role in BR signaling. SERK1 and SERK4 have a similar role as of BAK1/SERK3 in BR signaling. Just to avoid confusion it should be noted that BAK1 and SERK3 were discovered and named separately, however later on it came out that BAK1 and SERK3 are the same protein.
26.3 BRASSINOSTEROID SIGNALING IN PLANTS BR signaling is a phosphorylation and dephosphorylation relay system among BR receptors, coreceptors,
PLANT SIGNALING MOLECULES
26.4 TRANSCRIPTION FACTORS INVOLVED IN BR SIGNALING
and downstream transcription factors. In absence of BR, a BRI1-KINASE INHIBITOR 1 (BKI1) remains bound to BRI1 (Wang et al., 2005; Wang and Chory, 2006). The binding of BR to BRI1 and coreceptor BAK1 releases BKI1 and makes it available for 14-3-3 proteins that phosphorylate it and thus inhibit its binding to BRI1 (Gampala et al., 2007). Furthermore the mutual phosphorylation of BRI1 and BAK1 leads to activation of downstream signaling. The activation of BRI1 and BAK1 also requires the TWISTED DWARF 1 (TWD1/ FKBP42) protein (Zhao et al., 2016). An activated BRI1 phosphorylates the downstream signaling proteins namely BR-SIGNALING KINASE (BSK1) and CONSTITUTIVE DIFFERENTIAL GROWTH 1 (CDG1) kinase (Tang et al., 2008; Kim et al., 2009, 2011; Sreeramulu et al., 2013). After phosphorylation, this in turn leads to the activation of BRI1-SUPPRESSOR 1 (BSU1). BSU1 is a PP1-type phosphatase (Kim et al., 2011). The activation of BRI1 and BAK1 also requires the TWISTED DWARF 1 (TWD1/FKBP42) protein. The BSU1 further dephosphorylates and inactivates BRASSINOSTEROID INSENSITIVE 2 (BIN2). BIN2 is a G11SK3-like kinase and proposed to be degraded via its ubiquitinylation by a ubiquitin ligase KINK SUPPRESSED IN BZR1-1D (KIB1) (Zhu et al., 2017). Another protein, BES1/BZR1 (BRI1 EMS SUPPRESSOR
409
1/BRASSINAZOLE RESISTANT 1), a BR responsive transcription factor, plays a key role in activation of BRinduced genes. In absence of BR, the BIN2 phosphorylates BES1/BZR1 leading to its inactivation. But in the presence of BR, BIN2 is degraded and PROTEIN PHOSPHATASE 2A (PP2A) dephosphorylates BES1/ BZR1 (He et al., 2001). The BES1/BZR1 later enters in the nucleus, binds to DNA and activates the BR-induced genes with the help of some additional transcription factors (Ryu et al., 2007). For a schematic view, refer to Fig. 26.2A B.
26.4 TRANSCRIPTION FACTORS INVOLVED IN BR SIGNALING Genome-wide analysis of genes regulated by BES1/ BZR1 revealed that the expression of several thousand genes is influenced in BR signaling (Yu et al., 2011; Sun et al., 2010). The downstream BR signaling genes are either directly or indirectly regulated by BES1/BZR1. Several BES1/BZR1 interacting proteins and transcription factors have been identified so far. The complex interplay with these transcription factors in turn regulates the expression of BR signaling genes (Li, 2010). This include PHYTOCHROME-INTERACTING FACTORS
FIGURE 26.2 (A) A schematic view of BR-signaling in plant cell. A BR-regulated transcription factor BES1/BZR1 is the main player in BRsignaling. In absence of BR, it remains phosphorylated and cannot bind to BR responsive gene in the nucleus. 14-3-3 protein sequesters BES1/ BZR1 and keeps it phosphorylated. (See Section 26.3 for details.) (B) A schematic view of BR-signaling in plant cell. When BR is available and binds to BR receptors and coreceptors, this phosphorylates several interacting proteins. A protein, BKI1, when phosphorylated, sequesters 143-3 protein thus keeping BES1/BZR1 free. PP2A dephosphorylates BES1/BZR1 and later it enters in the nucleus to activates the BR responsive genes. (See Section 26.3 for details.) Source: Model adapted from Nolan, T.M., Brennan, B., Yang, M., Chen, J., Zhang, M., Li, Z., et al., 2017. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev. Cell 41, 33 46.
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410 TABLE 26.1 Stability
26. BRASSINOSTEROID SIGNALING IN PLANTS
List of Proteins That Directly Bind to BES1 and or BZR1 and Regulate BR Responsive Gene Expression or Protein Binding partner
Gene name
Molecular activity
PIFs (PHYTOCHROME-INTERACTING FACTORS)
Regulation of BR responsive genes
BES1/BZR1 De Lucas and Prat (2014)
ARF6/8 (AUXIN RESPONSIVE TRANSCRIPTION FACTORS)
Regulation of growth and defense related genes
PIF4 and BZR1
Oh et al. (2012)
MYB30
Regulation of BR responsive gene induction and ABA response
BES1
Li et al. (2009)
HAT1 (HOMEODOMAIN-LEUCINE ZIPPER PROTEIN 1)
Control of BR responsive genes
BES1
Li et al. (2009)
BRAVO(BRs AT VASCULAR AND ORGANIZING Regulation of cell division in quiescent center CENTER)
BES1
Vilarrasa-Blasi et al. (2014)
BIM1 (BES1-INTERACTING MYC-LIKE1)
Control of BR responsive genes
BES1
Yin et al. (2005)
TOPLESS and TOPLESS Related (TPR)
Antagonist of ABA signaling
BES1
Espinosa-Ruiz et al. (2017)
DSK2(DOMINANT SUPPRESSOR OF KAR2)
BES1 degradation during stress condition
BES1
Nolan et al. (2017)
(PIFs), BES1-INTERACTING MYC-LIKE1 (BIM1), the auxin responsive transcription factors (ARFs), ATBS1/ PRE (ACTIVATION-TAGGED bri1 SUPPRESSOR1/ PACLOBUTRAZOL-RESISTANCE), AIFs/IBH1 (ATBS1INTERACTING FACTORS/INCREASED LAMINA INCLINATION INTERACTING bHLH1) bHLH transcription factors, etc. (Wang et al., 2009; Zhang et al., 2009; de Lucas and Prat, 2014; Oh et al., 2012; Wang et al., 2012). PIFs are the transcription factors regulated by light and circadian clock. PIF4 has been validated to interact with BZR1 and forms a heterodimer, which together binds to the G-BOX (CACGTG) element present in the upstream promoter region of BR responsive genes. Similarly BIM1 interacts with BES1 and binds together with E-Box (CANNTG) element. The ARF6 and ARF8 also shown to interact with BZR1 and later on bind to ARF motif (TGTCTC) present in the promoter region of BR signaling genes. BZR1, PIFs, and ARFs together activate the downstream basic HELIX LOOP HELIX (bHLH) transcription factors including ATBS1/PRE family protein, which works as antagonist to AIFs/IBH1 proteins and activate proteins, which promotes the cell elongation. Similarly, a number of other transcription factors are involved in BR signaling that are directly regulated by BES1/BZR1. A list of such proteins is included in Table 26.1.
26.5 ROLE OF RD26 IN BR SIGNALING BR plays an important role in stress acclimation. Plants, being sessile in nature, try to reduce its growth
References
and development to expense the resources in stress management (Claeys and Inze, 2013). BES1 is known to be involved in reduction of plant growth under stress conditions especially when the drought stress is encountered. RESPONSIVE TO DESICCATION 26 (RD26) is a NAC transcription factor, which has been shown to play a crucial role in abiotic stress signaling in plants. The expression of RD26 gene is regulated by BES1. BES1 binds to the BRRE-binding site present in the promoter region of RD26 gene (Tran et al., 2004). BR response was found to be aberrated in plants overexpressing RD26 gene. The plants showed a strong phenotype of reduced growth and development. RD26 is induced under stress conditions thus providing a hint for RD26 as a connecting link between stress signaling and BR responses (Fujita et al., 2004). Genomewide analysis of these RD26OX plants revealed the antagonist expression of RD26 and BR-responsive genes. The output provided a hint that RD26 might inhibit BR responsive signaling under stress conditions (Chung et al., 2014). BES1 and RD26 share their target genes, however one is an inducer and another is a repressor or vice versa. These two transcription factors are known to bind to E-Box element and BR-response element (BRRE) respectively. Both BES1 and RD26 were experimentally validated to be the interacting partner and together bind on to the DNA elements in an antagonistic fashion, thus neutralizing the gene regulation under normal plant growth conditions (Ye et al., 2017). While under stress conditions the expression of RD26 increases this result in increased expression of BR-repressed genes and reduced expression of
PLANT SIGNALING MOLECULES
26.6 BR MEDIATED DEFENSE SIGNALING
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FIGURE 26.3 Antagonistic regulation of RD26 and BES1 during drought stress.RD26 and BES1 are known to compete with each other for binding to BR-responsive gene promoters. When plants experience drought stress, the expression of RD26 is elevated and this inhibits binding of BES1 to BR-responsive genes thus inhibiting their expression. (See Section 26.5 for details.)
BES1 targeted or BR-induced growth related genes. Extensive gene expression analysis of BR-responsive genes and RD26 target gene under drought stress conditions (with external application of ABA) indicated that RD26, BES1 and their target genes fluctuate in terms of expression to mitigate changing environmental conditions and sustain the plant growth (Fujita et al., 2004 ) (Fig. 26.3).
26.6 BR MEDIATED DEFENSE SIGNALING The relationship of BR signaling and plant defense is similar to that of the BR signaling- drought crosstalk (Lozano-Dura´n and Zipfel, 2015). Plants need to utilize their resources carefully under stress conditions and this sometimes leads to a temporary inhibition of the growth and development while making the plant ready to tolerate the stress. As many BR responsive genes are involved in regulating plant growth and development, they are the first target to be suppressed to reduce the resource utilization and hence the crosstalk between BR-signaling genes and defense related genes needs to be established. Studies on the influence of BR signaling and defense indicated that PAMP triggered immunity or PTI in plants is somehow influenced by BR-receptors or BR-responsive genes. PTI is a defense mechanism in plants, which recognizes the pathogen associated molecular patterns (PAMPs) and activates the downstream defense signaling cascade. PAMPs are the chemical signature moiety derived from the pathogens and recognized by specific receptors present on the plasma membrane. Two main components of the BR signaling cascade, namely BAK1
and BRI1, have been shown to play an important role in PTI (Albrecht et al., 2012; Goddard et al., 2014). BAK1, a coreceptor for BR, also serves as coreceptor for bacterial PAMPs. It has been proved that bacterial flagellin (a PAMP) binds to its receptor FLAGELLIN SENSING 2 (FLS2) together with coreceptor BAK1 and hence it is proposed that bacterial PAMPs and BR compete with each other for BAK1 (Chinchilla et al., 2007). So in the case when the PTI is activated, the BR pathway is inhibited up to a certain extent and vice versa. Although several studies proposed different hypothesis for the mechanism of BAK1 action in PTI, the conclusion remains the same (Albrecht et al., 2012; Belkhadir et al., 2014). PTI in plants activates the ROS signaling, which leads to an oxidative burst in the cell, resulting in several defense related phenotypes like stomatal movement and callose deposition on the cell wall (Ingle et al., 2006; Nu¨rnberger et al., 2004). An elevated BR signaling has been shown to reduce the oxidative burst in the plant cell and made plants more susceptible to the pathogen. For example, the overexpression of a BR biosynthetic gene has been shown to limit the plant’s response against a bacterial PAMP, flg22 (Belkhadir et al., 2012). Moreover, the plants overexpressing BRI1 (BR receptor) resulted in similar phenotype indicating the antagonistic relationship between PTI and BR-signaling. A list of different experiments carried out to understand the effect of manipulation of BR-signaling genes on plants’ pathogen defense has been summarized in Table 26.2 (also reviewed by Nolan et al., 2017). Another protein, BSK1, involved in BR-signaling, also plays a direct role in PTI via its interaction with FLS2 and positively regulates ROS production in the cell (Shi et al., 2013a,b). Two other members of BR-signaling related genes,
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412 TABLE 26.2
26. BRASSINOSTEROID SIGNALING IN PLANTS
Effect of Genetic Manipulation of BR-Signaling Genes on Disease Susceptibility
Host
Pathogen/PAMP
Genetic manipulation
Phenotype
References
Arabidopsis thaliana
flg22, elf19
BRI1 Overexprssion
Suppression of PTI, reduced ROS production
Belkhadir et al. (2012)
Arabidopsis thaliana
Pseudomonas syringae pv. tomatoDC3000
bik1 mutant
Enhanced Susceptibility
Lu et al. (2010)
Arabidopsis thaliana
flg22
bin2
Suppression of PTI, reduced ROS production
Lozano-Dura´n et al. (2013)
Arabidopsis thaliana
Thrips tabaci
bzr1-D mutant
Enhanced tolerance
Miyaji et al. (2014)
Arabidopsis thaliana
Pseudomonas syringae pv. tomatoDC3000
JUB1 Overexpression
Enhanced susceptibility
Shahnejat-Bushehri et al. (2016)
Arabidopsis thaliana
Pseudomonas syringae pv. tomatoDC3000
bes1 mutant
Enhanced susceptibility
Kang et al. (2015)
Hordeum vulgare
Fusarium culmorum
BRI1 mutation in kinase domain
Enhanced tolerance
Ali et al. (2014)
Brassica napus
Sclerotinia sclerotiorum, Leptosphaeria maculans
AtDWF4 Overexpression Enhanced tolerance
Sahni et al. (2016)
Brachypodium distachyon
Necrotrophic fungus
bri1 mutation
Goddard et al. (2014)
namely BIN2 and BZR1, were also reported to enhance tolerance against pathogen attack when inhibited or mutated (Lozano-Dura´n et al., 2013; Miyaji et al., 2014). Hence, providing supporting evidence for the hypothesis stating that the suppression of BR signaling decreases the susceptibility against pathogen attack. However this does not hold true for every experiment carried out and for different kinds of pathogen, indicating that the mechanism and interplay of BRsignaling is complex and the response might vary according to experimental setup. A study on BES1 is one such example where the mutants were shown to behave differently for a fungal and a bacterial pathogen. BES1 was shown to be a potential candidate connecting the MAPK (mitogen-activated protein kinase) signaling pathway of plant defense to BR-signaling (Kang et al., 2015). Another example comes from Brassica napus, where the overexpression of a BR biosynthetic gene, AtDWF4, leads to enhance disease tolerance against fungal pathogens. While plants from Belkhadir et al. (2012), where bacterial PAMP were used, displayed compromised tolerance.
26.7 BR MEDIATED ROS SIGNALING AND ITS ROLE IN PLANT DEFENSE ROS are often considered as major determinant of stress and serve as a key player in various signaling pathways in plant cells, entailing in photosynthetic
Enhanced tolerance
regulation, perception of abiotic or pathogen response and hormonal action, programmed cell death (PCD), and other important growth and developmental pathways (Dat et al., 2000; Mittler, 2002; Mullineaux and Karpinski, 2002; Apel and Hirt, 2004; Khan and Khan, 2017). ROS consist of free radicals corresponding to superoxide ( O22) and hydroxyl radicals ( OH), and nonfree radicals such as hydrogen peroxide (H2O2) 1 and singlet oxygen ( O2). In plants, ROS are mainly generated during the process of respiration, photosynthesis, and N2 fixation in the chloroplast, mitochondria, peroxisome, cytosol, plasma membrane, and the apoplastic space. Furthermore, generation of ROS in cell wall bound peroxidases takes place in the apoplastic space. While, in the plasma membrane, an NADPH oxidase complex functions as the ROSproducing system (Bolwell, 1999). Suzuki and Mittler (2006) interpreted that ROS, like superoxide (.O2-), are produced by NADPH oxidases during stress and trigger the downstream stress-response pathways and thereby induce several underlying defense pathways. Besides this, ROS lead to oxidative burst by initiating membrane depolarization and influx of calcium ions inside the cell, which evoke several pathways required for combating both biotic and abiotic stresses. This includes defense related pathways, production of antioxidant enzymes, dehydrins and heat shock proteins, synthesis of pathogenesis-related proteins (Gechev et al., 2006), MAPKs signaling (Apel and Hirt, 2004), etc.
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REFERENCES
H2O2 is one of the most stable ROS having the ability to behave both as an oxidant and as a reductant (Salin, 1991). Being a strong oxidant it may trigger localized oxidative damage leading to disruption of vital metabolic function and can also diffuse. Conversely, to mediate ROS signaling, H2O2 plays multiple roles by behaving as a signal, a mediator, and an effector molecule (Levine et al., 1994) and was found to accumulate in response to both biotic and abiotic stresses. Additionally, to reinforce the cell wall, H2O2 is utilized by apoplastic peroxidases that catalyze the cross-linking between and polysaccharides and cell wall extension, hampering the pathogen penetration (Passardi et al., 2004). Moreover, being as a secondary messenger in intracellular signaling pathways, it induces expression of genes involved in pathogen response and chilling acclimation (Chen et al., 1993; Prasad et al., 1994). It is also identified as one of the earliest factors involved in the transcriptional activation of defense related genes in Birch (Pellinen et al., 2002). Owing to stresses, sudden and transient increase of H2O2 is considered as a general alarm signal for subsequent eliciting the durable form of defenses that are helpful in facilitating protection against all these stresses (Mittler and Berkowitz, 2001). Additionally, H2O2 may also contribute in induction of systemic acquired acclimation (SAA), which is raised due to exposure of one part of the plant to high light that renders the unexposed parts resilient to high light (Karpinski et al., 1999). BR-induced H2O2 accumulation is caused by increased activity of NADPH oxidase as confirmed by measuring the activity of plasma membrane NADPH oxidase in plants treated with 24epibrassinolide (EBR), which is a bioactive brassinosteroid derivative (Xia et al., 2009). Additionally, EBR was also shown to be effective in restoring the NADPH oxidase activity of brassinazole (BRZ, a specific inhibitor of BR biosynthesis) treated plants. Similarly exogenously applied H2O2 showed a similar pattern to that of EBR (Deng et al., 2016). Studies suggest that apart from BAK1 (for BRI1-associated receptor kinase 1), BIN2 (a GSK3/SHAGGY-like kinase), BSU1 (for BRI1 suppressor 1, a phosphatase) and, three other regulatory genes, RBOH (respiratory burst oxidase homolog), MAPK1 (mitogen-activated protein kinases), and MAPK3, were upregulated upon treatment with EBR but downregulated after BRZ treatment emphasizing their vital role (Xia et al., 2009). Exogenous application of BR on the leaves of Niotiana benthamiana were shown to enhance the plant tolerance against several different pathogens (Nakashita et al., 2003). This is accompanied by accumulation of BR-induced MAPK and RBOHB (an NADPH oxidase B) genes and subsequent ROS burst. Eventually, the end products of the target genes directly take part into
the cellular protection. Nevertheless, further studies are warranted to provide genetic evidence for NADPH oxidase’s role in BR-induced ROS generation (Deng et al., 2016). This would pave the way to unveil the critical signaling components in BR signal perception and downstream stress responses, and to elucidate the molecular mechanisms involved in the crosstalk between BR and other hormones.
26.8 CONCLUSION Elucidation of BR signaling pathways is still a challenging task for scientists worldwide. Its multifaceted nature and crosstalk with different growth and developmental pathways in plants make it a complex system to study. As far as stress signaling and BR crosstalk is concerned, a clear role of BR has been established. However, the availability of different model systems and different experimental approaches make it more complicated to untangle the exact pathway. The role of BR signaling in both biotic and abiotic stresses seems to be connected with ROS signaling and potential of an extensive crosstalk between two pathways can be visualized but the BR signaling research is still in its juvenile phase and many more factors are needed to be uncovered to have a clear view of this complex machinery in the plant cell.
References Albrecht, C., Boutrot, F., Segonzac, C., Schwessinger, B., GimenezIbanez, S., Chinchilla, D., et al., 2012. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signalling independent of the receptor kinase BAK1. Proc. Natl Acad. Sci. U.S.A. 109, 303 308. Ali, S.S., Gunupuru, L.R., Kumar, G.B.S., Khan, M., Scofield, S., Nicholson, P., et al., 2014. Plant disease resistance is augmented in uzu barley lines modified in the brassinosteroid receptor BRI1. BMC Plant Biol. 14, 227. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373 399. Ashraf, M., Akram, N.A., Arteca, R.N., Foolad, M.R., 2010. The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Crit Rev. Plant Sci. 29, 162 190. Bajguz, A., 2007. Metabolism of brassinosteroids in plants. Plant Physiol Biochem. 45, 95 107. Bajguz, A., Hayat, S., 2009. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem. 47, 1 8. Belkhadir, Y., Jaillais, Y., Epple, P., Balsemao-Pires, E., Dangl, J.L., Chory, J., 2012. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc. Natl Acad. Sci. U.S.A. 109, 297 302. Belkhadir, Y., Yang, L., Hetzel, J., Dangl, J.L., Chory, J., 2014. The growth-defence pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem. Sci. 39, 447 456.
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Bishop, G.J., Yokota, T., 2001. Plants steroid hormones, brassinosteroids: current highlights of molecular aspects on their synthesis/ metabolism, transport, perception and response. Plant Cell Physiol. 42, 114 120. Bolwell, G.P., 1999. Role of reactive oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol. 2, 287 294. Cano-Delgado, A., Yin, Y., Yu, C., Vafeados, D., Mora-Garcia, S., Cheng, J.C., et al., 2004. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341 5351. Chen, Z., Silva, H., Klessig, D.F., 1993. Chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6, 65 74. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nu¨rnberger, T., Jones, J.D.G., et al., 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497 500. Choudhary, S.P., Yu, J.Q., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.P., 2012. Benefits of brassinosteroid crosstalk. Trends in Plant Sci. 17 (10), 594 605. Chung, Y., Kwon, S.I., Choe, S., 2014. Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol. Cells 37, 795 803. Claeys, H., Inze, D., 2013. The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol. 162, 1768 1779. Clouse, S.D., 2011. Brassinosteroids. The Arabidopsis Book 011 (9), e0151. Clouse, S.D., Langford, M., McMorris, T.C., 1996. A brassinosteroidinsensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111, 671 678. Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inze, D., Van Breusegem, F., 2000. Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57, 779 795. de Lucas, M., Prat, S., 2014. PIFs get BR right: phytochrome interacting factors as integrators of light and hormonal signals. New Phytol. 202, 1126 1141. Deng, X.G., Zhu, T., Zou, L.J., Han, X.Y., Zhou, X., Xi, D.H., et al., 2016. Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid-mediated systemic virus resistance in Nicotiana benthamiana. The Plant Journal 85, 478 493. Espinosa-Ruiz, A., Martı´nez, C., de Lucas, M., Fa`bregas, N., Bosch, N., Can˜o-Delgado, A.I., et al., 2017. TOPLESS mediates brassinosteroid control of shoot boundaries and root meristem development in Arabidopsis thaliana. Development 144, 1619 1628. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., OhmeTakagi, M., et al., 2004. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signalling pathway. Plant J. 39, 863 876. Gampala, S.S., Kim, T.-W., He, J.-X., Tang, W., Deng, Z., Bai, M.-Y., et al., 2007. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13, 177 189. Gechev, T.S., Van Breusegem, F., Stone, J.M., Denev, I., Laloi, C., 2006. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28 (11), 1091 1101. Goddard, R., Peraldi, A., Ridout, C., Nicholson, P., 2014. Enhanced disease resistance caused by BRI1 mutation is conserved between Brachypodium distachyon and barley (Hordeum vulgare). Mol. Plant Microbe Interact. 27, 1095 1106. Grove, M.D., Spencer, G.F., Rohwedder, W.K., Mandava, N., Worley, J.F., Warthen, J.D., et al., 1979. Brassinolide, a plant growth promoting steroid isolated from Brassica napus pollen. Nature 281, 216 217. Hecht, V., Vielle-Calzada, J.P., Hartog, M.V., Schmidt, E.D., Boutilier, K., Grossniklaus, U., et al., 2001. The Arabidopsis SOMATIC
EMBRYOGENESIS RECEPTOR KINASE 1gene is expressed in developing ovules and embryos and enhancesembryogenic competence in culture. Plant Physiol. 127, 803 816. Ingle, R.A., Carstens, M., Denby, K.J., 2006. PAMP recognition and the plant pathogen arms race. Bioessays 28, 880 889. Kadota, Y., Shirasu, K., Zipfel, C., 2015. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol. 56 (8), 1472 1480. Kang, S., Yang, F., Li, L., Chen, H., Chen, S., Zhang, J., 2015. The Arabidopsis transcription factor BRASSINOSTEROID INSENSITIVE 1-ETHYL METHANESULFONATE-SUPPRESSOR 1 is a direct substrate of MITOGEN-ACTIVATED PROTEIN KINASE 6 and regulates immunity. Plant Physiol. 167, 1076 1086. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., Mullineaux, P., 1999. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654 657. Khan, M.I.R., Khan, N., 2017. Reactive Oxygen Species and Antioxidant System in Plants: Role and Regulation Under Abiotic Stress. Springer Nature 978-981-10-5254-5. Kim, T.-W., Guan, S., Sun, Y., Deng, Z., Tang, W., Shang, J.-X., et al., 2009. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11, 1254 1260. Kim, T.-W., Guan, S., Burlingame, A.L., Wang, Z.-Y., 2011. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43, 561 571. Krishna, P., 2003. Brassinosteroid-mediated stress responses. J. Plant Growth Regul. 22, 289 297. Kutschera, U., Wang, Z.Y., 2012. Brassinosteroid action in flowering plants: a Darwinian perspective. J. Exp. Bot. 63, 3511 3522. Levine, A., Tenhaken, R., Dixon, R., Lamb, C., 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583 593. Li, J., 2010. Regulation of the nuclear activities of brassinosteroid signalling. Curr. Opin. Plant Biol. 13, 540 547. Li, J., Chory, J., 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929 938. Li, L., Yu, X., Thompson, A., Guo, M., Yoshida, S., Asami, T., et al., 2009. Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J. 58 (2), 275 286. Lorenzo, O., Solano, R., 2005. Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8, 532 540. Lozano-Dura´n, R., Zipfel, C., 2015. Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci. 20, 12 19. Lozano-Dura´n, R., Macho, A.P., Boutrot, F., Segonzac, C., Somssich, I.E., Zipfel, C., 2013. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2, e00983. Lu, D., Wu, S., Gao, X., Zhang, Y., Shan, L., He, P., 2010. A receptorlike cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl Acad. Sci. U.S.A. 107, 496 501. Mauch-Mani, B., Mauch, F., 2005. The role of abscisic acid in plant pathogen interactions. Curr. Opin. Plant Biol. 8, 409 414. Mitchell, J., Mandava, N., Worley, J., Plimmer, J., Smith, M., 1970. Brassins-a new family of plant hormones from rape pollen. Nature 225, 1065 1066. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405 410. Mittler, R., Berkowitz, B., 2001. Hydrogen peroxide, a messenger with too many roles? Redox Rep. 6, 69 72.
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REFERENCES
Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V.B., Vandepoele, K., et al., 2011. ROS signalling: the new wave? Trends Plant Sci. 16, 300 910. Miyaji, T., Yamagami, A., Kume, N., Sakuta, M., Osada, H., Asami, T., et al., 2014. Brassinosteroid-related transcription factor BIL1/BZR1 increases plant resistance to insect feeding. Biosci. Biotechnol. Biochem. 78, 960 968. Mullineaux, P., Karpinski, S., 2002. Signal transduction in response to excess light: getting out of the chloroplast. Curr. Opin. Plant Biol. 5, 43 48. Nakashita, H., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., et al., 2003. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33, 887 898. Nam, K.H., Li, J., 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signalling. Cell 110, 203 212. Nolan, T.M., Brennan, B., Yang, M., Chen, J., Zhang, M., Li, Z., et al., 2017. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev. Cell 41, 33 46. Nu¨rnberger, T., Brunner, F., Kemmerling, B., Piater, L., 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249 266. Oh, E., Zhu, J.-Y., Wang, Z.-Y., 2012. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802 809. Passardi, F., Penel, C., Dunand, C., 2004. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci. 9 (11), 534 540. Pellinen, R.I., Korhonen, M.-S., Tauriainen, A.A., Palva, T., Kangasja¨rvi, J., 2002. Hydrogen peroxide activates cell death and defence gene expression in birch. Plant Physiol. 130, 549 560. Prasad, T.K., Anderson, M.D., Stewart, C.R., 1994. Acclimation, Hydrogen peroxide, and Abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol. 105, 619 627. Ryu, H., Kim, K., Cho, H., Park, J., Choe, S., Hwang, I., 2007. Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signalling. Plant Cell 19, 2749 2762. Sahni, S., Prasad, B.D., Liu, Q., Grbic, V., Sharpe, A., Singh, S.P., et al., 2016. Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Sci. Rep. 6, 28298. Salin, M.L., 1991. Chloroplast and mitochondrial mechanisms for protection against oxygen toxicity. Free Rad. Res. Commun. 12, 851 858. Sewelam, N., Kazan, K., Schenk, P.M., 2016. Global plant stress signalling: reactive oxygen species at the cross-road. Front. Plant Sci. Shahnejat-Bushehri, S., Nobmann, B., Devi Allu, A., Balazadeh, S., 2016. JUB1 suppresses Pseudomonas syringae-induced defence responses through accumulation of DELLA proteins. Plant Signal. Behav. 11, e1181245. Shi, H., Shen, Q., Qi, Y., Yan, H., Nie, H., Chen, Y., et al., 2013a. BRSIGNALLING KINASE 1 physically associates with FLAGELLIN SENSING 2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25, 1143 1157. Shi, H., Yan, H., Li, J., Tang, D., 2013b. BSK1, a receptor-like cytoplasmic kinase, involved in both BR signalling and innate immunity in Arabidopsis. Plant Signal. Behav. 8, e24996. Sun, Y., Fan, X.-Y., Cao, D.-M., Tang, W., He, K., Zhu, J.-Y., et al., 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 765 777. Suzuki, N., Mittler, R., 2006. Reactive oxygen species and temperature stresses: a delicate balance between signalling and destruction. Physiol Plant. 126, 45.
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Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., Mittler, R., 2011. Respiratory burst oxidases: the engines of ROS signalling. Curr. Opin. Plant Biol. 14 (6), 691 699. Takatsuto, S., 1994. Brassinosteroids: distribution in plants, bioassays and microanalysts by gas chromatography mass spectrometry. J Chromatogr. A 658, 3 15. Tang, J., Han, Z., Chai, J., 2016. Q&A: what are brassinosteroids and how do they act in plants? BMC biology 14, 113. Tang, W., Kim, T.-W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., et al., 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557 560. Teale, W.D., Ditengou, F.A., Dovzhenko, A.D., Li, X., Molendijk, A.M., Ruperti, B., et al., 2008. Auxin as a model for the integration of hormonal signalprocessing and transduction. Mol. Plant 1, 229 237. Tran, L.S.P., Nakashima, K., Sakuma, Y., Simpson, S.D., Fujita, Y., Maruyama, K., et al., 2004. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16, 2481 2498. Vilarrasa-Blasi, J., Gonza´lez-Garcı´a, M.-P., Frigola, D., Fa´bregas, N., Alexiou, K.G., Lo´pez-Bigas, N., et al., 2014. Regulation of plant stem cell quiescence by a brassinosteroid signalling module. Dev. Cell 30, 36 47. Wang, H., Zhu, Y., Fujioka, S., Asami, T., Li, J., Li, J., 2009. Regulation of Arabidopsis brassinosteroid signalling by atypical basic helix-loop-helix proteins. Plant Cell 21, 3781 3791. Wang, X., Chory, J., 2006. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signalling, from the plasma membrane. Science 313, 1118 1122. Wang, X., Goshe, M.B., Soderblom, E.J., Phinney, B.S., Kuchar, J.A., Li, J., et al., 2005. Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROIDINSENSITIVE1 receptor kinase. Plant Cell 17, 1685 1703. Wang, Z.-Y., Bai, M.-Y., Oh, E., Zhu, J.-Y., 2012. Brassinosteroid signalling network and regulation of photomorphogenesis. Ann. Rev. Genet. 46, 701 724. Wei, Z., Li, J., 2016. Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant. 9, 86 100. Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., et al., 2009. Reactive oxygen species are involved in brassinosteroids induced stress tolerance in Cucumis sativus. Plant Physiol. 150, 801 814. Ye, H., Liu, S., Tang, B., Chen, J., Xie, Z., Nolan, T.M., et al., 2017. RD26 mediates crosstalk between drought and brassinosteroidsignalling pathways. Nat. Commun. 8, 14573. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., Chory, J., 2005. A new class of transcription factors mediates brassinosteroidregulated gene expression in Arabidopsis. Cell 120 (2), 249 259. Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., et al., 2011. A brassinosteroid transcriptional network revealed by genomewide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634 646. Zhang, L.-Y., Bai, M.-Y., Wu, J., Zhu, J.-Y., Wang, H., Zhang, Z., et al., 2009. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21, 3767 3780. Zhao, B., Lv, M., Feng, Z., Campbell, T., Liscum, E., Li, J., 2016. TWISTED DWARF 1 associates with BRASSINOSTEROIDINSENSITIVE 1 to regulate early events of the brassinosteroid signalling pathway. Mol. Plant 9, 582 592. Zhu, J.-Y., Li, Y., Cao, D.-M., Yang, H., Oh, E., Bi, Y., et al., 2017. The F-box protein KIB1 mediates brassinosteroid-induced inactivation and degradation of GSK3-like kinases in Arabidopsis. Mol. Cell 66, 648 657.
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Further Reading He, J.-X., Gendron, J.M., Yang, Y., Li, J., Wang, Z.-Y., 2002. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signalling pathway in Arabidopsis. Proc. Natl Acad. Sci. U.S.A. 99, 10185 10190. Lin, F., Ding, H.D., Wang, J.X., Zhang, H., Zhang, A.Y., Zhang, Y., et al., 2009. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot. 60, 3221 3238. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F., 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490 498.
Xia, X.-J., Gao, C.-J., Song, L.-X., Zhou, Y.-H., Shi, K., Yu, J.-Q., 2014. Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ. 37, 2036 2050. Zhang, A.Y., Jiang, M.Y., Zhang, J.H., Tan, M.P., Hu, X.L., 2006. Mitogenactivatedprotein kinase is involved in abscisic acidinduced antioxidant defence and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol. 141, 475 487. Zhou, J., Wang, J., Li, X., Xia, X.-J., Zhou, Y.-H., Shi, K., et al., 2014. H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J. Exp. Bot. 65, 4371 4383.
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26 Brassinosteroid Signaling and Complex Interplay of ROS, NADPH Oxidase, and MAPK Mediated Biotic and Abiotic Stress Acclimation in Plants Deepesh Bhatt1, , Mayank Sharma2,, Manoj Nath3, Megha D. Bhatt4 and Saurabh Badoni5 1
Department of Biotechnology, Shree Ramkrishna Institute of Computer Education and Applied Sciences, Veer Narmad South Gujarat University, Surat, Gujarat, India 2Martin Luther University of Halle-Wittenberg, Halle, Germany 3 Indian Council of Agricultural Research, New Delhi, Uttar Pradesh, India 4GSFC AgroTech Ltd. Gujarat State Fertilizers & Chemicals Ltd., Vadodara, India 5Plant Breeding Division, International Rice Research Institute, Metro Manila, Philippines
O U T L I N E 26.1 Introduction
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26.6 BR Mediated Defense Signaling
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26.2 Brassinosteroids
408
26.3 Brassinosteroid Signaling in Plants
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26.7 BR Mediated ROS Signaling and Its Role in Plant Defense
412
26.8 Conclusion
413
26.4 Transcription Factors Involved in BR Signaling
409
References
413
26.5 Role of RD26 in BR Signaling
410
Further Reading
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26.1 INTRODUCTION Plants are constantly exposed to multiple biotic and abiotic stresses during their entire life, which include pathogen attacks and insect herbivory, high or low
temperatures stress, drought and salinity stress, etc. Therefore, to survive, plants have evolved a range of intricate signaling mechanisms thus adapting towards these fluctuating environments. Plant growth regulators, also termed as phytohormones, are increasingly
The authors (Deepesh Bhatt and Mayank Sharma) contributed equally to this work.
Plant Signaling Molecules. DOI: https://doi.org/10.1016/B978-0-12-816451-8.00025-3
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© 2019 Elsevier Inc. All rights reserved.
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26. BRASSINOSTEROID SIGNALING IN PLANTS
recognized to play vital roles in plant stress adaptations. Several studies indicated that biological processes in plants are influenced by stressful conditions, which are regulated through different hormonal signaling pathways in plants (Teale et al., 2008). Phytohormones, like salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA), are primary signals that regulate responses to mitigate biotic and abiotic stresses in plants (Lorenzo and Solano, 2005; Mauch-Mani and Mauch, 2005). These stresses, if not properly regulated, may further lead to the generation of a key intermediate termed as reactive oxygen species (ROS). ROS are generated in response to stress as well as to regulate normal metabolic processes as a signaling agent (Mittler et al., 2011; Sewelam et al., 2016). Additionally, respiratory burst oxidase homologs (RBOHs) and NADPH oxidases are also known to be major components of ROS production system in plants (Suzuki et al., 2011; Kadota et al., 2015). Furthermore several other studies also propose that ROS plays a critical role in enhancing stress tolerance by activating mitogenactivated protein kinases (MAPKs), antioxidant enzymes, and other related transcription factors (Gechev et al., 2006). The generation of ROS has been shown to be a key process that is shared among many transcriptional pathways related to stress signaling. Thus at the molecular level, the perception of external stimuli results in the subsequent activation of stress signaling through some intermediate signal molecules. Brassinosteroids are a group of steroidal hormones and play a major role in various developmental pathways and are involved in stress response (Choudhary et al., 2012). Here in this chapter we will mainly emphasize how brassinosteroids are able to influence and regulate concomitant generation of ROS, NADPH oxidase, and MAPK, which act as intermediate components in the signaling cascade to regulate biotic and abiotic stress acclimation in plants.
26.2 BRASSINOSTEROIDS Mitchell and coworkers explored a sixth class of plant hormones named brassinosteroids (BRs) in 1970 (Mitchell et al., 1970). BR was first isolated from the pollen of Brassica napus. BRs are polyhydroxysteroids similar to steroid hormones from animals (Clouse, 2011). Furthermore they play an important role in regulating various aspects of plant growth and development (Wei and Li, 2016). This includes cell division and elongation, tissue morphogenesis, plant defense, seed germination, and reproduction (Krishna, 2003; Ashraf et al., 2010). They also play a direct or indirect role in stress signaling in plants (Bajguz and Hayat, 2009). Approximately 70 different kinds of analogue of BRs have been identified to date from various plant species and tissue samples. Brassinolide has
FIGURE 26.1 Chemical structure of the most active brassinosteroid ‘brassinolide’ C28H48O6 (Image from PubChem) and its phytochemical compounds tree.
been reported as a most active BR identifies hitherto (Grove et al., 1979, Tang et al., 2016) (Fig. 26.1). BRs are continuously biosynthesized, mostly in pollens, immature seeds, roots, and flower (Takatsuto, 1994; Kutschera and Wang, 2012). Excess of BRs can be metabolized by plants via different chemical reactions to render them into inactive form. However, they can be converted into the active form whenever needed to maintain the BR homeostasis (Bishop and Yokota, 2001; Bajguz, 2007). Plant cell consists of various receptors for BRs, which recognize them and stimulate the downstream signaling processes. Characterization of BR-insensitive (bri1) mutants led to the discovery of the first BR receptor in Arabidopsis thaliana (Clouse et al., 1996). BRI1 encodes a leucine-rich repeat-receptor like kinase (LRR-RLK) composing of an intracellular kinase domain and extracellular LRR domain (Li and Chory, 1997). The bri1 mutants were shown to be male sterile with several developmental and tissue deformities. Three BRI1 homologs namely BRL1, BRL2, and BRL3 (BRI1 like 1, 2, and 3) were also reported to recognize BRs in Arabidopsis (Cano-Delgado et al., 2004), though they display a weak phenotype in respective knockout plants when compared with BRI1. A further molecular dissection, by two different scientific groups, contributed in identification of interacting partners of BRI1 named BRI1 associated kinase 1 (BAK1) or somatic embryogenesis receptor-like kinase (SERK3) (Hecht et al., 2001; Nam and Li, 2002). BAK1 interacts with BRI1 to persuade the BR signaling. The SERK family of proteins with five members seems to play an important role in BR signaling. SERK1 and SERK4 have a similar role as of BAK1/SERK3 in BR signaling. Just to avoid confusion it should be noted that BAK1 and SERK3 were discovered and named separately, however later on it came out that BAK1 and SERK3 are the same protein.
26.3 BRASSINOSTEROID SIGNALING IN PLANTS BR signaling is a phosphorylation and dephosphorylation relay system among BR receptors, coreceptors,
PLANT SIGNALING MOLECULES
26.4 TRANSCRIPTION FACTORS INVOLVED IN BR SIGNALING
and downstream transcription factors. In absence of BR, a BRI1-KINASE INHIBITOR 1 (BKI1) remains bound to BRI1 (Wang et al., 2005; Wang and Chory, 2006). The binding of BR to BRI1 and coreceptor BAK1 releases BKI1 and makes it available for 14-3-3 proteins that phosphorylate it and thus inhibit its binding to BRI1 (Gampala et al., 2007). Furthermore the mutual phosphorylation of BRI1 and BAK1 leads to activation of downstream signaling. The activation of BRI1 and BAK1 also requires the TWISTED DWARF 1 (TWD1/ FKBP42) protein (Zhao et al., 2016). An activated BRI1 phosphorylates the downstream signaling proteins namely BR-SIGNALING KINASE (BSK1) and CONSTITUTIVE DIFFERENTIAL GROWTH 1 (CDG1) kinase (Tang et al., 2008; Kim et al., 2009, 2011; Sreeramulu et al., 2013). After phosphorylation, this in turn leads to the activation of BRI1-SUPPRESSOR 1 (BSU1). BSU1 is a PP1-type phosphatase (Kim et al., 2011). The activation of BRI1 and BAK1 also requires the TWISTED DWARF 1 (TWD1/FKBP42) protein. The BSU1 further dephosphorylates and inactivates BRASSINOSTEROID INSENSITIVE 2 (BIN2). BIN2 is a G11SK3-like kinase and proposed to be degraded via its ubiquitinylation by a ubiquitin ligase KINK SUPPRESSED IN BZR1-1D (KIB1) (Zhu et al., 2017). Another protein, BES1/BZR1 (BRI1 EMS SUPPRESSOR
409
1/BRASSINAZOLE RESISTANT 1), a BR responsive transcription factor, plays a key role in activation of BRinduced genes. In absence of BR, the BIN2 phosphorylates BES1/BZR1 leading to its inactivation. But in the presence of BR, BIN2 is degraded and PROTEIN PHOSPHATASE 2A (PP2A) dephosphorylates BES1/ BZR1 (He et al., 2001). The BES1/BZR1 later enters in the nucleus, binds to DNA and activates the BR-induced genes with the help of some additional transcription factors (Ryu et al., 2007). For a schematic view, refer to Fig. 26.2A B.
26.4 TRANSCRIPTION FACTORS INVOLVED IN BR SIGNALING Genome-wide analysis of genes regulated by BES1/ BZR1 revealed that the expression of several thousand genes is influenced in BR signaling (Yu et al., 2011; Sun et al., 2010). The downstream BR signaling genes are either directly or indirectly regulated by BES1/BZR1. Several BES1/BZR1 interacting proteins and transcription factors have been identified so far. The complex interplay with these transcription factors in turn regulates the expression of BR signaling genes (Li, 2010). This include PHYTOCHROME-INTERACTING FACTORS
FIGURE 26.2 (A) A schematic view of BR-signaling in plant cell. A BR-regulated transcription factor BES1/BZR1 is the main player in BRsignaling. In absence of BR, it remains phosphorylated and cannot bind to BR responsive gene in the nucleus. 14-3-3 protein sequesters BES1/ BZR1 and keeps it phosphorylated. (See Section 26.3 for details.) (B) A schematic view of BR-signaling in plant cell. When BR is available and binds to BR receptors and coreceptors, this phosphorylates several interacting proteins. A protein, BKI1, when phosphorylated, sequesters 143-3 protein thus keeping BES1/BZR1 free. PP2A dephosphorylates BES1/BZR1 and later it enters in the nucleus to activates the BR responsive genes. (See Section 26.3 for details.) Source: Model adapted from Nolan, T.M., Brennan, B., Yang, M., Chen, J., Zhang, M., Li, Z., et al., 2017. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev. Cell 41, 33 46.
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410 TABLE 26.1 Stability
26. BRASSINOSTEROID SIGNALING IN PLANTS
List of Proteins That Directly Bind to BES1 and or BZR1 and Regulate BR Responsive Gene Expression or Protein Binding partner
Gene name
Molecular activity
PIFs (PHYTOCHROME-INTERACTING FACTORS)
Regulation of BR responsive genes
BES1/BZR1 De Lucas and Prat (2014)
ARF6/8 (AUXIN RESPONSIVE TRANSCRIPTION FACTORS)
Regulation of growth and defense related genes
PIF4 and BZR1
Oh et al. (2012)
MYB30
Regulation of BR responsive gene induction and ABA response
BES1
Li et al. (2009)
HAT1 (HOMEODOMAIN-LEUCINE ZIPPER PROTEIN 1)
Control of BR responsive genes
BES1
Li et al. (2009)
BRAVO(BRs AT VASCULAR AND ORGANIZING Regulation of cell division in quiescent center CENTER)
BES1
Vilarrasa-Blasi et al. (2014)
BIM1 (BES1-INTERACTING MYC-LIKE1)
Control of BR responsive genes
BES1
Yin et al. (2005)
TOPLESS and TOPLESS Related (TPR)
Antagonist of ABA signaling
BES1
Espinosa-Ruiz et al. (2017)
DSK2(DOMINANT SUPPRESSOR OF KAR2)
BES1 degradation during stress condition
BES1
Nolan et al. (2017)
(PIFs), BES1-INTERACTING MYC-LIKE1 (BIM1), the auxin responsive transcription factors (ARFs), ATBS1/ PRE (ACTIVATION-TAGGED bri1 SUPPRESSOR1/ PACLOBUTRAZOL-RESISTANCE), AIFs/IBH1 (ATBS1INTERACTING FACTORS/INCREASED LAMINA INCLINATION INTERACTING bHLH1) bHLH transcription factors, etc. (Wang et al., 2009; Zhang et al., 2009; de Lucas and Prat, 2014; Oh et al., 2012; Wang et al., 2012). PIFs are the transcription factors regulated by light and circadian clock. PIF4 has been validated to interact with BZR1 and forms a heterodimer, which together binds to the G-BOX (CACGTG) element present in the upstream promoter region of BR responsive genes. Similarly BIM1 interacts with BES1 and binds together with E-Box (CANNTG) element. The ARF6 and ARF8 also shown to interact with BZR1 and later on bind to ARF motif (TGTCTC) present in the promoter region of BR signaling genes. BZR1, PIFs, and ARFs together activate the downstream basic HELIX LOOP HELIX (bHLH) transcription factors including ATBS1/PRE family protein, which works as antagonist to AIFs/IBH1 proteins and activate proteins, which promotes the cell elongation. Similarly, a number of other transcription factors are involved in BR signaling that are directly regulated by BES1/BZR1. A list of such proteins is included in Table 26.1.
26.5 ROLE OF RD26 IN BR SIGNALING BR plays an important role in stress acclimation. Plants, being sessile in nature, try to reduce its growth
References
and development to expense the resources in stress management (Claeys and Inze, 2013). BES1 is known to be involved in reduction of plant growth under stress conditions especially when the drought stress is encountered. RESPONSIVE TO DESICCATION 26 (RD26) is a NAC transcription factor, which has been shown to play a crucial role in abiotic stress signaling in plants. The expression of RD26 gene is regulated by BES1. BES1 binds to the BRRE-binding site present in the promoter region of RD26 gene (Tran et al., 2004). BR response was found to be aberrated in plants overexpressing RD26 gene. The plants showed a strong phenotype of reduced growth and development. RD26 is induced under stress conditions thus providing a hint for RD26 as a connecting link between stress signaling and BR responses (Fujita et al., 2004). Genomewide analysis of these RD26OX plants revealed the antagonist expression of RD26 and BR-responsive genes. The output provided a hint that RD26 might inhibit BR responsive signaling under stress conditions (Chung et al., 2014). BES1 and RD26 share their target genes, however one is an inducer and another is a repressor or vice versa. These two transcription factors are known to bind to E-Box element and BR-response element (BRRE) respectively. Both BES1 and RD26 were experimentally validated to be the interacting partner and together bind on to the DNA elements in an antagonistic fashion, thus neutralizing the gene regulation under normal plant growth conditions (Ye et al., 2017). While under stress conditions the expression of RD26 increases this result in increased expression of BR-repressed genes and reduced expression of
PLANT SIGNALING MOLECULES
26.6 BR MEDIATED DEFENSE SIGNALING
411
FIGURE 26.3 Antagonistic regulation of RD26 and BES1 during drought stress.RD26 and BES1 are known to compete with each other for binding to BR-responsive gene promoters. When plants experience drought stress, the expression of RD26 is elevated and this inhibits binding of BES1 to BR-responsive genes thus inhibiting their expression. (See Section 26.5 for details.)
BES1 targeted or BR-induced growth related genes. Extensive gene expression analysis of BR-responsive genes and RD26 target gene under drought stress conditions (with external application of ABA) indicated that RD26, BES1 and their target genes fluctuate in terms of expression to mitigate changing environmental conditions and sustain the plant growth (Fujita et al., 2004 ) (Fig. 26.3).
26.6 BR MEDIATED DEFENSE SIGNALING The relationship of BR signaling and plant defense is similar to that of the BR signaling- drought crosstalk (Lozano-Dura´n and Zipfel, 2015). Plants need to utilize their resources carefully under stress conditions and this sometimes leads to a temporary inhibition of the growth and development while making the plant ready to tolerate the stress. As many BR responsive genes are involved in regulating plant growth and development, they are the first target to be suppressed to reduce the resource utilization and hence the crosstalk between BR-signaling genes and defense related genes needs to be established. Studies on the influence of BR signaling and defense indicated that PAMP triggered immunity or PTI in plants is somehow influenced by BR-receptors or BR-responsive genes. PTI is a defense mechanism in plants, which recognizes the pathogen associated molecular patterns (PAMPs) and activates the downstream defense signaling cascade. PAMPs are the chemical signature moiety derived from the pathogens and recognized by specific receptors present on the plasma membrane. Two main components of the BR signaling cascade, namely BAK1
and BRI1, have been shown to play an important role in PTI (Albrecht et al., 2012; Goddard et al., 2014). BAK1, a coreceptor for BR, also serves as coreceptor for bacterial PAMPs. It has been proved that bacterial flagellin (a PAMP) binds to its receptor FLAGELLIN SENSING 2 (FLS2) together with coreceptor BAK1 and hence it is proposed that bacterial PAMPs and BR compete with each other for BAK1 (Chinchilla et al., 2007). So in the case when the PTI is activated, the BR pathway is inhibited up to a certain extent and vice versa. Although several studies proposed different hypothesis for the mechanism of BAK1 action in PTI, the conclusion remains the same (Albrecht et al., 2012; Belkhadir et al., 2014). PTI in plants activates the ROS signaling, which leads to an oxidative burst in the cell, resulting in several defense related phenotypes like stomatal movement and callose deposition on the cell wall (Ingle et al., 2006; Nu¨rnberger et al., 2004). An elevated BR signaling has been shown to reduce the oxidative burst in the plant cell and made plants more susceptible to the pathogen. For example, the overexpression of a BR biosynthetic gene has been shown to limit the plant’s response against a bacterial PAMP, flg22 (Belkhadir et al., 2012). Moreover, the plants overexpressing BRI1 (BR receptor) resulted in similar phenotype indicating the antagonistic relationship between PTI and BR-signaling. A list of different experiments carried out to understand the effect of manipulation of BR-signaling genes on plants’ pathogen defense has been summarized in Table 26.2 (also reviewed by Nolan et al., 2017). Another protein, BSK1, involved in BR-signaling, also plays a direct role in PTI via its interaction with FLS2 and positively regulates ROS production in the cell (Shi et al., 2013a,b). Two other members of BR-signaling related genes,
PLANT SIGNALING MOLECULES
412 TABLE 26.2
26. BRASSINOSTEROID SIGNALING IN PLANTS
Effect of Genetic Manipulation of BR-Signaling Genes on Disease Susceptibility
Host
Pathogen/PAMP
Genetic manipulation
Phenotype
References
Arabidopsis thaliana
flg22, elf19
BRI1 Overexprssion
Suppression of PTI, reduced ROS production
Belkhadir et al. (2012)
Arabidopsis thaliana
Pseudomonas syringae pv. tomatoDC3000
bik1 mutant
Enhanced Susceptibility
Lu et al. (2010)
Arabidopsis thaliana
flg22
bin2
Suppression of PTI, reduced ROS production
Lozano-Dura´n et al. (2013)
Arabidopsis thaliana
Thrips tabaci
bzr1-D mutant
Enhanced tolerance
Miyaji et al. (2014)
Arabidopsis thaliana
Pseudomonas syringae pv. tomatoDC3000
JUB1 Overexpression
Enhanced susceptibility
Shahnejat-Bushehri et al. (2016)
Arabidopsis thaliana
Pseudomonas syringae pv. tomatoDC3000
bes1 mutant
Enhanced susceptibility
Kang et al. (2015)
Hordeum vulgare
Fusarium culmorum
BRI1 mutation in kinase domain
Enhanced tolerance
Ali et al. (2014)
Brassica napus
Sclerotinia sclerotiorum, Leptosphaeria maculans
AtDWF4 Overexpression Enhanced tolerance
Sahni et al. (2016)
Brachypodium distachyon
Necrotrophic fungus
bri1 mutation
Goddard et al. (2014)
namely BIN2 and BZR1, were also reported to enhance tolerance against pathogen attack when inhibited or mutated (Lozano-Dura´n et al., 2013; Miyaji et al., 2014). Hence, providing supporting evidence for the hypothesis stating that the suppression of BR signaling decreases the susceptibility against pathogen attack. However this does not hold true for every experiment carried out and for different kinds of pathogen, indicating that the mechanism and interplay of BRsignaling is complex and the response might vary according to experimental setup. A study on BES1 is one such example where the mutants were shown to behave differently for a fungal and a bacterial pathogen. BES1 was shown to be a potential candidate connecting the MAPK (mitogen-activated protein kinase) signaling pathway of plant defense to BR-signaling (Kang et al., 2015). Another example comes from Brassica napus, where the overexpression of a BR biosynthetic gene, AtDWF4, leads to enhance disease tolerance against fungal pathogens. While plants from Belkhadir et al. (2012), where bacterial PAMP were used, displayed compromised tolerance.
26.7 BR MEDIATED ROS SIGNALING AND ITS ROLE IN PLANT DEFENSE ROS are often considered as major determinant of stress and serve as a key player in various signaling pathways in plant cells, entailing in photosynthetic
Enhanced tolerance
regulation, perception of abiotic or pathogen response and hormonal action, programmed cell death (PCD), and other important growth and developmental pathways (Dat et al., 2000; Mittler, 2002; Mullineaux and Karpinski, 2002; Apel and Hirt, 2004; Khan and Khan, 2017). ROS consist of free radicals corresponding to superoxide ( O22) and hydroxyl radicals ( OH), and nonfree radicals such as hydrogen peroxide (H2O2) 1 and singlet oxygen ( O2). In plants, ROS are mainly generated during the process of respiration, photosynthesis, and N2 fixation in the chloroplast, mitochondria, peroxisome, cytosol, plasma membrane, and the apoplastic space. Furthermore, generation of ROS in cell wall bound peroxidases takes place in the apoplastic space. While, in the plasma membrane, an NADPH oxidase complex functions as the ROSproducing system (Bolwell, 1999). Suzuki and Mittler (2006) interpreted that ROS, like superoxide (.O2-), are produced by NADPH oxidases during stress and trigger the downstream stress-response pathways and thereby induce several underlying defense pathways. Besides this, ROS lead to oxidative burst by initiating membrane depolarization and influx of calcium ions inside the cell, which evoke several pathways required for combating both biotic and abiotic stresses. This includes defense related pathways, production of antioxidant enzymes, dehydrins and heat shock proteins, synthesis of pathogenesis-related proteins (Gechev et al., 2006), MAPKs signaling (Apel and Hirt, 2004), etc.
PLANT SIGNALING MOLECULES
413
REFERENCES
H2O2 is one of the most stable ROS having the ability to behave both as an oxidant and as a reductant (Salin, 1991). Being a strong oxidant it may trigger localized oxidative damage leading to disruption of vital metabolic function and can also diffuse. Conversely, to mediate ROS signaling, H2O2 plays multiple roles by behaving as a signal, a mediator, and an effector molecule (Levine et al., 1994) and was found to accumulate in response to both biotic and abiotic stresses. Additionally, to reinforce the cell wall, H2O2 is utilized by apoplastic peroxidases that catalyze the cross-linking between and polysaccharides and cell wall extension, hampering the pathogen penetration (Passardi et al., 2004). Moreover, being as a secondary messenger in intracellular signaling pathways, it induces expression of genes involved in pathogen response and chilling acclimation (Chen et al., 1993; Prasad et al., 1994). It is also identified as one of the earliest factors involved in the transcriptional activation of defense related genes in Birch (Pellinen et al., 2002). Owing to stresses, sudden and transient increase of H2O2 is considered as a general alarm signal for subsequent eliciting the durable form of defenses that are helpful in facilitating protection against all these stresses (Mittler and Berkowitz, 2001). Additionally, H2O2 may also contribute in induction of systemic acquired acclimation (SAA), which is raised due to exposure of one part of the plant to high light that renders the unexposed parts resilient to high light (Karpinski et al., 1999). BR-induced H2O2 accumulation is caused by increased activity of NADPH oxidase as confirmed by measuring the activity of plasma membrane NADPH oxidase in plants treated with 24epibrassinolide (EBR), which is a bioactive brassinosteroid derivative (Xia et al., 2009). Additionally, EBR was also shown to be effective in restoring the NADPH oxidase activity of brassinazole (BRZ, a specific inhibitor of BR biosynthesis) treated plants. Similarly exogenously applied H2O2 showed a similar pattern to that of EBR (Deng et al., 2016). Studies suggest that apart from BAK1 (for BRI1-associated receptor kinase 1), BIN2 (a GSK3/SHAGGY-like kinase), BSU1 (for BRI1 suppressor 1, a phosphatase) and, three other regulatory genes, RBOH (respiratory burst oxidase homolog), MAPK1 (mitogen-activated protein kinases), and MAPK3, were upregulated upon treatment with EBR but downregulated after BRZ treatment emphasizing their vital role (Xia et al., 2009). Exogenous application of BR on the leaves of Niotiana benthamiana were shown to enhance the plant tolerance against several different pathogens (Nakashita et al., 2003). This is accompanied by accumulation of BR-induced MAPK and RBOHB (an NADPH oxidase B) genes and subsequent ROS burst. Eventually, the end products of the target genes directly take part into
the cellular protection. Nevertheless, further studies are warranted to provide genetic evidence for NADPH oxidase’s role in BR-induced ROS generation (Deng et al., 2016). This would pave the way to unveil the critical signaling components in BR signal perception and downstream stress responses, and to elucidate the molecular mechanisms involved in the crosstalk between BR and other hormones.
26.8 CONCLUSION Elucidation of BR signaling pathways is still a challenging task for scientists worldwide. Its multifaceted nature and crosstalk with different growth and developmental pathways in plants make it a complex system to study. As far as stress signaling and BR crosstalk is concerned, a clear role of BR has been established. However, the availability of different model systems and different experimental approaches make it more complicated to untangle the exact pathway. The role of BR signaling in both biotic and abiotic stresses seems to be connected with ROS signaling and potential of an extensive crosstalk between two pathways can be visualized but the BR signaling research is still in its juvenile phase and many more factors are needed to be uncovered to have a clear view of this complex machinery in the plant cell.
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Further Reading He, J.-X., Gendron, J.M., Yang, Y., Li, J., Wang, Z.-Y., 2002. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signalling pathway in Arabidopsis. Proc. Natl Acad. Sci. U.S.A. 99, 10185 10190. Lin, F., Ding, H.D., Wang, J.X., Zhang, H., Zhang, A.Y., Zhang, Y., et al., 2009. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot. 60, 3221 3238. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F., 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490 498.
Xia, X.-J., Gao, C.-J., Song, L.-X., Zhou, Y.-H., Shi, K., Yu, J.-Q., 2014. Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ. 37, 2036 2050. Zhang, A.Y., Jiang, M.Y., Zhang, J.H., Tan, M.P., Hu, X.L., 2006. Mitogenactivatedprotein kinase is involved in abscisic acidinduced antioxidant defence and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol. 141, 475 487. Zhou, J., Wang, J., Li, X., Xia, X.-J., Zhou, Y.-H., Shi, K., et al., 2014. H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J. Exp. Bot. 65, 4371 4383.
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