Abstract
Arabidopsis MOM1 is required for the heritable maintenance of transcriptional gene silencing (TGS). Unlike many other silencing factors, depletion of MOM1 evokes transcription at selected loci without major changes in DNA methylation or histone modification. These loci retain unusual, bivalent chromatin properties, intermediate to both euchromatin and heterochromatin. The structure of MOM1 previously suggested an integral nuclear membrane protein with chromatin-remodeling and actin-binding activities. Unexpected results presented here challenge these presumed MOM1 activities and demonstrate that less than 13% of MOM1 sequence is necessary and sufficient for TGS maintenance. This active sequence encompasses a novel Conserved MOM1 Motif 2 (CMM2). The high conservation suggests that CMM2 has been the subject of strong evolutionary pressure. The replacement of Arabidopsis CMM2 by a poplar motif reveals its functional conservation. Interspecies comparison suggests that MOM1 proteins emerged at the origin of vascular plants through neo-functionalization of the ubiquitous eukaryotic CHD3 chromatin remodeling factors. Interestingly, despite the divergent evolution of CHD3 and MOM1, we observed functional cooperation in epigenetic control involving unrelated protein motifs and thus probably diverse mechanisms.
Highlights
transcriptional gene silencing (TGS) heritably suppresses transcription of repetitive elements, transgenes and chromosomal genes and is generally associated with repressive histone marks and hypermethylation of DNA
We provide evidence that the two proteins are still able to cooperate in the control of TGS, despite the divergent evolution associated with the creation of a novel, MOM1-specific gene silencing domain and the degeneration of domains essential for CHD3 function
MOM1 Has Three Novel, Conserved Motifs Earlier homology searches with MOM1 identified no other conserved sequences than the SNF2 domain and an actin-binding region [8]
Summary
TGS heritably suppresses transcription of repetitive elements, transgenes and chromosomal genes and is generally associated with repressive histone marks and hypermethylation of DNA. Transcriptionally silent or active states of chromatin are thought to be regulated by changes in DNA and by modifications of histones. Contradicting this general view, mom mutations release silencing without obvious changes in DNA methylation, histone modification or degree of chromatin condensation [2,3]. A MOM1-specific subset of silencing targets has chromatin properties intermediate between hetero- and euchromatin. Silent these genes are poised for activation [6]. Mammalian epigenetic regulators responsible for controlling the transcriptional status of the intermediate chromatin have not been identified and MOM1 is the only example so far of a regulator determining the transcriptional status of targets associated with bivalent epigenetic marks
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