Formation and Dissociation of the BSS1 Protein Complex Regulates Plant Development via Brassinosteroid Signaling

Shimada, Setsuko; Komatsu, Tomoyuki; Yamagami, Ayumi; Nakazawa, Miki; Matsui, Minami; Kawaide, Hiroshi; Natsume, Masahiro; Osada, Hiroyuki; Asami, Tadao; Nakano, Takeshi

doi:10.1105/tpc.114.131508

Cited by 48 publications

(37 citation statements)

References 53 publications

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“…5c). A similar punctate BiFC signal has been previously reported for BZR1 with BRZ-SENSITIVE-SHORT HYPOCOTYL1 (BSS1) 50 or BES1 with DOMINANT SUPPRESSOR OF KAR 2 (DSK2) 7 , although its significance remains unknown.…”

Section: Resultssupporting

confidence: 80%

TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in plant cells

Amorim‐Silva

García-Moreno

Lakhssassi

et al. 2018

Preprint

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36Brassinosteroids (BRs) form a group of steroidal hormones essential for plant 37 growth, development and stress responses. Here, we report that plant-specific 38 TETRATRICOPEPTIDE THIOREDOXIN-LIKE (TTL) proteins are positive 39 regulators of BR signaling functioning as scaffold for BR signaling components 40 in Arabidopsis. TTL3 forms a complex with all core components involved in BR 41 signaling, including the receptor kinase BRASSINOSTEROID INSENSITIVE1 42 (BRI1), the transcription factor BRASSINAZOLE RESISTANT1 (BZR1) and the 43 phosphatase BRI1-SUPPRESSOR1 (BSU1), but excluding the co-receptor 44 BAK1. TTL3 is mainly localized in the cytoplasm, but BR treatment increases its 45 localization at the plasma membrane, where it strengthens the association with 46 BR signaling components. Consistent with a role in BR signaling, mutations in 47We propose a mechanistic model for BR signaling, in which cytoplasmic/nuclear 49 BR components bound to TTL proteins are recruited to the plasma membrane 50 upon BR perception, which in turn allows the assembly of a BR signaling 51 complex, leading to the de-phosphorylation and nuclear accumulation of the 52 transcription factors BZR1 and BES1. 53 Introduction 54Plants live in constantly changing environments that are often unfavorable or 55 stressful for growth and development. In these conditions it is essential to 56 balance growth and stress responses to ensure proper allocation of resources 1 . 57While an active growth causes the generation of new roots and leaves, allowing 58 a better exploitation of environmental resources, it can also cause the depletion 59 of resources that could be important for the survival under stress episodes 2,3 . 60Brassinosteroids (BRs) are a family of growth-promoting hormones having 61 essential roles in a wide range of developmental and physiological processes 62 2,4,5 . However, in addition to their well-established function in growth, essential 63 roles in the trade-off between growth and tolerance to biotic and abiotic stress 64 episodes are now being unveiled 6-9 . 65 BRs are perceived at the plasma membrane by ligand-induced heterodimers of 66 the receptors kinases BRASSINOSTEROID INSENSITIVE1 (BRI1) and 67 SOMATIC EMBBRYOGENESIS RECEPTOR KINASE (SERK) protein family-68 members, which activates an interconnected signal transduction cascade, 69 leading to the transcriptional regulation of BR-responsive genes 5 . BRI1 70 KINASE INHIBITOR 1 (BKI1) dissociates from activated BRI1, which 71 phosphorylates the kinases BR-SIGNALING KINASE1 (BSK1) and the 72 CONSTITUTIVE DIFFERENTIAL GROWTH1 (CDG1), which in turn 73 phosphorylate the phosphatase BRI1-SUPPRESSOR1 (BSU1). Then, the 74 active (phosphorylated) BSU1 lead to dephosphorylation and inactivation of the 75 glycogen synthase kinase 3 (GSK3)-like BRASSINOSTEROID INSENSITIVE2 76 (BIN2), a key regulator in BR signaling. In the absence of BRs, BIN2 is active 77 and phosphorylates the two homologous transcription factors BRASSINAZOLE 78 RESISTANT1 (BZR1) and BRI1-ETHYL METHANESULFONATE ...

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Section: Resultssupporting

confidence: 80%

TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in plant cells

Amorim‐Silva

García-Moreno

Lakhssassi

et al. 2018

Preprint

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“…BIN2-induced phosphorylation inactivates BES1 and BZR1 by promoting their cytoplasmic retention via 14-3-3 proteins (Gampala et al, 2007;Ryu et al, 2007), inhibiting their DNA binding activity (Vert and Chory, 2006), and stimulating their degradation Yin et al, 2002;Nolan et al, 2017b;Kim et al, 2019). Moreover, BES1 and BZR1 are kept in an inactivate state through interactions with the BROAD COMPLEX/TRAMTRACK/BRIC-A-BRAC family protein BRZ-SENSITIVE-SHORT HYPOCOTYL1 (BSS1) under BR-deficient conditions (Shimada et al, 2015).…”

Section: Inhibition Of Br Signalingmentioning

confidence: 99%

“…BSS1, also known as BLADE ON PETIOLE1 (BOP1), acts as part of a CUL3 BOP1/BOP2 E3 ubiquitin ligase complex that facilitates PIF4 degradation during photomorphogenesis . Thus, given that BSS1/BOP1 also interacts with BES1 and BZR1 and affects their protein levels (Shimada et al, 2015), it would be interesting to determine if BSS1 plays a role in BES1 and BZR1 ubiquitination.…”

Section: Bes1 and Bzr1 Regulation: More Than Just Phosphorylationmentioning

confidence: 99%

Brassinosteroids: Multidimensional Regulators of Plant Growth, Development, and Stress Responses

et al. 2019

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Brassinosteroids (BRs) are a group of polyhydroxylated plant steroid hormones that are crucial for many aspects of a plant's life. BRs were originally characterized for their function in cell elongation, but it is becoming clear that they play major roles in plant growth, development, and responses to several stresses such as extreme temperatures and drought. A BR signaling pathway from cell surface receptors to central transcription factors has been well characterized. Here, we summarize recent progress toward understanding the BR pathway, including BR perception and the molecular mechanisms of BR signaling. Next, we discuss the roles of BRs in development and stress responses. Finally, we show how knowledge of the BR pathway is being applied to manipulate the growth and stress responses of crops. These studies highlight the complex regulation of BR signaling, multiple points of crosstalk between BRs and other hormones or stress responses, and the finely tuned spatiotemporal regulation of BR signaling.

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“…At the BIN2 level, it has been reported that BIN2 is regulated by OCTOPUSor POLAR-mediated membrane sequestration, HDA6-mediated deacetylation, KIB1-mediated ubiquitination, TTL-enhanced interaction with BSU1, ABI1/2-mediated dephosphorylation, and ROS (reactive oxygen species)-mediated oxidation [74][75][76][77][78][79][80]. At the transcription level, it has been reported that PP2A phosphatases can promote BR signaling by dephosphorylating BES1 and BZR1, whereas 14-3-3 and BRZ-SENSITIVE-SHORT HYPOCOTYL1 (BSS1) negatively regulate BR signaling by inhibiting the translocation of BES1 and BZR1 from the cytosol to the nucleus [81][82][83]. Besides, protein degradation of BES1 and/or BZR1 has been reported to be regulated by many factors, including an F-box protein MORE AXILLARY GROWTH LOCUS2 (MAX2), ubiquitin E3 ligases such as PLANT U-BOX40 (PUB40), CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and SINA of Arabidopsis thaliana (SINATs), photoreceptors such as UV RESISTANCE LOCUS 8 (UVR8), CRYPTOCHROME1 (CRY1) and PHYTOCHROME B (PHYB), and an autophagy receptor DOMINANT SUPPRESSOR OF KAR2 (DSK2) [84][85][86][87][88][89][90][91][92][93].…”

mentioning

confidence: 99%

Molecular Mechanisms of Brassinosteroid-Mediated Responses to Changing Environments in Arabidopsis

2020

IJMS

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Plant adaptations to changing environments rely on integrating external stimuli into internal responses. Brassinosteroids (BRs), a group of growth-promoting phytohormones, have been reported to act as signal molecules mediating these processes. BRs are perceived by cell surface receptor complex including receptor BRI1 and coreceptor BAK1, which subsequently triggers a signaling cascade that leads to inhibition of BIN2 and activation of BES1/BZR1 transcription factors. BES1/BZR1 can directly regulate the expression of thousands of downstream responsive genes. Recent studies in the model plant Arabidopsis demonstrated that BR biosynthesis and signal transduction, especially the regulatory components BIN2 and BES1/BZR1, are finely tuned by various environmental cues. Here, we summarize these research updates and give a comprehensive review of how BR biosynthesis and signaling are modulated by changing environments and how these changes regulate plant adaptive growth or stress tolerance.Int. J. Mol. Sci. 2020, 21, 2737 3 of 20 BR signal cascade by phosphorylating BR SIGNALING KINASE 1 (BSK1) and CDG1, two receptor-like cytoplasmic kinases (RLCKs) that are anchored to the cell membrane [59,60]. Activated CDG1 can subsequently phosphorylate and activate a protein phosphatase BSU1, which then dephosphorylates and inactivates a GSK3 kinase BRASSINOSTEROID INSENSITIVE 2 (BIN2) [60][61][62]. BIN2 is a negative regulator in the BR signaling pathway because it phosphorylates and destabilizes two well-characterized downstream transcription factors, BRI1-EMS-SUPPRESSOR 1 (BES1) and BRSSINAZOLE-RESISTANT 1 (BZR1), and presumably other four members of their entire subfamily [63][64][65][66][67]. BR-induced BIN2 inactivation allows the accumulation of nonphosphorylated BES1 and BZR1 in the nucleus, thereby promoting expression of thousands of their target genes [62,68]. The intensity of BR signaling can be controlled at multiple levels (Figure 2). At the receptor level, the function of BRI1 can be post-translationally regulated by PUB12/13-directed ubiquitination, PP2A-mediated dephosphorylation, BKI1-mediated kinase inhibition, and BIK1-and BIR3-mediated competition for the coreceptor BAK1 [69][70][71][72][73]. At the BIN2 level, it has been reported that BIN2 is regulated by OCTOPUSor POLAR-mediated membrane sequestration, HDA6-mediated deacetylation, KIB1-mediated ubiquitination, TTL-enhanced interaction with BSU1, ABI1/2-mediated dephosphorylation, and ROS (reactive oxygen species)-mediated oxidation [74][75][76][77][78][79][80]. At the transcription level, it has been reported that PP2A phosphatases can promote BR signaling by dephosphorylating BES1 and BZR1, whereas 14-3-3 and BRZ-SENSITIVE-SHORT HYPOCOTYL1 (BSS1) negatively regulate BR signaling by inhibiting the translocation of BES1 and BZR1 from the cytosol to the nucleus [81][82][83]. Besides, protein degradation of BES1 and/or BZR1 has been reported to be regulated by many factors, including an F-box protein MORE AXILLARY GROWTH LOCUS2 (MAX2), ubiquitin E3 ligases suc...

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Formation and Dissociation of the BSS1 Protein Complex Regulates Plant Development via Brassinosteroid Signaling

Cited by 48 publications

References 53 publications

TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in plant cells

TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in plant cells

Brassinosteroids: Multidimensional Regulators of Plant Growth, Development, and Stress Responses

Molecular Mechanisms of Brassinosteroid-Mediated Responses to Changing Environments in Arabidopsis

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