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Divergent evolution of CHD3 proteins resulted in MOM1 refining epigenetic control in vascular plants.

Caikovski M, Yokthongwattana C, Habu Y, Nishimura T, Mathieu O, Paszkowski J - PLoS Genet. (2008)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Plant Genetics, University of Geneva, Geneva, Switzerland.

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.

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Related in: MedlinePlus

MOM1 and PKL together contribute to the control of TGS.(A) Schematic comparison of predicted protein domains of MOM1, PKL and PtMOM1 (color code as in Figure 1). (B) Northern blot showing levels of TSI transcripts of four wild-type plants (WT) and five plants of each mutant strain; pkl, mom1 and mom1pkl double mutant. Below the blot: ethidium bromide-stained RNA gel used for the blotting as a loading control.
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pgen-1000165-g004: MOM1 and PKL together contribute to the control of TGS.(A) Schematic comparison of predicted protein domains of MOM1, PKL and PtMOM1 (color code as in Figure 1). (B) Northern blot showing levels of TSI transcripts of four wild-type plants (WT) and five plants of each mutant strain; pkl, mom1 and mom1pkl double mutant. Below the blot: ethidium bromide-stained RNA gel used for the blotting as a loading control.

Mentions: The sequence of PtMOM1 also predicts, in addition to an integral SNF2 domain with all six helicase motifs, the presence of a PHD finger and double chromodomains (Figure 1). The combination of PHD fingers, double chromodomains and an SNF2 domain is a distinctive feature of CHD3 proteins (Chromodomain-Helicase-DNA binding) [14]; noticeably plant CHD3-like proteins retained only a single PHD finger domain. The intact SNF2 domain is critical for the silencing function of CHD3 proteins. The long life-span of poplar and continuous production of “ancient” gametes is thought to reduce significantly the speed of genome evolution compared with Arabidopsis (estimated at six times) [11]. Therefore, PtMOM1 presumably reflects a more ancient sequence arrangement than those of the Arabidopsis or rice MOM1 proteins and the presence of all CHD3 domains in PtMOM1 provides strong support for an evolutionary link between MOM1 and CHD3 proteins (Figures 1, 4 and Figure S4). PtMOM1structural features were also found in SmMOM1 (Figure 1) providing additional support to this conclusion.


Divergent evolution of CHD3 proteins resulted in MOM1 refining epigenetic control in vascular plants.

Caikovski M, Yokthongwattana C, Habu Y, Nishimura T, Mathieu O, Paszkowski J - PLoS Genet. (2008)

MOM1 and PKL together contribute to the control of TGS.(A) Schematic comparison of predicted protein domains of MOM1, PKL and PtMOM1 (color code as in Figure 1). (B) Northern blot showing levels of TSI transcripts of four wild-type plants (WT) and five plants of each mutant strain; pkl, mom1 and mom1pkl double mutant. Below the blot: ethidium bromide-stained RNA gel used for the blotting as a loading control.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2507757&req=5

pgen-1000165-g004: MOM1 and PKL together contribute to the control of TGS.(A) Schematic comparison of predicted protein domains of MOM1, PKL and PtMOM1 (color code as in Figure 1). (B) Northern blot showing levels of TSI transcripts of four wild-type plants (WT) and five plants of each mutant strain; pkl, mom1 and mom1pkl double mutant. Below the blot: ethidium bromide-stained RNA gel used for the blotting as a loading control.
Mentions: The sequence of PtMOM1 also predicts, in addition to an integral SNF2 domain with all six helicase motifs, the presence of a PHD finger and double chromodomains (Figure 1). The combination of PHD fingers, double chromodomains and an SNF2 domain is a distinctive feature of CHD3 proteins (Chromodomain-Helicase-DNA binding) [14]; noticeably plant CHD3-like proteins retained only a single PHD finger domain. The intact SNF2 domain is critical for the silencing function of CHD3 proteins. The long life-span of poplar and continuous production of “ancient” gametes is thought to reduce significantly the speed of genome evolution compared with Arabidopsis (estimated at six times) [11]. Therefore, PtMOM1 presumably reflects a more ancient sequence arrangement than those of the Arabidopsis or rice MOM1 proteins and the presence of all CHD3 domains in PtMOM1 provides strong support for an evolutionary link between MOM1 and CHD3 proteins (Figures 1, 4 and Figure S4). PtMOM1structural features were also found in SmMOM1 (Figure 1) providing additional support to this conclusion.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Plant Genetics, University of Geneva, Geneva, Switzerland.

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.

Show MeSH
Related in: MedlinePlus