2016 article

Brassinosteroid/Abscisic Acid Antagonism in Balancing Growth and Stress

Clouse, S. D. (2016, July 25). DEVELOPMENTAL CELL, Vol. 38, pp. 118–120.

By: S. Clouse n

TL;DR: In this issue of Developmental Cell, Gui et al. (2016) show that an abscisic acid-inducible remorin protein in rice directly interacts with critical brassinosteroid signaling components to attenuate the brass inosteroid response, thus illuminating one aspect of the brassInosteroid/abscisicsic acid antagonism. (via Semantic Scholar)
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In this issue of Developmental Cell, Gui et al., 2016Gui J. Zheng S. Liu C. Shen J. Li J. Li L. Dev. Cell. 2016; 38 (this issue): 201-213Google Scholar show that an abscisic acid-inducible remorin protein in rice directly interacts with critical brassinosteroid signaling components to attenuate the brassinosteroid response, thus illuminating one aspect of the brassinosteroid/abscisic acid antagonism. In this issue of Developmental Cell, Gui et al., 2016Gui J. Zheng S. Liu C. Shen J. Li J. Li L. Dev. Cell. 2016; 38 (this issue): 201-213Google Scholar show that an abscisic acid-inducible remorin protein in rice directly interacts with critical brassinosteroid signaling components to attenuate the brassinosteroid response, thus illuminating one aspect of the brassinosteroid/abscisic acid antagonism. Plant hormones regulate numerous aspects of plant growth, development, and environmental response through a diverse array of signal transduction pathways that modulate the expression of thousands of different genes required for cell elongation, division, and differentiation. Brassinosteroids (BRs), belonging to one such class of plant hormones, have structural similarity to mammalian steroid hormones and, like their animal counterparts, have a profound influence on cellular dynamics and function. Null mutations in genes encoding BR biosynthetic enzymes or signal transduction components show severe phenotypes including dwarfism, disruptions in leaf, flower, and root development, and altered vascular structure, suggesting that BRs are essential for normal plant development (Belkhadir and Jaillais, 2015Belkhadir Y. Jaillais Y. New Phytol. 2015; 206: 522-540Crossref PubMed Scopus (159) Google Scholar). In changing environmental conditions, plants must shift resources from growth and development to adaptation to stresses such as drought and temperature extremes. This process is accelerated by another plant hormone, abscisic acid (ABA), which responds to drought in part by regulating leaf stomatal aperture, although it also functions in embryo development and seed germination (Hauser et al., 2011Hauser F. Waadt R. Schroeder J.I. Curr. Biol. 2011; 21: R346-R355Abstract Full Text Full Text PDF PubMed Scopus (334) Google Scholar). As part of the adaptive response to stress, ABA can inhibit vegetative growth and thus oppose the growth-promoting properties of BRs. Twenty years ago it was found that mutants unresponsive to the inhibitory effect of BRs on root elongation were hypersensitive to root length inhibition by ABA, suggesting an antagonistic interaction between these two hormones (Clouse et al., 1996Clouse S.D. Langford M. McMorris T.C. Plant Physiol. 1996; 111: 671-678Crossref PubMed Scopus (630) Google Scholar). Numerous other examples of the BR/ABA antagonism have been reported since, but the precise molecular mechanisms that are responsible for this physiological response could not be uncovered until both BR and ABA signal transduction pathways became well characterized (Saini et al., 2015Saini S. Sharma I. Pati P.K. Front. Plant Sci. 2015; 6: 1-17Crossref Scopus (131) Google Scholar). Gui et al., 2016Gui J. Zheng S. Liu C. Shen J. Li J. Li L. Dev. Cell. 2016; 38 (this issue): 201-213Google Scholar now describe one mechanism of BR/ABA interaction involving a remorin protein that is regulated by ABA and in turn regulates BR signal transduction. BRs are perceived by the extracellular domain of a leucine-rich repeat receptor kinase named BRASSINOSTEROID INSENSITIVE 1 (BRI1), which, in the presence of ligand, interacts with and reciprocally transphosphorylates a co-receptor from the SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) family of smaller leucine-rich repeat receptor kinases (Figure 1). The formation of an active complex between BRI1 and SERK family members such as SERK1 and SERK3 (also known as BRI1-ASSOCIATED RECEPTOR KINASE 1 or BAK1) is a critical step in BR signaling because it initiates a phospho-relay involving cytoplasmic kinases and phosphatases that ultimately results in the activation of specific transcription factors that regulate the expression of nearly 1,000 genes (Belkhadir and Jaillais, 2015Belkhadir Y. Jaillais Y. New Phytol. 2015; 206: 522-540Crossref PubMed Scopus (159) Google Scholar). In both Arabidopsis thaliana and rice, BRI1 INHIBITIOR KINASE 1 (BKI1) is a membrane-bound negative regulator of BR signaling that binds to BRI1 in the absence of BR and prevents the interaction of BRI1 with SERK co-receptors. Upon BR binding to BRI1, BKI1 is phosphorylated on a tyrosine residue and released from the membrane, allowing the BRI1/SERK complex to form, which propagates BR signaling downstream (Jiang et al., 2015Jiang J. Wang T. Wu Z. Wang J. Zhang C. Wang H. Wang Z.X. Wang X. Mol. Plant. 2015; 8: 1675-1678Abstract Full Text Full Text PDF Scopus (33) Google Scholar). Gui et al., 2016Gui J. Zheng S. Liu C. Shen J. Li J. Li L. Dev. Cell. 2016; 38 (this issue): 201-213Google Scholar have now identified a protein that has a function similar to BKI1, i.e., disruption of the BRI1/SERK complex formation and downregulation of BR signaling, but with a twist: this rice protein, termed OsREM4.1, is encoded by a gene whose transcript levels are regulated by ABA. Specifically, OsREM4.1 levels are increased by elevated ABA levels through a bZIP transcription factor (OsbZIP23) in the ABA signal transduction pathway. In Arabidopsis, it is known that binding of ABA to its soluble receptor results in inactivation of a PP2C phosphatase, which in turn allows activation of a SnRK2 kinase that phosphorylates downstream transcription factors and ion channels required for the ABA response (Hauser et al., 2011Hauser F. Waadt R. Schroeder J.I. Curr. Biol. 2011; 21: R346-R355Abstract Full Text Full Text PDF PubMed Scopus (334) Google Scholar). Recently, it was also shown in rice that OsbZIP23 is phosphorylated by a SnRK2 kinase in response to ABA (Zong et al., 2016Zong W. Tang N. Yang J. Peng L. Ma S. Xu Y. Li G. Xiong L. Plant Physiol. 2016; (in press. Published online June 20, 2016)https://doi.org/10.1104/pp.16.00469Crossref Scopus (165) Google Scholar). OsREM4.1 belongs to the plant-specific remorin family of proteins whose members are membrane-associated and often involved in plant-microbe interactions or hormone response. After establishing that OsREM4.1 transcription was specifically upregulated by ABA, Gui et al., 2016Gui J. Zheng S. Liu C. Shen J. Li J. Li L. Dev. Cell. 2016; 38 (this issue): 201-213Google Scholar then searched for OsREM4.1-interacting proteins by immunoprecipitation followed by liquid chromatography/tandem mass spectrometry. A particularly interesting candidate uncovered was OsSERK1, the co-receptor of BRI1 in rice. Numerous independent lines of analysis confirmed the OsREM4.1/OsSERK1 interaction, and examination of the phenotype of transgenic lines expressing either high or low levels of OsREM4.1 showed that OsREM4.1 was a negative regulator of BR signaling. Moreover, OsREM4.1 binds to the activation loop of the OsSERK1 kinase domain, thereby inhibiting the formation of the OsSERK1/OsBRI1 complex and preventing transphosphorylation of BRI1 and SERK1, thus negatively regulating BR signaling. Interestingly, increased BR levels caused OsBRI1 to directly phosphorylate OsREM4.1 and release its inhibition of the OsSERK1/OsBRI1 active complex in a manner reminiscent of the BKI1 protein. When viewed together, the accumulated evidence of Gui et al., 2016Gui J. Zheng S. Liu C. Shen J. Li J. Li L. Dev. Cell. 2016; 38 (this issue): 201-213Google Scholar suggests a central role for OSREM4.1 in mediating the ABA/BR antagonism in rice. Under conditions of stress, ABA levels are rapidly elevated, increasing OsREM4.1 levels to facilitate disruption of the critical OsBRI1/OsSERK1 complex and downregulation of BR signaling, which would favor shifting plant resources from BR-promoted growth to ABA-regulated stress responses. When stress decreases, ABA levels fall and BR-promoted phosphorylation of OsREM4.1 by OsBRI1 increases, releasing OsREM4.1 from the complex and thus allowing transphosphorylation of OsBRI1/OsSERK1 to reactivate the growth-promoting BR signal transduction pathway (Figure 1). A recent study demonstrated direct interaction between downstream elements of the BR and ABA signaling pathways in Arabidopsis, providing another mechanism of antagonistic crosstalk in the regulation of root growth. BRASSINAZOLE RESISTANT 1 (BZR1), one of the primary transcription factors regulating BR-responsive genes (Figure 1), was found to directly bind to the promoter of ABSCISIC ACID INSENSTIVE 5 (ABI5), an important transcription factor in ABA signaling, leading to suppressed ABI5 expression and reduced ABA response (Yang et al., 2016Yang X. Bai Y. Shang J. Xin R. Tang W. Plant Cell Environ. 2016; (in press. Published online May 5, 2016)https://doi.org/10.1111/pce.12763Crossref Scopus (59) Google Scholar). Several other examples of direct interaction between BR and ABA signaling components in a variety of physiological processes have also been reported (Hu and Yu, 2014Hu Y. Yu D. Plant Cell. 2014; 26: 4394-4408Crossref PubMed Scopus (177) Google Scholar, Shang et al., 2016Shang Y. Dai C. Lee M.M. Kwak J.M. Nam K.H. Mol. Plant. 2016; 9: 447-460Abstract Full Text Full Text PDF PubMed Scopus (113) Google Scholar). The work of Gui et al. in this issue provides an addition to this growing list of mechanisms integrating distinct hormone signal transduction pathways that balance complex developmental programs leading to plant growth with those regulating adaptation to changing environments. This article was written while serving in a paid position at the National Science Foundation. Any opinions or conclusions expressed in this article are those of the author and do not necessarily reflect the views of the National Science Foundation. OsREM4.1 Interacts with OsSERK1 to Coordinate the Interlinking between Abscisic Acid and Brassinosteroid Signaling in RiceGui et al.Developmental CellJuly 14, 2016In BriefThe hormones abscisic acid (ABA) and brassinosteroid (BR) exhibit antagonistic interactions during plant development. Gui et al. now identify rice OsREM4.1 as a link between the ABA and BR signaling pathways. OsREM4.1, which is transcriptionally upregulated by ABA, inhibits the formation and activation of a BR receptor kinase (OsBRI1-OsSERK1) complex. Full-Text PDF Open Archive