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Demethylation of ERECTA receptor genes by IBM1 histone demethylase affects stomatal development

DNA methylation and histone modifications interact to modulate gene expression in biological organisms. The histone demethylase IBM1 suppresses DNA methylation and gene silencing, primarily by targeting genic regions in the Arabidopsis genome. The chromatin regulator EDM2 is also required for prevention of genic DNA methylation because it maintains IBM1 expression by promoting IBM1 mRNA distal polyadenylation. Loss-of-function ibm1 and edm2 mutant plants display a wide range of developmental defects, but little is known about which developmentally important genes are regulated by IBM1 and EDM2. Here, we show that both ibm1 and edm2 mutants display defects in production of stomatal lineage cells, which is linked to DNA hypermethylation of the ERECTA family genes, including ER, ERL1 and ERL2. Stomatal phenotypes and DNA methylation levels of ER genes in ibm1 and edm2 mutants are restored by mutations in the genes encoding the histone methyltransferase KYP and DNA methyltransferase CMT3. Our data demonstrate that a specific plant developmental context is influenced by IBM1-regulated histone modification and DNA methylation on the gene body region of the ERECTA receptors. Summary: The histone demethylase IBM1 regulates Arabidopsis stomatal development by suppressing DNA methylation on the gene body region of ERECTA receptors.