Specifying the role of BAK1‐interacting receptor‐like kinase 3 in brassinosteroid signaling

Großeholz, Ruth; Feldman‐Salit, Anna; Wanke, Friederike; Schulze, Sarina; Glöckner, Nina; Kemmerling, Birgit; Harter, Klaus; Kummer, Ursula

doi:10.1111/jipb.12803

Cited by 15 publications

(20 citation statements)

References 64 publications

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“…As revealed by the RLP44 interaction pattern, signaling integration and ramification is realized at the level of the receptor complex in the plasma membrane. Additional examples are the interaction of the BRI1-BAK1 complex with G-proteins to mediate sugar-responsive growth (Peng et al, 2018), with the proton pumps of the P-ATPase type to regulate plasma membrane hyperpolarization and wall swelling that precede cell elongation growth (Caesar et al, 2011), and with the BAK1-interacting receptor-like kinase 3 (BIR3) that represses the activity of the complex in the absence of BR (Imkampe et al, 2017;Hohmann et al, 2018;Großeholz et al, 2019). In addition, BRI1 phosphorylates a homolog of the mammalian transforming growth factor-b (TGF-b) receptor interacting protein/ eIF3 eukaryotic translation initiation factor subunit TRIP-1 (Ehsan et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

A Mutant Allele Uncouples the Brassinosteroid-Dependent and Independent Functions of BRASSINOSTEROID INSENSITIVE 1

et al. 2019

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Plants depend on various cell surface receptors to integrate extracellular signals with developmental programs. One of the beststudied receptors is BRASSINOSTEROID INSENSITIVE 1 (BRI1) in Arabidopsis (Arabidopsis thaliana). Upon binding of its hormone ligands, BRI1 forms a complex with a shape-complementary coreceptor and initiates a signal transduction cascade, which leads to a variety of responses. At the macroscopic level, brassinosteroid (BR) biosynthetic and receptor mutants have similar growth defects, which initially led to the assumption that the signaling pathways were largely linear. However, recent evidence suggests that BR signaling is interconnected with several other pathways through various mechanisms. We recently described that feedback from the cell wall is integrated at the level of the receptor complex through interaction with RECEPTOR-LIKE PROTEIN 44 (RLP44). Moreover, BRI1 is required for another function of RLP44: the control of procambial cell fate. Here, we report a BRI1 mutant, bri1 cnu4 , which differentially affects canonical BR signaling and RLP44 function in the vasculature. Although BR signaling is only mildly impaired, bri1 cnu4 mutants show ectopic xylem in place of procambium. Mechanistically, this is explained by an increased association between RLP44 and the mutated BRI1 protein, which prevents the former from acting in vascular cell fate maintenance. Consistent with this, the mild BR response phenotype of bri1 cnu4 is a recessive trait, whereas the RLP44-mediated xylem phenotype is semidominant. Our results highlight the complexity of plant plasma membrane receptor function and provide a tool to dissect BR signaling-related roles of BRI1 from its noncanonical functions. Plant cells perceive a multitude of extracellular signals through a battery of plasma membrane-bound receptors that are crucial for the integration of environmental and developmental signals. The response to the growth-regulatory brassinosteroid (BR) phytohormones is mediated by one of the best-characterized plant signaling pathways (Singh and Savaldi-Goldstein, 2015) initiated by a receptor complex containing the Leu-rich repeat receptor-like kinase BRASSINOSTE-ROID INSENSITIVE 1 (BRI1; Li and Chory, 1997) and its coreceptors of the SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) family (Ma et al., 2016; Hohmann et al., 2017). Binding of the brassinosteroid ligand mediates hetero-dimerization of BRI1 and SERK family members such as BRI1-ASSOCIATED RECEPTOR KINASE 1 (BAK1; Li et al., 2002; Nam and Li, 2002), which in turn triggers extensive autoand transphosphorylation of the intracellular BAK1 and BRI1 kinase domains (Hohmann et al., 2017). The activated kinases recruit and activate downstream BR signaling components, which eventually leads to vast changes in gene expression mediated by BR signalingregulated transcription factors such as BRASSINA-ZOLE-RESISTANT 1 (BZR1; Wang et al., 2002) and BRI1-EMS-SUPPRESSOR 1 (BES1; Yin et al., 2002). Among the transcriptional targets of these transcription factors, cell...

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Section: Discussionmentioning

confidence: 99%

A Mutant Allele Uncouples the Brassinosteroid-Dependent and Independent Functions of BRASSINOSTEROID INSENSITIVE 1

et al. 2019

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“…As revealed by the RLP44 interaction pattern, signalling integration and ramification is realised at the level of the receptor complex in the plasma membrane. Additional examples are the interaction of the BRI1-BAK1 complex with G-proteins to mediate sugar-responsive growth (Peng et al , 2018), with the proton pumps of the P-ATPase type to regulate plasma membrane hyperpolarisation and wall swelling that precede cell elongation growth (Caesar et al , 2011) and with the BAK1-interacting receptor-like kinase 3 (BIR3) that represses the activity of the complex in the absence of BR (Großeholz et al , Imkampe et al , 2017, Hohmann et al , 2018)(Imkampe et al, 2017; Hohmann et al, 2018; Großeholz et al, 2019). In addition, BRI1 phosphorylates a homolog of the mammalian TGF-β receptor interacting protein/eIF3 eukaryotic translation initiation factor subunit TRIP-1 (Ehsan et al , 2005).…”

Section: Discussionmentioning

confidence: 99%

A novel mutant allele uncouples brassinosteroid-dependent and independent functions of BRI1

Holzwart

Gloeckner

Hoefte

et al. 2019

Preprint

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Plants depend on an array of cell surface receptors to integrate extracellular signals with developmental programs. One of the best-studied receptors is BRASSINOSTEROID INSENSITIVE 1 (BRI1), which upon binding of its hormone ligands forms a complex with shape-complimentary co-receptors and initiates a signal transduction cascade leading to a wide range of responses. BR biosynthetic and receptor mutants have similar growth defects on the macroscopic level, which had initially led to the assumption of a largely linear signalling pathway. However, recent evidence suggests that BR signalling is interconnected with a number of other pathways through a variety of different mechanisms. We recently described that feedback information from the cell wall is integrated at the level of the receptor complex through interaction with RLP44. Moreover, BRI1 is required for a second function of RLP44, the control of procambial cell fate. Here, we report on a BRI1 mutant, bri1cnu4, which differentially affects canonical BR signalling and RLP44 function in the vasculature. While BR signalling is only mildly impaired, bri1cnu4 mutants show ectopic xylem in the position of procambium. Mechanistically, this is explained by an increased association of RLP44 and the mutated BRI1 protein, which prevents the former from acting in vascular cell fate maintenance. Consistent with this, the mild BR response phenotype of bri1cnu4 is a recessive trait, whereas the RLP44-mediated xylem phenotype is semi-dominant. Our results highlight the complexity of plant plasma membrane receptor function and provide a tool to dissect BR signalling-related roles of BRI1 from its non-canonical functions.One sentence summaryA novel mutant allows to dissect brassinosteroid signalling related and non-canonical functions of the receptor-like kinase BRI1.

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“…Despite lack of experimental evidence or structural information, it has been widely accepted that stable association of the extracellular domains of BRI1 and BAK1 brings their cytoplasmic domains into close proximity, thus permitting cross phosphorylation, especially at Ser 1044 of BRI1 and Thr 450 of BAK1 within their respective activation loop, and subsequent activation of both kinases [ 45 , 46 , 59 ]. A recent structural modeling study suggested that the cytoplasmic domains of BRI1 and BAK1 could weakly interact independently of BR binding to their extracellular domains [ 60 ]. However, it is important to point out that the structural models of the kinase domains of BRI1 and BAK1 used for the modeling study were derived from autophosphorylated and activated kinase domains with stabilized αC-helixes and activation segments.…”

Section: Bri1 the Br Receptormentioning

confidence: 99%

Regulation of Three Key Kinases of Brassinosteroid Signaling Pathway

Mao

2020

IJMS

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Brassinosteroids (BRs) are important plant growth hormones that regulate a wide range of plant growth and developmental processes. The BR signals are perceived by two cell surface-localized receptor kinases, Brassinosteroid-Insensitive1 (BRI1) and BRI1-Associated receptor Kinase (BAK1), and reach the nucleus through two master transcription factors, bri1-EMS suppressor1 (BES1) and Brassinazole-resistant1 (BZR1). The intracellular transmission of the BR signals from BRI1/BAK1 to BES1/BZR1 is inhibited by a constitutively active kinase Brassinosteroid-Insensitive2 (BIN2) that phosphorylates and negatively regulates BES1/BZR1. Since their initial discoveries, further studies have revealed a plethora of biochemical and cellular mechanisms that regulate their protein abundance, subcellular localizations, and signaling activities. In this review, we provide a critical analysis of the current literature concerning activation, inactivation, and other regulatory mechanisms of three key kinases of the BR signaling cascade, BRI1, BAK1, and BIN2, and discuss some unresolved controversies and outstanding questions that require further investigation.

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Specifying the role of BAK1‐interacting receptor‐like kinase 3 in brassinosteroid signaling

Cited by 15 publications

References 64 publications

A Mutant Allele Uncouples the Brassinosteroid-Dependent and Independent Functions of BRASSINOSTEROID INSENSITIVE 1

A Mutant Allele Uncouples the Brassinosteroid-Dependent and Independent Functions of BRASSINOSTEROID INSENSITIVE 1

A novel mutant allele uncouples brassinosteroid-dependent and independent functions of BRI1

Regulation of Three Key Kinases of Brassinosteroid Signaling Pathway

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