Regulation of the Arabidopsis GSK3-like Kinase BRASSINOSTEROID-INSENSITIVE 2 through Proteasome-Mediated Protein Degradation

Peng, Peng; Yan, Zhenyan; Zhu, Yanjing; Li, Jianming

doi:10.1093/mp/ssn001

Cited by 171 publications

(152 citation statements)

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“…PIF41A expression partially suppresses the dwarf phenotype of bin2-1 mutants To further assess constitutive activation of this mutant protein, we analyzed whether PIF41A overexpression suppresses the severe dwarf phenotype of bin2-1 mutants, impaired in BR signaling due to constitutive BIN2 activation (Peng et al 2008). As shown in Supplemental Figures S9 and S10, PIF41A expression rescued the semidwarf phenotype of heterozygous bin2-1 +/À mutants but did not suppress the more severe phenotype of homozygous plants.…”

Section: Bin2 Phosphorylates Pif4 In Vitromentioning

confidence: 99%

BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth

et al. 2014

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Signaling by the hormones brassinosteroid (BR) and gibberellin (GA) is critical to normal plant growth and development and is required for hypocotyl elongation in response to dark and elevated temperatures. Active BR signaling is essential for GA promotion of hypocotyl growth and suppresses the dwarf phenotype of GA mutants. Cross-talk between these hormones occurs downstream from the DELLAs, as GA-induced destabilization of these GA signaling repressors is not affected by BRs. Here we show that the light-regulated PIF4 (phytochromeinteracting factor 4) factor is a phosphorylation target of the BR signaling kinase BRASSINOSTEROID-INSENSITIVE 2 (BIN2), which marks this transcriptional regulator for proteasome degradation. Expression of a mutated PIF41A protein lacking a conserved BIN2 phosphorylation consensus causes a severe elongated phenotype and strongly up-regulated expression of the gene targets. However, PIF41A is not able to suppress the dwarf phenotype of the bin2-1 mutant with constitutive activation of this kinase. PIFs were shown to be required for the constitutive BR response of bes1-D and bzr1-1D mutants, these factors acting in an interdependent manner to promote cell elongation. Here, we show that bes1-D seedlings are still repressed by the inhibitor BRZ in the light and that expression of the nonphosphorylatable PIF41A protein makes this mutant fully insensitive to brassinazole (BRZ). PIF41A is preferentially stabilized at dawn, coinciding with the diurnal time of maximal growth. These results uncover a main role of BRs in antagonizing light signaling by inhibiting BIN2-mediated destabilization of the PIF4 factor. This regulation plays a prevalent role in timing hypocotyl elongation to late night, before light activation of phytochrome B (PHYB) and accumulation of DELLAs restricts PIF4 transcriptional activity.

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Section: Bin2 Phosphorylates Pif4 In Vitromentioning

confidence: 99%

BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth

et al. 2014

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“…To understand at which point ABA becomes involved in the BR signaling cascade, we examined whether the downstream BR signaling component, BIN2, a negative regulator of BR signaling, is required for their cross-talk. Because BIN2 has several homologues, we used a specific GSK3 kinase inhibitor, lithium chloride (LiCl), to block the activity of BIN2 kinase (44). First, we treated the seedlings of aba1 with 10 mM LiCl, 10 mM KCl, and 10 mM LiCl plus 1 M ABA or 10 mM KCl plus 1 M ABA, and measured the transcript levels of DWF4 and CPD.…”

Section: Newly Identified Br-related Mutants and Overexpression Linesmentioning

confidence: 99%

The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling

Zhang

Cai

Wang

2009

Proc. Natl. Acad. Sci. U.S.A.

245

207

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Phytohormones have essential roles in coordinately regulating a large array of developmental processes. Studies have revealed that brassinosteroids (BRs) and abscisic acid (ABA) interact to regulate hundreds of expression in genes, governing many biological processes. However, whether their interaction is through modification or intersection of their primary signaling cascades, or by independent or parallel pathways remains a big mystery. Using biochemical and molecular markers of BR signaling and ABA biosynthetic mutants, we demonstrated that exogenous ABA rapidly inhibits BR signaling outputs as indicated by the phosphorylation status of BES1 and BR-responsive gene expression. Experiments using a bri1 null-allele, bri1-116, and analysis of subcellular localization of BKI1-YFP further revealed that the BR receptor complex is not required for ABA to act on BR signaling outputs. However, when the BR downstream signaling component BIN2 is inhibited by LiCl, ABA failed to inhibit BR signaling outputs. Also, using a set of ABA insensitive mutants, we found that regulation of ABA on the BR primary signaling pathway depends on the ABA early signaling components, ABI1 and ABI2. We propose that the signaling cascades of ABA and BR primarily cross-talk after BR perception, but before their transcriptional activation. This model provides a reasonable explanation for why a large proportion of BR-responsive genes are also regulated by ABA, and provides an insight into the molecular mechanisms by which BRs could interact with ABA.cross-talk ͉ gene expression ͉ phosphorylation ͉ seed germination ͉ signal transduction U nlike animals, plants are sessile and need to constantly regulate their developmental and physiological processes to respond to various internal and external stimuli. Studies have revealed that many biological processes result from integrating multiple hormonal signals, and extensive cross-talk among different hormonal signaling pathways is present in plants (1, 2). Recently, a large set of microarray data verified that many genes are coregulated by multiple hormones, suggesting the importance of hormones to coordinately regulate biological processes in plants (3,4). A few studies have also elucidated specific molecular mechanisms of hormonal cross-talk. They include the role of auxin and ethylene in regulating root meristem development (1), the antagonistic relationship between abscisic acid (ABA) and gibberellins (GAs) on seed dormancy and germination (5, 6), and integration of the primary signaling pathways of auxin and brassinosteroids (BRs) by auxin response factor 2 (ARF2) (7).Studies have indicated that BRs and ABA can coregulate the expression of hundreds of genes (4), and they interact physiologically in controlling many developmental processes (5,(8)(9)(10). It is also well known that ABA is required to establish seed dormancy during embryo maturation and to inhibit seed germination (5), whereas BRs promote seed germination, likely through enhancing the embryo growth potential to antagonize the effect...

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“…In the absence of BRs, BRI1 and its coreceptor BRI1-Associated receptor Kinase (BAK1) are inactive kinases Nam and Li, 2002;Wang et al, 2005a), while a GSK3-like kinase BRASSINOSTEROID-INSENSITIVE2 (BIN2) is constitutively active to phosphorylate two highly similar transcription factors, bri1-EMS-Suppressor 1 (BES1) and BrassinazoleResistant1 (BZR1) Wang et al, 2002;Yin et al, 2002;Zhao et al, 2002), thus promoting their degradation, retaining them in cytosol, and/or inhibiting their DNA binding activity (Vert and Chory, 2006;Bai et al, 2007;Gampala et al, 2007;Ryu et al, 2007). BR binding to BRI1 triggers a rapid dissociation of BRI1 Kinase Inhibitor1 from BRI1 and promotes heterotetramerization and transphosphorylation of BRI1 and BAK1 (Wang et al, 2005bWang and Chory, 2006), leading to phosphorylation of BR-signaling kinases and inhibition of BIN2 (Peng et al, 2008;Tang et al, 2008). Consequently, BES1 and BZR1 accumulate in the nucleus to regulate expression of their target genes (He et al, 2005;Yin et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Regulation ofArabidopsisBrassinosteroid Signaling by Atypical Basic Helix-Loop-Helix Proteins

et al. 2009

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Basic helix-loop-helix (bHLH) proteins are highly conserved transcription factors critical for cell proliferation and differentiation. Recent studies have implicated bHLH proteins in many plant signaling processes, including brassinosteroid (BR) signaling. Here, we report identification of two families of atypical bHLH proteins capable of modulating BR signaling. We found that activation-tagged bri1 suppressor 1-Dominant (atbs1-D), previously identified as a dominant suppressor of a weak BR receptor mutant bri1-301, was caused by overexpression of a 93-amino acid atypical bHLH protein lacking amino acids critical for DNA binding. Interestingly, atbs1-D only suppresses weak BR mutants, while overexpression of a truncated ATBS1 lacking the basic motif also rescues bri1-301, suggesting that ATBS1 likely stimulates BR signaling by sequestering negative BR signaling components. A yeast two-hybrid screen using ATBS1 as bait discovered four ATBS1-Interacting Factors (AIFs) that are members of another atypical bHLH protein subfamily. AIF1 exhibits an overlapping expression pattern with ATBS1 and its homologs and interacts with ATBS1 in vitro and in vivo. AIF1 overexpression nullifies the suppressive effect of atbs1-D on bri1-301 and results in dwarf transgenic plants resembling BR mutants. By contrast, silencing of AIF1 partially suppressed the bri1-301 phenotype. Our results suggested that plants use these atypical bHLH proteins to regulate BR signaling.

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Regulation of the Arabidopsis GSK3-like Kinase BRASSINOSTEROID-INSENSITIVE 2 through Proteasome-Mediated Protein Degradation

Cited by 171 publications

References 48 publications

BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth

BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth

The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling

Regulation ofArabidopsisBrassinosteroid Signaling by Atypical Basic Helix-Loop-Helix Proteins

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