DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements

Persistent Link:
http://hdl.handle.net/10150/614757
Title:
DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements
Author:
Wang, Jun; Yu, Yeisoo; Tao, Feng; Zhang, Jianwei; Copetti, Dario; Kudrna, Dave; Talag, Jayson; Lee, Seunghee; Wing, Rod A.; Fan, Chuanzhu
Affiliation:
Univ Arizona, Arizona Genom Inst, Inst BIO5; Univ Arizona, Sch Plant Sci
Issue Date:
2016-05-06
Publisher:
BIOMED CENTRAL LTD
Citation:
DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements 2016, 17 (1) Genome Biology
Journal:
Genome Biology
Rights:
© 2016 Wang et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/).
Collection Information:
This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu.
Abstract:
Background: Mutator-like transposable elements, a class of DNA transposons, exist pervasively in both prokaryotic and eukaryotic genomes, with more than 10,000 copies identified in the rice genome. These elements can capture ectopic genomic sequences that lead to the formation of new gene structures. Here, based on whole-genome comparative analyses, we comprehensively investigated processes and mechanisms of the evolution of putative genes derived from Mutator-like transposable elements in ten Oryza species and the outgroup Leersia perieri, bridging similar to 20 million years of evolutionary history. Results: Our analysis identified thousands of putative genes in each of the Oryza species, a large proportion of which have evidence of expression and contain chimeric structures. Consistent with previous reports, we observe that the putative Mutator-like transposable element-derived genes are generally GC-rich and mainly derive from GC-rich parental sequences. Furthermore, we determine that Mutator-like transposable elements capture parental sequences preferentially from genomic regions with low methylation levels and high recombination rates. We explicitly show that methylation levels in the internal and terminated inverted repeat regions of these elements, which might be directed by the 24-nucleotide small RNA-mediated pathway, are different and change dynamically over evolutionary time. Lastly, we demonstrate that putative genes derived from Mutator-like transposable elements tend to be expressed in mature pollen, which have undergone de-methylation programming, thereby providing a permissive expression environment for newly formed/transposable element-derived genes. Conclusions: Our results suggest that DNA methylation may be a primary mechanism to facilitate the origination, survival, and regulation of genes derived from Mutator-like transposable elements, thus contributing to the evolution of gene innovation and novelty in plant genomes.
ISSN:
1474-760X
DOI:
10.1186/s13059-016-0954-8
Keywords:
Comparative genomics; DNA methylation; GC content; Molecular evolution; MULEs; New genes; Oryza; Recombination rate
Version:
Final published version
Sponsors:
The project was funded by a start-up fund from Wayne State University to CF; RAW was supported by the National Science Foundation Plant Genome Program ( grant number 1026200), the Bud Antle Endowed Chair of Excellence in Agriculture, and the AXA Chair for Evolutionary Genomic and Genome Biology.
Additional Links:
http://genomebiology.biomedcentral.com/articles/10.1186/s13059-016-0954-8

Full metadata record

DC FieldValue Language
dc.contributor.authorWang, Junen
dc.contributor.authorYu, Yeisooen
dc.contributor.authorTao, Fengen
dc.contributor.authorZhang, Jianweien
dc.contributor.authorCopetti, Darioen
dc.contributor.authorKudrna, Daveen
dc.contributor.authorTalag, Jaysonen
dc.contributor.authorLee, Seungheeen
dc.contributor.authorWing, Rod A.en
dc.contributor.authorFan, Chuanzhuen
dc.date.accessioned2016-06-24T22:46:06Z-
dc.date.available2016-06-24T22:46:06Z-
dc.date.issued2016-05-06-
dc.identifier.citationDNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements 2016, 17 (1) Genome Biologyen
dc.identifier.issn1474-760X-
dc.identifier.doi10.1186/s13059-016-0954-8-
dc.identifier.urihttp://hdl.handle.net/10150/614757-
dc.description.abstractBackground: Mutator-like transposable elements, a class of DNA transposons, exist pervasively in both prokaryotic and eukaryotic genomes, with more than 10,000 copies identified in the rice genome. These elements can capture ectopic genomic sequences that lead to the formation of new gene structures. Here, based on whole-genome comparative analyses, we comprehensively investigated processes and mechanisms of the evolution of putative genes derived from Mutator-like transposable elements in ten Oryza species and the outgroup Leersia perieri, bridging similar to 20 million years of evolutionary history. Results: Our analysis identified thousands of putative genes in each of the Oryza species, a large proportion of which have evidence of expression and contain chimeric structures. Consistent with previous reports, we observe that the putative Mutator-like transposable element-derived genes are generally GC-rich and mainly derive from GC-rich parental sequences. Furthermore, we determine that Mutator-like transposable elements capture parental sequences preferentially from genomic regions with low methylation levels and high recombination rates. We explicitly show that methylation levels in the internal and terminated inverted repeat regions of these elements, which might be directed by the 24-nucleotide small RNA-mediated pathway, are different and change dynamically over evolutionary time. Lastly, we demonstrate that putative genes derived from Mutator-like transposable elements tend to be expressed in mature pollen, which have undergone de-methylation programming, thereby providing a permissive expression environment for newly formed/transposable element-derived genes. Conclusions: Our results suggest that DNA methylation may be a primary mechanism to facilitate the origination, survival, and regulation of genes derived from Mutator-like transposable elements, thus contributing to the evolution of gene innovation and novelty in plant genomes.en
dc.description.sponsorshipThe project was funded by a start-up fund from Wayne State University to CF; RAW was supported by the National Science Foundation Plant Genome Program ( grant number 1026200), the Bud Antle Endowed Chair of Excellence in Agriculture, and the AXA Chair for Evolutionary Genomic and Genome Biology.en
dc.language.isoenen
dc.publisherBIOMED CENTRAL LTDen
dc.relation.urlhttp://genomebiology.biomedcentral.com/articles/10.1186/s13059-016-0954-8en
dc.rights© 2016 Wang et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/).en
dc.subjectComparative genomicsen
dc.subjectDNA methylationen
dc.subjectGC contenten
dc.subjectMolecular evolutionen
dc.subjectMULEsen
dc.subjectNew genesen
dc.subjectOryzaen
dc.subjectRecombination rateen
dc.titleDNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elementsen
dc.typeArticleen
dc.contributor.departmentUniv Arizona, Arizona Genom Inst, Inst BIO5en
dc.contributor.departmentUniv Arizona, Sch Plant Scien
dc.identifier.journalGenome Biologyen
dc.description.collectioninformationThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
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