BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in arabidopsis

PLoS One. 2013;8(3):e58588. doi: 10.1371/journal.pone.0058588. Epub 2013 Mar 11.

Abstract

SWI/SNF chromatin remodeling complexes perform a pivotal function in the regulation of eukaryotic gene expression. Arabidopsis (Arabidopsis thaliana) mutants in major SWI/SNF subunits display embryo-lethal or dwarf phenotypes, indicating their critical role in molecular pathways controlling development and growth. As gibberellins (GA) are major positive regulators of plant growth, we wanted to establish whether there is a link between SWI/SNF and GA signaling in Arabidopsis. This study revealed that in brm-1 plants, depleted in SWI/SNF BRAHMA (BRM) ATPase, a number of GA-related phenotypic traits are GA-sensitive and that the loss of BRM results in markedly decreased level of endogenous bioactive GA. Transcriptional profiling of brm-1 and the GA biosynthesis mutant ga1-3, as well as the ga1-3/brm-1 double mutant demonstrated that BRM affects the expression of a large set of GA-responsive genes including genes responsible for GA biosynthesis and signaling. Furthermore, we found that BRM acts as an activator and directly associates with promoters of GA3ox1, a GA biosynthetic gene, and SCL3, implicated in positive regulation of the GA pathway. Many GA-responsive gene expression alterations in the brm-1 mutant are likely due to depleted levels of active GAs. However, the analysis of genetic interactions between BRM and the DELLA GA pathway repressors, revealed that BRM also acts on GA-responsive genes independently of its effect on GA level. Given the central position occupied by SWI/SNF complexes within regulatory networks controlling fundamental biological processes, the identification of diverse functional intersections of BRM with GA-dependent processes in this study suggests a role for SWI/SNF in facilitating crosstalk between GA-mediated regulation and other cellular pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Catalytic Domain
  • Chromatin Assembly and Disassembly*
  • Chromosomal Proteins, Non-Histone / chemistry
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / drug effects
  • Gibberellins / antagonists & inhibitors
  • Gibberellins / metabolism*
  • Molecular Sequence Annotation
  • Mutation
  • Phenotype
  • Plant Growth Regulators / metabolism*
  • Promoter Regions, Genetic
  • Quantitative Trait, Heritable
  • Signal Transduction / drug effects
  • Transcription Factors / chemistry
  • Transcription Factors / metabolism*
  • Triazoles / pharmacology

Substances

  • Arabidopsis Proteins
  • Chromosomal Proteins, Non-Histone
  • Gibberellins
  • Plant Growth Regulators
  • SWI-SNF-B chromatin-remodeling complex
  • Transcription Factors
  • Triazoles
  • paclobutrazol
  • Adenosine Triphosphatases
  • BRM protein, Arabidopsis

Grants and funding

This work was supported by Ministerstwo Nauki i Szkolnictwa Wyzszego (MNiSW) and National Science Centre grants: N N301 158735 and 2011/01/D/NZ1/01614 for AJ and RA, Marie Curie Reintegration Grant FP7-PEOPLE-2010-RG 268313 and W29/7. PR/2011 (MNiSW) for TJS, and Deutsche Forschunggemeinschaft–DFG-DA grant 1061/2-1 for SJD. URLs: (http://www.nauka.gov.pl/home/) (http://www.ncn.gov.pl/?language=en) (http://cordis.europa.eu/mariecurie-actions/home.html) (http://www.dfg.de/en/index.jsp). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.