The SWI/SNF subunit SWI3B functions with the m6A writer complex to establish embryo patterning in Arabidopsis

Abstract

N6-methyladenosine (m6A) is the most abundant mRNA modification in eukaryotes and is essential for Arabidopsis embryogenesis. However, how m6A mRNA methylation is coordinated with other regulatory pathways during development including embryogenesis remains largely unknown. Here, we report the SWI/SNF chromatin-remodeling subunit SWI3B as a bona fide interactor of the m6A methyltransferase MTA. Like m6A writer mutants, SWI3B is required for early embryo development. We demonstrate that the interaction between MTA and SWI3B is required for MTA function during embryogenesis. MTA and SWI3B are both required to establish the correct expression pattern of WOX8 and proper auxin maxima during early embryogenesis. Transcriptome analysis of isolated embryos from mta, swi3b, and fip37 mutants identified a shared set of upregulated transcripts, including STM as well as several NAC and ERF transcription factors that are normally absent or expressed at very low levels during early embryogenesis. Embryo-specific overexpression of ANAC087 and ERF114 genes phenocopied early embryonic defects observed in mta and swi3b mutants, indicating that their ectopic expression contributes to the observed developmental phenotype. Moreover, SWI3B and MTA are both required for m6A deposition on specific developmental transcripts. Together, our findings uncover a mechanism by which chromatin remodeling and m6A-mediated RNA regulation cooperate to suppress the precocious stability of key developmental regulators, thereby contributing to the establishment of the transcriptional program required for early embryo patterning in Arabidopsis. HighlightsO_LIThe SWI/SNF subunit SWI3B is a functional interactor of the m6A methyltransferase MTA during Arabidopsis embryogenesis C_LIO_LISWI3B and MTA cooperate to establish embryo patterning, WOX8 expression, and auxin maxima C_LIO_LIMTA and SWI3B suppress precocious expression of STM, ANAC087 and ERF114 transcription factors that disrupt early embryo development C_LIO_LISWI3B links chromatin-associated regulation with m6A-mediated control of transcript stability C_LI Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=161 HEIGHT=200 SRC="FIGDIR/small/744595v1_ufig1.gif" ALT="Figure 1"> View larger version (39K): org.highwire.dtl.DTLVardef@1056f76org.highwire.dtl.DTLVardef@1d8b9d6org.highwire.dtl.DTLVardef@190918corg.highwire.dtl.DTLVardef@439ce1_HPS_FORMAT_FIGEXP M_FIG C_FIG