Genome‐wide occupancy of Arabidopsis SWI/SNF chromatin remodeler SPLAYED provides insights into its interplay with its close homolog BRAHMA and Polycomb proteins

Abstract

SUMMARY SPLAYED (SYD) is a SWItch/Sucrose Non‐Fermentable (SWI/SNF)‐type chromatin remodeler identified in Arabidopsis thaliana (Arabidopsis). It is believed to play both redundant and differential roles with its closest homolog BRAHMA (BRM) in diverse plant growth and development processes. To better understand how SYD functions, we profiled the genome‐wide occupancy of SYD and its impact on the global transcriptome and trimethylation of histone H3 on lysine 27 (H3K27me3). To map the global occupancy of SYD, we generated a GFP‐tagged transgenic line and used it for chromatin immunoprecipitation experiments followed by next‐generation sequencing, by which more than 6000 SYD target genes were identified. Through integrating SYD occupancy and transcriptome profiles, we found that SYD preferentially targets to nucleosome‐free regions of expressed genes. Further analysis revealed that SYD occupancy peaks exhibit five distinct patterns, which were also shared by BRM and BAF60, a conserved SWI/SNF complex component, indicating the common target sites of these SWI/SNF chromatin remodelers and the functional relevance of such distinct patterns. To investigate the interplay between SYD and Polycomb‐group (PcG) proteins, we performed a genome‐wide analysis of H3K27me3 in syd‐5. We observed both increases and decreases in H3K27me3 levels at a few hundred genes in syd‐5 compared to wild type. Our results imply that SYD can act antagonistically or synergistically with PcG at specific genes. Together, our SYD genome‐wide occupancy data and the transcriptome and H3K27me3 profiles provide a much‐needed resource for dissecting SYD’s crucial roles in the regulation of plant growth and development.

The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and 5’ transcript length determination in Arabidopsis

“…The fact that TPF contains 3xPHD and Tudor domains, previously shown to interact with methylated and acetylated histones (49,50,78), makes these two histone marks likely direct targets of TPF proteins to promote recruitment or stability of the complex on target sites. On the contrary, the complex was not found over facultative or constitutive heterochromatic regions, similar to what was observed for BRM and SYD targets, indicating that plant SWI/SNF complexes do not normally localize to these regions (38,39,76). Interestingly, BRM and SYD have been shown to play antagonistic and synergistic interactions with the Polycomb complex, responsible for the deposition of the facultative heterochromatic mark H3K27me3 (79–81).…”

“…This location is shared by other SWI/SNF chromatin remodeling proteins in animals, and fungi (74,75). Studies of the genomic location of the BRM and SYD ATPases revealed their location over TSS regions of many genes (38,39,76), pointing to their colocalization with the BAF-like complex. An open question is whether there is functional crosstalk between the plant BAF-like and ncBAF-like complexes over shared targets.…”

“…However, previously reported functional redundancy between BRM and SYD (40) supports its presence in ncBAF-like. BRM and SYD ATPases were also found over more distal promoter regions and downstream genic regions (39,42,76). Indeed, BRM participates over the 3´ regions of genes to regulate antisense transcription (77).…”

Histone modifications and chromatin remodelling in plants in response to salt stress

“…Immunoprecipitation of BRM‐GFP successfully isolated the subunits of the SWI/SNF complex in A. thaliana , including SWP73A, SWP73B, SWI3A, SWI3B, SWI3C, SWI3D, and SYD (Li et al, 2016). ChIP‐seq also demonstrated that SYD and BRM targeted a common set of genes under normal conditions (Shu et al, 2021).…”

Multiple functions of SWI/SNF chromatin remodeling complex in plant-pathogen interactions

“…Meanwhile, SYD functions antagonistically with MOS1 and MOS9 at the chromatin level to regulate SNC1 transcription and SNC1-mediated immunity (Johnson et al 2015). Strikingly, the expression levels of SYD were found to be dramatically decreased upon indoleacetic acid (IAA), ABA, and benzothiadiazole (BTH) treatments and increased upon flg22 treatment, which suggests that SYD responds to pathogen attack at the transcription level (Shu et al 2021).…”