Arabidopsis SWI/SNF chromatin remodeling complex binds both promoters and terminators to regulate gene expression

Abstract

ATP-dependent chromatin remodeling complexes are important regulators of gene expression in Eukaryotes. In plants, SWI/SNF-type complexes have been shown critical for transcriptional control of key developmental processes, growth and stress responses. To gain insight into mechanisms underlying these roles, we performed whole genome mapping of the SWI/SNF catalytic subunit BRM in Arabidopsis thaliana, combined with transcript profiling experiments. Our data show that BRM occupies thousands of sites in Arabidopsis genome, most of which located within or close to genes. Among identified direct BRM transcriptional targets almost equal numbers were up- and downregulated upon BRM depletion, suggesting that BRM can act as both activator and repressor of gene expression. Interestingly, in addition to genes showing canonical pattern of BRM enrichment near transcription start site, many other genes showed a transcription termination site-centred BRM occupancy profile. We found that BRM-bound 3΄ gene regions have promoter-like features, including presence of TATA boxes and high H3K4me3 levels, and possess high antisense transcriptional activity which is subjected to both activation and repression by SWI/SNF complex. Our data suggest that binding to gene terminators and controlling transcription of non-coding RNAs is another way through which SWI/SNF complex regulates expression of its targets.

The histone variant H2A.Z and chromatin remodeler BRAHMA act coordinately and antagonistically to regulate transcription and nucleosome dynamics in Arabidopsis

“…Both H2A.Z and BRM contribute to transcriptional repression and transcriptional activation, but it is unknown how the role of one factor at a gene might affect the role of the other in transcriptional regulation. (Marques et al ., ; Archacki et al ., ). To identify the genes in Arabidopsis that are transcriptionally regulated by BRM and H2A.Z, we performed RNA sequencing (RNA‐seq) experiments.…”

“…From this point on in the study, we focused our analysis on the DE BRM and H2A.Z target genes and considered their transcription to be directly regulated by H2A.Z and/or BRM. Collectively, the defined DE target genes support the notion that both BRM and H2A.Z contribute to gene repression and activation in different contexts (Marques et al ., ; Archacki et al ., ).…”

“…We identified 2109 genes that were DE in arp6 (1036 genes upregulated and 1073 genes downregulated), 4250 genes DE in brm (2317 genes up and 1933 genes down), and 3203 genes DE in arp6;brm mutants (1517 genes up and 1686 genes down) (Figure S1b, summarized in Table S1). The gene sets we defined as DE in arp6‐1 and brm‐1 overlap significantly with those defined in previous studies (Archacki et al ., ; Sura et al ., ). Gene Ontology terms that were overrepresented among DE genes in each mutant were largely associated with responses to biotic and abiotic stress (Table S2).…”

Genome‐wide occupancy of histone H3K27 methyltransferases CURLY LEAF and SWINGER in Arabidopsis seedlings

“…In that work we demonstrated that the chromatin remodeler BRM could promote gene expression by limiting the deposition of H3K27me3 through suppressing the recruitment and/or the activity of CLF/SWN. Therefore, to find out whether the lack of H3K27me3 deposition is due to the presence of BRM, we checked the BRM occupancy at those CLF/SWN targets (Archacki et al., ; Li et al., ). Indeed, we saw nearly half of these genes (63 out of 136) were bound by BRM as well (Supporting Information ).…”

Seed germination and dormancy: The classic story, new puzzles, and evolution

“…The genomic region of DOG1 that differentiates shDOG1 and lgDOG1 (2nd intron/3rd exon) contains a promoter in the antisense orientation, which drives asDOG1 expression (Fedak et al ) (Figure ). The expression of antisense RNA from terminator regions may be a common phenomenon (Lin et al ; Archacki et al ). In the case of DOG1 , the expression of asDOG1 negatively regulates sense DOG1 expression, presumably through transcriptional control (possible mechanisms summarized in Nonogaki ) and reduces seed dormancy (Fedak et al ).…”