SUMO Conjugation to BZR1 Enables Brassinosteroid Signaling to Integrate Environmental Cues to Shape Plant Growth

Srivastava, Moumita; Srivastava, Anjil Kumar; Orosa, Beatriz; Campanaro, Alberto; Zhang, Cunjin; Sadanandom, Ari

doi:10.1016/j.cub.2020.01.089

Cited by 58 publications

(58 citation statements)

References 45 publications

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“…This temporally suppressed BR signaling, however, recovers soon due to BR-induced degradation of ULP1a [165]. ULP1a was reported to inhibit growth during salt stress and ulp1a mutants were salt-tolerant [165]. Taken together, the antagonistic regulation of ULP1a by salinity and BRs seems to be a molecular switch determining plant growth and salt stress response.…”

Section: Minerals and Ionsmentioning

confidence: 96%

“…BRs might regulate plasma membrane localized cation and anion channels that implicate in ion stress response [162,163]. It was not until recently that two studies proposed a molecular mechanism by which BR signaling dynamically respond to salt stress and positively contribute to salt tolerance [164,165]. In the early stage of salt stress response, salinity stimulates the protein accumulation of ULP1a, a deSUMOylating enzyme which is able to deSUMOylate BZR1 and facilitate its phosphorylation by BIN2 and ultimately degradation, thus inhibiting BR signaling [165].…”

Section: Minerals and Ionsmentioning

confidence: 99%

“…It was not until recently that two studies proposed a molecular mechanism by which BR signaling dynamically respond to salt stress and positively contribute to salt tolerance [164,165]. In the early stage of salt stress response, salinity stimulates the protein accumulation of ULP1a, a deSUMOylating enzyme which is able to deSUMOylate BZR1 and facilitate its phosphorylation by BIN2 and ultimately degradation, thus inhibiting BR signaling [165]. This temporally suppressed BR signaling, however, recovers soon due to BR-induced degradation of ULP1a [165].…”

Section: Minerals and Ionsmentioning

confidence: 99%

“…In the early stage of salt stress response, salinity stimulates the protein accumulation of ULP1a, a deSUMOylating enzyme which is able to deSUMOylate BZR1 and facilitate its phosphorylation by BIN2 and ultimately degradation, thus inhibiting BR signaling [165]. This temporally suppressed BR signaling, however, recovers soon due to BR-induced degradation of ULP1a [165]. ULP1a was reported to inhibit growth during salt stress and ulp1a mutants were salt-tolerant [165].…”

Section: Minerals and Ionsmentioning

confidence: 99%

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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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Section: Minerals and Ionsmentioning

confidence: 96%

Section: Minerals and Ionsmentioning

confidence: 99%

Section: Minerals and Ionsmentioning

confidence: 99%

Section: Minerals and Ionsmentioning

confidence: 99%

See 2 more Smart Citations

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

2020

IJMS

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“…its kinase activity and is required for endocytosis and control of protein levels [42,43] . BZR1 protein levels are modulated by the U-Box40 E3 ligase [44] and by sumoylation [45] . Cross-talk influencing DA1 activity is fundamentally different as it does not involve ubiquitin-mediated targeting or proteasomal degradation [14,44] .…”

Section: Polyubiquitylation Of Bri1 By the U-box E3 Ligases Pub12 Andmentioning

confidence: 99%

The Receptor Kinase BRI1 promotes cell proliferation in Arabidopsis by phosphorylation- mediated inhibition of the growth repressing peptidase DA1

Dong

Smith

et al. 2020

Preprint

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Brassinosteroids (BR) have centrally important functions in plant growth by promoting cell proliferation and cell expansion through phosphorylation-mediated regulatory cascades that are initiated by perception of BR by receptor-like kinases of the BRI1 family. These BR-mediated growth responses have been explained by transcriptional controls mediated by phosphorylation of BES1/BZR1 transcription factors. Here we link BRI1-mediated phosphorylation to another growth regulatory network that directly mediates protein stability. BRI1 and its co-receptor BAK1 phosphorylate and inhibit the activities of the growth repressor DA1 by promoting the formation of high molecular weight complexes. Phospho-mimic forms of DA1 are less active while phospho-dead mutants have increased growth-repressive activity, while their regulatory monoubiquitylation is unaffected. BR inhibition of DA1 activity maintains higher levels of DA1 substrates such as UBP15 that sustain the potential for cell proliferation during leaf growth. Reduced BR levels lead to activation of DA1 peptidase activity and a transition from cell proliferation to cell growth and differentiation. This dual monoubiquitylation-phosphorylation regulation supports the key role of BR levels in maintaining the proliferative potential of cells during organ growth.

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Chloroplast Stress Signals: Control of Retrograde Signaling, Chloroplast Turn-Over, and Cell Fate Decisions

Woodson,

Lemke,

Tano

et al. 2024

Nucleic Acids and Molecular Biology

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SUMO Conjugation to BZR1 Enables Brassinosteroid Signaling to Integrate Environmental Cues to Shape Plant Growth

Cited by 58 publications

References 45 publications

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

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

The Receptor Kinase BRI1 promotes cell proliferation in Arabidopsis by phosphorylation- mediated inhibition of the growth repressing peptidase DA1

Chloroplast Stress Signals: Control of Retrograde Signaling, Chloroplast Turn-Over, and Cell Fate Decisions

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