Gene body methylation is conserved between plant orthologs and is of evolutionary consequence

Proceedings of the National Academy of Sciences of the United States of America
Shohei Takuno, Brandon S Gaut

Abstract

DNA methylation is a common feature of eukaryotic genomes and is especially common in noncoding regions of plants. Protein coding regions of plants are often methylated also, but the extent, function, and evolutionary consequences of gene body methylation remain unclear. Here we investigate gene body methylation using an explicit comparative evolutionary approach. We generated bisulfite sequencing data from two tissues of Brachypodium distachyon and compared genic methylation patterns to those of rice (Oryza sativa ssp. japonica). Gene body methylation was strongly conserved between orthologs of the two species and affected a biased subset of long, slowly evolving genes. Because gene body methylation is conserved over evolutionary time, it shapes important features of plant genome evolution, such as the bimodality of G+C content among grass genes. Our results superficially contradict previous observations of high cytosine methylation polymorphism within Arabidopsis thaliana genes, but reanalyses of these data are consistent with conservation of methylation within gene regions. Overall, our results indicate that the methylation level is a long-term property of individual genes and therefore of evolutionary consequence.

References

Apr 11, 1980·Nucleic Acids Research·A P Bird
Dec 29, 2000·Nature·Arabidopsis Genome Initiative
Jul 23, 2004·Nature·Zachary LippmanRob Martienssen
Oct 7, 2004·Nature Structural & Molecular Biology·Matthew C LorinczMark Groudine
Jun 23, 2006·TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik·John P VogelDevin Coleman-Derr
Jun 21, 2007·PLoS Biology·Matthew W VaughnRobert A Martienssen
Dec 20, 2007·Nucleic Acids Research·Rice Annotation ProjectManuel Echeverria
Apr 23, 2009·The EMBO Journal·Felipe Karam Teixeira, Vincent Colot
Jul 28, 2009·Annual Review of Genomics and Human Genetics·Laurent Duret, Nicolas Galtier
Oct 24, 2009·Trends in Genetics : TIG·François RoudierVincent Colot
Dec 25, 2009·Bioinformatics·Elena Y HarrisStefano Lonardi
Feb 6, 2010·Science·Reini F LucoTom Misteli
Feb 10, 2010·Nature Reviews. Genetics·Julie A Law, Steven E Jacobsen
Feb 12, 2010·Nature·International Brachypodium Initiative
Apr 17, 2010·Science·Assaf ZemachDaniel Zilberman
Apr 17, 2010·Proceedings of the National Academy of Sciences of the United States of America·Suhua FengSteven E Jacobsen
May 18, 2010·BMC Genomics·Tatiana V TatarinovaKenneth A Feldmann
Jun 1, 2010·Nature·Ramakrishna K ChodavarapuMatteo Pellegrini
Jul 9, 2010·Nature·Alika K MaunakeaJoseph F Costello
Sep 14, 2010·The EMBO Journal·Soichi InagakiTetsuji Kakutani
Oct 6, 2010·Proceedings of the National Academy of Sciences of the United States of America·Mark A BeilsteinSarah Mathews
Oct 13, 2010·Proceedings of the National Academy of Sciences of the United States of America·Assaf ZemachDaniel Zilberman
Jan 15, 2011·Current Opinion in Plant Biology·Suhua Feng, Steven E Jacobsen
Mar 4, 2011·Proceedings of the National Academy of Sciences of the United States of America·James C SchnableMichael Freeling
Apr 1, 2011·Current Opinion in Plant Biology·Marie Mirouze, Jerzy Paszkowski
Aug 5, 2011·Molecular Biology and Evolution·Shohei Takuno, Brandon S Gaut
Oct 4, 2011·Nature·Sanjeev ShuklaShalini Oberdoerffer
Nov 8, 2011·Nature·Claude BeckerDetlef Weigel
Feb 15, 2012·Proceedings of the National Academy of Sciences of the United States of America·Ian K GreavesElizabeth S Dennis
Apr 12, 2012·The Plant Cell·Laurana Serres-GiardiSylvain Glémin
Jun 27, 2012·Proceedings of the National Academy of Sciences of the United States of America·Robert H DowenJoseph R Ecker
Oct 17, 2012·PLoS Genetics·Devin Coleman-Derr, Daniel Zilberman

Citations

Jun 12, 2014·Trends in Genetics : TIG·Sylvain GléminAdrienne Ressayre
Dec 21, 2013·Science·Amborella Genome Project
May 20, 2014·Integrative and Comparative Biology·Isabel MendizabalSoojin V Yi
Apr 9, 2014·Proceedings of the National Academy of Sciences of the United States of America·Thomas E Keller, Soojin V Yi
Feb 25, 2014·Briefings in Functional Genomics·Kyung Do KimScott A Jackson
Mar 22, 2014·Briefings in Functional Genomics·Todd P Michael
Aug 26, 2014·Annual Review of Genetics·Amanda K LaneRobert J Schmitz
Jan 21, 2016·Proceedings of the National Academy of Sciences of the United States of America·Mathew G LewseyJoseph R Ecker
Jun 2, 2016·Nature Plants·Shohei TakunoBrandon S Gaut
May 13, 2015·Proceedings of the National Academy of Sciences of the United States of America·Adriaan van der GraafFrank Johannes
Jan 7, 2016·Frontiers in Plant Science·Hirotomo Takatsuka, Masaaki Umeda
Mar 6, 2016·Journal of Experimental Botany·Andriy Bilichak, Igor Kovalchuk
Dec 12, 2013·Environmental and Molecular Mutagenesis·Klaas MensaertTim De Meyer
Apr 9, 2015·Molecular Genetics and Genomics : MGG·Xiupeng MeiYilin Cai
Jul 8, 2015·BMC Genomics·Jack M ColicchioLena C Hileman
Nov 26, 2013·Molecular Plant·Chad E Niederhuth, Robert J Schmitz
Aug 24, 2013·Molecular Plant·Qing-Xin SongJin-Song Zhang
Nov 26, 2013·Current Opinion in Genetics & Development·K Christin FalkeGregor Schmitz
Mar 13, 2014·Trends in Plant Science·M Yvonne Kim, Daniel Zilberman
Jan 16, 2014·Current Opinion in Plant Biology·Concepcion M DiezBrandon S Gaut
Feb 11, 2014·Biochemical and Biophysical Research Communications·Wangxiong HuHongzhi Li
Feb 19, 2015·Nature Protocols·Mark A UrichJoseph R Ecker
Mar 28, 2016·Genome Biology and Evolution·Jana AsselmanKarel A C De Schamphelaere
Dec 21, 2014·Genome Biology and Evolution·Yves ClémentSylvain Glémin
May 10, 2016·Nature Reviews. Genetics·Aaron TaudtFrank Johannes
May 18, 2016·Molecular Biology and Evolution·Groves DixonMikhail Matz
Sep 7, 2016·Trends in Plant Science·Blaise WeberMaike Stam
Sep 28, 2016·Genome Biology·Chad E NiederhuthRobert J Schmitz
Mar 24, 2017·Molecular Biology and Evolution·Shohei TakunoBrandon S Gaut
Jan 18, 2017·Proceedings of the National Academy of Sciences of the United States of America·Kim A SteigeTanja Slotte
Oct 17, 2017·Genome Biology and Evolution·Soojin V Yi
Nov 7, 2018·Molecular Biology and Evolution·Aline Muyle, Brandon S Gaut
Sep 21, 2016·G3 : Genes - Genomes - Genetics·Zaixuan ZhongShunping He
Jan 11, 2017·The EMBO Journal·Marco CatoniJerzy Paszkowski
Sep 11, 2019·Molecular Biology and Evolution·Danelle Seymour, Brandon S Gaut
May 13, 2020·International Journal of Molecular Sciences·Christoph C F SchinkelElvira Hörandl
May 13, 2017·Journal of Experimental Botany·Yun-Song LaiXixiang Li
May 23, 2018·Nature Reviews. Molecular Cell Biology·Huiming ZhangJian-Kang Zhu
Jul 31, 2019·Nature Plants·Frank Johannes
Feb 20, 2020·Proceedings of the National Academy of Sciences of the United States of America·Yinwen ZhangRobert J Schmitz
May 30, 2020·Integrative and Comparative Biology·Beth McCawLesley T Lancaster
Apr 28, 2017·Genome Biology·Colette L Picard, Mary Gehring
Oct 13, 2016·Annual Review of Genetics·Leandro Quadrana, Vincent Colot
Dec 22, 2016·Genome Biology·Amaryllis VidalisFrank Johannes
Oct 14, 2018·BMC Genomics·Jack M ColicchioLena C Hileman
Jun 4, 2020·The Plant Journal : for Cell and Molecular Biology·Daniel NiyikizaTarek Hewezi
Jul 13, 2016·Genome Biology and Evolution·Zi-Wen LiYa-Long Guo
Aug 5, 2017·Frontiers in Plant Science·Silvia FarinatiClaudio Bonghi
Jun 3, 2017·Scientific Reports·Xutong WangBao Liu
Nov 28, 2017·The Plant Journal : for Cell and Molecular Biology·Lin WangHaifeng Wang
Jul 10, 2018·DNA Research : an International Journal for Rapid Publication of Reports on Genes and Genomes·Satoshi TakahashiRyo Fujimoto
Jun 2, 2016·Nature Plants·Korbinian Schneeberger
Dec 21, 2016·Journal of Genetics·Pratima PandeyShashi Bhushan Tripathi
May 2, 2017·Genome Biology·Adam J BewickRobert J Schmitz
Oct 24, 2018·Frontiers in Plant Science·Katharina Bräutigam, Quentin Cronk
Jan 15, 2021·Current Opinion in Plant Biology·Eleanore J Ritter, Chad E Niederhuth
Nov 11, 2020·Molecular Plant·Aline MuyleAlexandros Bousios
Oct 16, 2020·Molecular Ecology Resources·Groves Dixon, Mikhail Matz
Mar 5, 2017·Current Opinion in Plant Biology·Adam J Bewick, Robert J Schmitz
Oct 17, 2017·Molecular Plant·Jered M Wendte, Robert J Schmitz
Apr 7, 2021·Nature Plants·Péter SzövényiFay-Wei Li

Related Concepts

G+C Composition
Rice (Dietary)
Unassigned Reading Frames
Genes, Plant
Arabidopsis thaliana <plant>
Genome, Plant
Evolution, Molecular
DNA Methylation
Chromosomes, Plant
Genetic Fitness

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