SWP73 Subunits of Arabidopsis SWI/SNF Chromatin Remodeling Complexes Play Distinct Roles in Leaf and Flower Development

Abstract

(T.J.S.)Arabidopsis thaliana SWP73A and SWP73B are homologs of mammalian BRAHMA-associated factors (BAF60s) that tether SWITCH/SUCROSE NONFERMENTING chromatin remodeling complexes to transcription factors of genes regulating various cell differentiation pathways. Here, we show that Arabidopsis thaliana SWP73s modulate several important developmental pathways. While undergoing normal vegetative development, swp73a mutants display reduced expression of FLOWERING LOCUS C and early flowering in short days. By contrast, swp73b mutants are characterized by retarded growth, severe defects in leaf and flower development, delayed flowering, and male sterility. MNase-Seq, transcript profiling, and ChIP-Seq studies demonstrate that SWP73B binds the promoters of ASYMMETRIC LEAVES1 and 2, KANADI1 and 3, and YABBY2, 3, and 5 genes, which regulate leaf development and show coordinately altered transcription in swp73b plants. Lack of SWP73B alters the expression patterns of APETALA1, APETALA3, and the MADS box gene AGL24, whereas other floral organ identity genes show reduced expression correlating with defects in flower development. Consistently, SWP73B binds to the promoter regions of APETALA1 and 3, SEPALLATA3, LEAFY, UNUSUAL FLORAL ORGANS, TERMINAL FLOWER1, AGAMOUS-LIKE24, and SUPPRESSOR OF CONSTANS OVEREXPRESSION1 genes, and the swp73b mutation alters nucleosome occupancy on most of these loci. In conclusion, SWP73B acts as important modulator of major developmental pathways, while SWP73A functions in flowering time control.

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

“…We demonstrate that BRM localizes to NDRs across the genome and is flanked by well positioned nucleosomes whose stability can depend on BRM (Figures S6 and ). These results expand on previous locus‐specific studies by both finding that well positioned nucleosomes surrounding BRM binding sites is a general genomic trend and that the stability of many of these flanking nucleosomes depends on BRM (Sacharowski et al ., ; Wu et al ., ). Since the BAF60 subunit of the SWI2/SNF2 complex has been observed localizing to open chromatin, we provide further evidence that the SWI2/SNF2 complex binds to NDRs by finding that the BRM SWI2/SNF2 ATPase also binds to NDRs (Jegu et al ., ).…”

“…As locus-specific studies have described roles for BRM and other SWI2/SNF2 subunits in nucleosome positioning and destabilization, we decided to quantify how often genomic BRM sites are associated with different types of nucleosome dynamics (Han et al 2015;Sacharowski et al, 2015;Wu et al, 2015;Brzezinka et al, 2016). Using DAN-POS2 software, nucleosomes were defined as dynamic if they had significant changes in nucleosome positioning (different position of nucleosome read summits), occupancy (different height of nucleosome read summits), fuzziness (difference in the standard deviation of nucleosome read positions), or any combination of the three in mutants relative to nucleosomes in WT tissue (Chen et al, 2013).…”

“…However, H2A.Z and/or BRM may have more consistent roles in chromatin regulation through interactions with specific transcription factors (TFs). Some previously reported interactions between either H2A.Z or BRM and TFs prompted us to evaluate how H2A.Z and BRM might contribute to nucleosome organization surrounding TF binding sites where they co-localize (John et al, 2008;Wu, 2012;Efroni et al, 2013;Vercruyssen et al, 2014;Sacharowski et al, 2015;Zhao and Garcia, 2015;Buszewicz et al, 2016;Cortijo et al, 2017;Jegu et al, 2017;Zhang et al, 2017a).…”

“…BRM also antagonizes the silencing function of the Polycomb Repressive Complex 2 (Li et al, 2015). Additionally, interchanging subunits of the SWI2/SNF2 complex can confer unique functions to modulate specific developmental processes (Vercruyssen et al, 2014;Sacharowski et al, 2015). This could mean that some of the variability in BRM's role in chromatin regulation could correspond with the SWI2/SNF2 subunits to which it co-localizes.…”

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

“…Since locus specific studies have described roles for BRM and other SWI2/SNF2 subunits in nucleosome positioning and destabilization, we decided to quantify how often BRM is associated with different types of nucleosome dynamics Wu et al, 2015;Brzezinka et al, 2016;Sacharowski et al, 2015). Using DANPOS2 software, nucleosomes were defined as dynamic if they had significant changes in nucleosome positioning (different position of nucleosome read summits), occupancy (different height of nucleosome read summits), fuzziness (difference in the standard deviation of nucleosome read positions), or any combination of the three in mutants relative to nucleosomes in WT tissue (Chen et al, 2013).…”