Transcription factor HAT1 is phosphorylated by BIN2 kinase and mediates brassinosteroid repressed gene expression in Arabidopsis

Plant J. 2014 Jan;77(1):59-70. doi: 10.1111/tpj.12368. Epub 2013 Dec 3.

Abstract

Plant steroid hormones, brassinosteroids (BRs), play essential roles in modulating cell elongation, vascular differentiation, senescence and stress responses. BRs signal through plasma membrane-localized receptor and other components to modulate the BES1/BZR1 (BRI1-EMS SUPPRESSOR 1/BRASSINAZOLE RESISTANT 1) family of transcription factors that modulate thousands of target genes. Arabodopsis thaliana homeodomain-leucine zipper protein 1 (HAT1), which encodes a homeodomain-leucine zipper (HD-Zip) class II transcription factor, was identified through chromatin immunoprecipitation (ChIP) experiments as a direct target gene of BES1. Loss-of-function and gain-of-function mutants of HAT1 display altered BR responses. HAT1 and its close homolog HAT3 act redundantly, as the double mutant hat1 hat3 displayed a reduced BR response that is stronger than the single mutants alone. Moreover, hat1 hat3 enhanced the phenotype of a weak allele of the BR receptor mutant bri1 and suppressed the phenotype of constitutive BR response mutant bes1-D. These results suggest that HAT1 and HAT3 function to activate BR-mediated growth. Expression levels of several BR-repressed genes are increased in hat1 hat3 and reduced in HAT1OX, suggesting that HAT1 functions to repress the expression of a subset of BR target genes. HAT1 and BES1 bind to a conserved homeodomain binding (HB) site and BR response element (BRRE) respectively, in the promoters of some BR-repressed genes. BES1 and HAT1 interact with each other and cooperate to inhibit BR-repressed gene expression. Furthermore, HAT1 can be phosphorylated and stabilized by GSK3 (GLYCOGEN SYNTHASE KINASE 3)-like kinase BIN2 (BRASSINOSTEROID-INSENSITIVE 2), a well established negative regulator of the BR pathway. Our results thus revealed a previously unknown mechanism by which BR signaling modulates BR-repressed gene expression and coordinates plant growth.

Keywords: Arabidopsis thaliana; BES1; BIN2; HAT1; HAT3; brassinosteroids; phosphorylation; transcription repression.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / cytology
  • Arabidopsis / enzymology
  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Base Sequence
  • Brassinosteroids / metabolism*
  • DNA-Binding Proteins
  • Gene Expression
  • Gene Expression Regulation, Plant*
  • Genes, Reporter
  • Hypocotyl / cytology
  • Hypocotyl / enzymology
  • Hypocotyl / genetics
  • Hypocotyl / physiology
  • Molecular Sequence Data
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phenotype
  • Phosphorylation
  • Plant Growth Regulators / metabolism
  • Plants, Genetically Modified
  • Promoter Regions, Genetic / genetics
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Seedlings / cytology
  • Seedlings / enzymology
  • Seedlings / genetics
  • Seedlings / physiology
  • Signal Transduction*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • BES1 protein, Arabidopsis
  • Brassinosteroids
  • DNA-Binding Proteins
  • Nuclear Proteins
  • Plant Growth Regulators
  • Transcription Factors
  • AT1G79000 protein, Arabidopsis
  • Protein Kinases
  • BIN2 protein, Arabidopsis