ABSTRACT
PICKLE (PKL) is a chromodomain helicase DNA-binding domain 3 (CHD3) chromatin remodeler that plays essential roles in controlling the gene expression patterns that determine developmental identity in plants, but the molecular mechanisms through which PKL is recruited to its target genes remain elusive. Here, we define a cis-motif and trans-acting factors mechanism that governs the genomic occupancy profile of PKL in Arabidopsis thaliana. We show that two homologous trans-factors VIVIPAROUS1/ABI3-LIKE1 (VAL1) and VAL2 physically interact with PKL in vivo, localize extensively to PKL-occupied regions in the genome, and promote efficient PKL recruitment at thousands of target genes, including those involved in seed maturation. Transcriptome analysis and genetic interaction studies reveal a close cooperation of VAL1/VAL2 and PKL in regulating gene expression and developmental fate. We demonstrate that this recruitment operates at two master regulatory genes, ABSCISIC ACID INSENSITIVE3 and AGAMOUS-LIKE 15, to repress the seed maturation program and ensure the seed-to-seedling transition. Together, our work unveils a general rule through which the CHD3 chromatin remodeler PKL binds to its target chromatin in plants.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Abscisic Acid/metabolism , Arabidopsis/genetics , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Chromatin/genetics , Chromatin/metabolism , DNA/metabolism , DNA Helicases/genetics , DNA Helicases/metabolism , Gene Expression Regulation, Plant/genetics , Seeds/genetics , Trans-Activators/metabolism , Transcription Factors/genetics , Transcription Factors/metabolismABSTRACT
Switch defective/sucrose non-fermentable (SWI/SNF) chromatin remodeling complexes are multi-subunit machines that play vital roles in the regulation of chromatin structure and gene expression. However, the mechanisms by which SWI/SNF complexes recognize their target loci in plants are not fully understood. Here, we show that the Arabidopsis thaliana bromodomain-containing proteins BRD1, BRD2, and BRD13 are core subunits of SWI/SNF complexes and critical for SWI/SNF genomic targeting. These three BRDs interact directly with multiple SWI/SNF subunits, including the BRAHMA (BRM) catalytic subunit. Phenotypic and transcriptomic analyses of the brd1 brd2 brd13 triple mutant revealed that these BRDs act largely redundantly to control gene expression and developmental processes that are also regulated by BRM. Genome-wide occupancy profiling demonstrated that these three BRDs extensively colocalize with BRM on chromatin. Simultaneous loss of function of three BRD genes results in reduced BRM protein levels and decreased occupancy of BRM on chromatin across the genome. Furthermore, we demonstrated that the bromodomains of BRDs are essential for genomic targeting of the BRD subunits of SWI/SNF complexes to their target sites. Collectively, these results demonstrate that BRD1, BRD2, and BRD13 are core subunits of SWI/SNF complexes and reveal their biological roles in facilitating genomic targeting of BRM-containing SWI/SNF complexes in plants.
