Mutations in two non‐canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects

Abstract

Summary SWI2/SNF2 chromatin remodeling ATPases play important roles in plant and metazoan development. While metazoans generally encode one or two SWI2/SNF2 ATPase genes, Arabidopsis encodes four such chromatin regulators: the well-studied BRAHMA and SPLAYED ATPases as well as two closely related non-canonical SWI2/SNF2 ATPases, CHR12 and CHR23. No developmental role has as yet been described for CHR12 and CHR23. Here we show that while strong single chr12 or chr23 mutants are morphologically indistinguishable from the wild type, chr12 chr23 double mutants cause embryonic lethality. The double mutant embryos fail to initiate root and shoot meristems and display few and aberrant cell division. Weak double mutant embryos give rise to viable seedlings with dramatic defects in the maintenance of both the shoot and the root stem cell populations. Paradoxically, the stem cell defects are correlated with increased expression of the stem cell markers WUSCHEL and WOX5. During subsequent development, the meristem defects are partially overcome to allow for the formation of very small, bushy adult plants. Based on the observed morphological defects we named the two chromatin remodelers MINUSCULE 1 and 2. Possible links between minu1 minu2 defects and defects in hormone signaling and replication-coupled chromatin assembly are discussed.

ANGUSTIFOLIA3 Binds to SWI/SNF Chromatin Remodeling Complexes to Regulate Transcription during Arabidopsis Leaf Development

“…Evolutionary conservation allowed for the description of various SWI/SNF complex subunits in Arabidopsis based on sequence similarity with metazoan subunits and include four SWI2/SNF2 ATPases (BRM, SPLAYED [SYD], MINU1/CHR12, and MINU2/ CHR23), four SWI3 proteins (SWI3A to SWI3D), two SWI/SNF ASSOCIATED PROTEINS 73 (SWP73A/CHC2 and SWP73B/ CHC1), two ACTIN RELATED PROTEINS predicted to belong to SWI/SNF complexes (ARP4 and ARP7), and a single protein termed BUSHY (BSH) (The Chromatin Database, www.chromdb.org; Meagher et al, 2005;Jerzmanowski, 2007;Kwon and Wagner, 2007;Sang et al, 2012). The complexes are assembled around one central ATPase, and differences in complex composition further result from the incorporation of distinct paralogous subunit family members and the more transient, often tissue-specific, interactions with other proteins like transcriptional coactivators and transcription factors (Clapier and Cairns, 2009;Hargreaves and Crabtree, 2011).…”

“…Mutation of BRM, SYD, SWI3C, and SWI3D and silencing of SWP73B, BSH, and ARP4 results in severely dwarfed plants that have reduced leaf and stem size, and perturbed flowering time and flower development, often leading to sterility (Brzeski et al, 1999;Wagner and Meyerowitz, 2002;Kandasamy et al, 2005b;Sarnowski et al, 2005;Hurtado et al, 2006;Crane and Gelvin, 2007). Moreover, loss of function of SWI3A, SWI3B, and ARP7 causes embryonic lethality, just as in the minu1 minu2 double mutation (Kandasamy et al, 2005a;Sarnowski et al, 2005;Sang et al, 2012). The molecular mechanisms by which the SWI/SNF complexes execute these roles are starting to be understood.…”

The SWI2/SNF2 Chromatin Remodeling ATPase BRAHMA Represses Abscisic Acid Responses in the Absence of the Stress Stimulus inArabidopsis

“…To investigate a possible link between SWI2/SNF2-dependent chromatin remodeling complexes and postgermination ABA responses, we probed the effect of mutations in each of the four Arabidopsis SWI2/SNF2 ATPases, SYD, BRM, MINU1, and MINU2 (Farrona et al, 2004;Flaus et al, 2006;Sang et al, 2012) on ABA-dependent growth arrest. Of all mutants tested, those in BRM displayed the most dramatic change in ABA sensitivity relative to the wild type (see Supplemental Figures 1A and 1B online).…”

“…SWI2/SNF2 subgroup ATPases are conserved from yeast to humans and plants (Flaus et al, 2006). Plant genomes contain three types of SWI2/SNF2 subgroup chromatin remodeling ATPases, which are called BRAHMA (BRM), SPLAYED (SYD), and MINUSCULE (MINU) (Flaus et al, 2006;Jerzmanowski, 2007;Kwon and Wagner, 2007;Sang et al, 2012). SWI2/SNF2 ATPases act in large protein complexes that are required for full activity in vivo and use the energy derived from ATP hydrolysis to alter histone-DNA interactions (Clapier and Cairns, 2009;Hargreaves and Crabtree, 2011).…”

Systems biology analysis of the WOX5 gene and its functions in the root stem cell niche

“…The bulk of WOX5 expression occurs in cells above the quiescent center but not in the quiescent center itself, where it is reduced (Sang et al, 2012) Transcription factors PHB and PHV Suppress WOX5 expression In se mutants, the expression level of mir165/166 is not sufficient to remove the PHB and PHV transcripts from the basal part of the embryo (Grigg et al, 2009). As a result, WOX5 expression is absent from this region SHR and SCR Activate WOX5 expression In shr and scr mutants, WOX5 expression is absent or not detected (Sarkar et al, 2007) Posttranscription and posttranslation regulation PRL1 Suppresses WOX5 expression in the meristematic zone…”