The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants
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 r...
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| Format: | Article |
| Language: | English |
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BMC
2017-05-01
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| Series: | Genome Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s13059-017-1195-1 |
| _version_ | 1818265913998180352 |
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| author | Adam J. Bewick Chad E. Niederhuth Lexiang Ji Nicholas A. Rohr Patrick T. Griffin Jim Leebens-Mack Robert J. Schmitz |
| author_facet | Adam J. Bewick Chad E. Niederhuth Lexiang Ji Nicholas A. Rohr Patrick T. Griffin Jim Leebens-Mack Robert J. Schmitz |
| author_sort | Adam J. Bewick |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-12T19:58:22Z |
| format | Article |
| id | doaj.art-d5f095cbeff041e492681551754bf45e |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-12T19:58:22Z |
| publishDate | 2017-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-d5f095cbeff041e492681551754bf45e2022-12-22T00:13:50ZengBMCGenome Biology1474-760X2017-05-0118111310.1186/s13059-017-1195-1The evolution of CHROMOMETHYLASES and gene body DNA methylation in plantsAdam J. Bewick0Chad E. Niederhuth1Lexiang Ji2Nicholas A. Rohr3Patrick T. Griffin4Jim Leebens-Mack5Robert J. Schmitz6Department of Genetics, University of GeorgiaDepartment of Genetics, University of GeorgiaInstitute of Bioinformatics, University of GeorgiaDepartment of Genetics, University of GeorgiaDepartment of Genetics, University of GeorgiaDepartment of Plant Biology, University of GeorgiaDepartment of Genetics, University of GeorgiaAbstract 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.http://link.springer.com/article/10.1186/s13059-017-1195-1CHROMOMETHYLASEPhylogeneticsDNA methylationWhole-genome bisulfite sequencingWGBS |
| spellingShingle | Adam J. Bewick Chad E. Niederhuth Lexiang Ji Nicholas A. Rohr Patrick T. Griffin Jim Leebens-Mack Robert J. Schmitz The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants Genome Biology CHROMOMETHYLASE Phylogenetics DNA methylation Whole-genome bisulfite sequencing WGBS |
| title | The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants |
| title_full | The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants |
| title_fullStr | The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants |
| title_full_unstemmed | The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants |
| title_short | The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants |
| title_sort | evolution of chromomethylases and gene body dna methylation in plants |
| topic | CHROMOMETHYLASE Phylogenetics DNA methylation Whole-genome bisulfite sequencing WGBS |
| url | http://link.springer.com/article/10.1186/s13059-017-1195-1 |
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