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On the origin and evolutionary consequences of gene body DNA methylation
Sunday, 2016/08/14 | 06:04:56

Adam J. Bewick, Lexiang Ji, Chad E. Niederhuth, Eva-Maria Willing, Brigitte T. Hofmeister, Xiuling Shi, Li Wang, Zefu Lu, Nicholas A. Rohr, Benjamin Hartwig, Christiane Kiefer, Roger B. Deal, Jeremy Schmutz, Jane Grimwood, Hume Stroud, Steven E. Jacobsen, Korbinian Schneeberger, Xiaoyu Zhang, and Robert J. Schmitz

Significance

DNA methylation in plants is found at CG, CHG, and CHH sequence contexts. In plants, CG DNA methylation is enriched in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM) and shows correlations with several chromatin modifications. Contrary to other types of DNA methylation, the evolution and function of gbM are largely unknown. Here we show two independent concomitant losses of the DNA methyltransferase CHROMOMETHYLASE 3 (CMT3) and gbM without the predicted disruption of transcription and of modifications to chromatin. This result suggests that CMT3 is required for the establishment of gbM in actively transcribed genes, and that gbM is dispensable for normal transcription as well as for the composition and modification of plant chromatin.

Abstract

In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, to our knowledge the first instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum. Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM, supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z, and various histone modifications in E. salsugineum and in Arabidopsis thaliana epigenetic recombinant inbred lines found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modification of chromatin over evolutionary timescales.

 

See: http://www.pnas.org/content/113/32/9111.full

PNAS August 9 2016; vol.113; no.32: 9111–9116

 

Fig. 2.

Fig. 2. CMT3 is required for CHG DNA methylation and establishment of gbM in angiosperms. (A) Similar to E. salsugineum, loss of CMT3 in C. planisiliqua leads to genome-wide reductions of CHG DNA methylation at a per-site level. Closely related species that possess CMT3 maintain higher per-site CHG DNA methylation compared with C. planisiliqua. (B) The loss of CMT3 also causes the loss of gene body methylation in C. planisiliqua. (C) The loss of CMT3 (–) in E. salsugineum and C. planisiliqua represents two independent events separated by at least 13.5 My; loss of CMT3 in C. planisiliqua and E. salsugineum occurred within the last 27.41 and 40.92 My, respectively (20). However, loss in C. planisiliqua could be more recent, ≤12.27 My (20).

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