Unique, Shared, and Redundant Roles for theArabidopsisSWI/SNF Chromatin Remodeling ATPases BRAHMA and SPLAYED

Abstract

Chromatin remodeling is emerging as a central mechanism for patterning and differentiation in multicellular eukaryotes. SWI/SNF chromatin remodeling ATPases are conserved in the animal and plant kingdom and regulate transcriptional programs in response to endogenous and exogenous cues. In contrast with their metazoan orthologs, null mutants in two Arabidopsis thaliana SWI/SNF ATPases, BRAHMA (BRM) and SPLAYED (SYD), are viable, facilitating investigation of their role in the organism. Previous analyses revealed that syd and brm null mutants exhibit both similar and distinct developmental defects, yet the functional relationship between the two closely related ATPases is not understood. Another central question is whether these proteins act as general or specific transcriptional regulators. Using global expression studies, double mutant analysis, and protein interaction assays, we find overlapping functions for the two SWI/SNF ATPases. This partial diversification may have allowed expansion of the SWI/SNF ATPase regulatory repertoire, while preserving essential ancestral functions. Moreover, only a small fraction of all genes depends on SYD or BRM for expression, indicating that these SWI/SNF ATPases exhibit remarkable regulatory specificity. Our studies provide a conceptual framework for understanding the role of SWI/SNF chromatin remodeling in regulation of Arabidopsis development.

Genetic analysis of functional redundancy of BRM ATPase and ATSWI3C subunits of Arabidopsis SWI/SNF chromatin remodelling complexes

“…The BRM transcript level was 1.5-fold higher than that of ATSWI3C in all organs. These results were also consistent with a previous RT-PCR study of ATSWI3C transcript levels by Bezhani et al (2007).…”

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

“…Furthermore, BRM was shown to repress ABSCISIC ACID INSENSITIVE5, a key positive regulator of ABA signaling, by binding to its promoter and regulating ABA-dependent nucleosome rearrangement . Although BRM and SYD are thought to perform partially overlapping functions, SYD interacts preferentially with the SWI3A and B core subunits, a binding partner of FCA required for FLC expression, whereas the binding partners of BRM in the SWI/SNF core are SWI3B and SWI3C (Sarnowski et al, 2002;Bezhani et al, 2007). For the majority of target genes showing altered transcription in SWI/ SNF subunit mutants, the composition of SWI/SNF complexes and their interacting transcription factor partners are thus far unknown.…”

“…This indicated that similarly to the BRM, SYD, and SWI3 subunits of SWI/SNF complexes (Sarnowski et al, 2005;Bezhani et al, 2007;Archacki et al, 2009), their associated SWP73 factors are likely involved in the control of vegetative-to-generative phase transition and/or regulation of floral homeotic genes. In fact, analogously to BRM, which was found to control the transcription of flowering time repressor FLC (Farrona et al, 2011), Jégu et al (2014 reported recently that SWP73B modulates chromatin loop formation at the FLC locus.…”

“…SWI/SNF, consisting of an SNF2 ATPase, two SWI3s, and an SNF5 subunit, is capable of nucleosome disruption through facilitation of reversible transition between normal (inaccessible) and altered (more accessible) conformations (Narlikar et al, 2002). In Arabidopsis thaliana, SWI/SNF complexes are involved in modulating various developmental and regulatory processes, including both vegetative and generative development, flowering time, and hormonal signaling (Sarnowski et al, 2005;Bezhani et al, 2007;Han et al, 2012;Archacki et al, 2013;Efroni et al, 2013;Sarnowska et al, 2013;Vercruyssen et al, 2014).…”

The BAF60 Subunit of the SWI/SNF Chromatin-Remodeling Complex Directly Controls the Formation of a Gene Loop at FLOWERING LOCUS C in Arabidopsis

“…Nevertheless, several components of these complexes are evolutionarily conserved in plants, such as the SWI3 subunits (Sarnowski et al, 2005), the SNF5/BSH subunit (Brzeski et al, 1999), the nuclear actin-related protein ARP4 , BRAHMA (BRM), or SPLAYED (SYD). Both of these latter proteins are ATPases of Arabidopsis SWI/SNF complexes and have been shown to participate in the control of flower development and flowering time (Wagner and Meyerowitz, 2002;Farrona et al, 2004;Hurtado et al, 2006;Bezhani et al, 2007;Fornara et al, 2010;Wu, 2012). Likewise, the SWI3B protein interacts with the flowering regulator FCA (Sarnowski et al, 2005).…”