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The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

Adam J. Bewick, Chad E. Niederhuth, Ji Lexiang, Nicholas A. Rohr, Patrick T. Griffin, Jim Leebens-Mack, Robert J. Schmitz
doi: https://doi.org/10.1101/054924
Adam J. Bewick
1Department of Genetics, University of Georgia, Athens, GA 30602, USA
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Chad E. Niederhuth
1Department of Genetics, University of Georgia, Athens, GA 30602, USA
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Ji Lexiang
2Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA
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Nicholas A. Rohr
1Department of Genetics, University of Georgia, Athens, GA 30602, USA
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Patrick T. Griffin
1Department of Genetics, University of Georgia, Athens, GA 30602, USA
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Jim Leebens-Mack
3Department of Plant Biology, University of Georgia, Athens, GA 30602, USA
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Robert J. Schmitz
1Department of Genetics, University of Georgia, Athens, GA 30602, USA
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ABSTRACT

Background The evolution of gene body methylation (gbM), its origins and its functional consequences are poorly understood. By pairing the largest collection of transcriptomes (>1000) and methylomes (77) across Viridiplantae we provide novel insights into the evolution of gbM and its relationship to CHROMOMETHYLASE (CMT) proteins.

Results CMTs are evolutionary conserved DNA methyltransferases in Viridiplantae. Duplication events gave rise to what are now referred to as CMT1, 2 and 3. Independent losses of CMT1, 2 and 3 in eudicots, CMT2 and ZMET in monocots and monocots/commelinids, variation in copy number and non-neutral evolution suggests overlapping or fluid functional evolution of this gene family. DNA methylation within genes is widespread and is found in all major taxonomic groups of Viridiplantae investigated. Genes enriched with methylated CGs (mCG) were also identified in species sister to angiosperms. The proportion of genes and DNA methylation patterns associated with gbM are restricted to angiosperms with a functional CMT3 or ortholog. However, mCG-enriched genes in the gymnosperm Pinus taeda shared some similarities with gbM genes in Amborella trichopoda. Additionally, gymnosperms and ferns share a CMT homolog closely related to CMT2 and 3. Hence, the dependency of gbM on a CMT most likely extends to all angiosperms and possibly gymnosperms and ferns.

Conclusions The resulting gene family phylogeny of CMT transcripts from the most diverse sampling of plants to date redefines our understanding of CMT evolution and its evolutionary consequences on DNA methylation. Future, functional tests of homologous and paralogous CMTs will uncover novel roles and consequences to the epigenome.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 31, 2017.
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The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants
Adam J. Bewick, Chad E. Niederhuth, Ji Lexiang, Nicholas A. Rohr, Patrick T. Griffin, Jim Leebens-Mack, Robert J. Schmitz
bioRxiv 054924; doi: https://doi.org/10.1101/054924
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The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants
Adam J. Bewick, Chad E. Niederhuth, Ji Lexiang, Nicholas A. Rohr, Patrick T. Griffin, Jim Leebens-Mack, Robert J. Schmitz
bioRxiv 054924; doi: https://doi.org/10.1101/054924

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