Genome-Wide Identification of DNA Methylases and Demethylases in Kiwifruit (Actinidia chinensis)

DNA methylation plays an important role in a wide range of developmental and physiological processes in plants. It is primarily catalyzed and regulated by cytosine-5 DNA methyltransferases (C5-MTases) and a group of DNA glycosylases that act as demethylases. To date, no genome-scale analysis of the two kiwifruit (Actinidia chinensis) families has been undertaken. In our study, nine C5-MTases and seven DNA demethylase genes were identified in the kiwifruit genome. Through selective evolution analysis, we found that there were gene duplications in C5-MTases and demethylases, which may have arisen during three genome doubling events followed by selection during evolution of kiwifruit. Expression analysis of DNA methylases (C5-MTases) and demethylases identified changes in transcripts of DNA methylation and demethylation genes during both vegetative and reproductive development. Moreover, we found that some members of the two methylase/demethylase families may also be involved in fruit ripening and the regulation of softening. Our results help to better understand the complex roles of methylation/demethylation in plants and provide a foundation for analyzing the role of DNA methylation modification in kiwifruit growth, development and ripening.

[1]  R D Appel,et al.  Protein identification and analysis tools in the ExPASy server. , 1999, Methods in molecular biology.

[2]  Albert Jeltsch,et al.  Beyond Watson and Crick: DNA Methylation and Molecular Enzymology of DNA Methyltransferases , 2002, Chembiochem : a European journal of chemical biology.

[3]  R. R. Ariza,et al.  ROS1, a Repressor of Transcriptional Gene Silencing in Arabidopsis, Encodes a DNA Glycosylase/Lyase , 2002, Cell.

[4]  Kathleen Marchal,et al.  PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences , 2002, Nucleic Acids Res..

[5]  Owen J. Marshall.  PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR , 2004, Bioinform..

[6]  O. Mathieu,et al.  RNA-directed DNA methylation , 2004, Journal of Cell Science.

[7]  R. Fischer,et al.  Biology of chromatin dynamics. , 2005, Annual review of plant biology.

[8]  J. Pech,et al.  Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. , 2006, Plant & cell physiology.

[9]  R. Fischer,et al.  DNA Methylation Is Critical for Arabidopsis Embryogenesis and Seed Viability , 2006, The Plant Cell Online.

[10]  Jun Li,et al.  KaKs_Calculator: Calculating Ka and Ks Through Model Selection and Model Averaging , 2007, Genom. Proteom. Bioinform..

[11]  Jon Penterman,et al.  DEMETER DNA Glycosylase Establishes MEDEA Polycomb Gene Self-Imprinting by Allele-Specific Demethylation , 2006, Cell.

[12]  Robin Holliday,et al.  Epigenetics: A Historical Overview , 2006, Epigenetics.

[13]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[14]  F. Berger,et al.  DNA Methylation Causes Predominant Maternal Controls of Plant Embryo Growth , 2008, PloS one.

[15]  R. R. Ariza,et al.  Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks , 2008, Plant Molecular Biology.

[16]  Geoffrey J. Barton,et al.  Jalview Version 2—a multiple sequence alignment editor and analysis workbench , 2009, Bioinform..

[17]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[18]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[19]  Jian‐Kang Zhu.  Active DNA demethylation mediated by DNA glycosylases. , 2009, Annual review of genetics.

[20]  D. Zilberman,et al.  Genome-Wide Demethylation of Arabidopsis Endosperm , 2009, Science.

[21]  Torsten Schwede,et al.  Automated comparative protein structure modeling with SWISS‐MODEL and Swiss‐PdbViewer: A historical perspective , 2009, Electrophoresis.

[22]  Krystyna A. Kelly,et al.  The De Novo Cytosine Methyltransferase DRM2 Requires Intact UBA Domains and a Catalytically Mutated Paralog DRM3 during RNA–Directed DNA Methylation in Arabidopsis thaliana , 2010, PLoS genetics.

[23]  Pedro Silva,et al.  Local DNA hypomethylation activates genes in rice endosperm , 2010, Proceedings of the National Academy of Sciences.

[24]  Julie A. Law,et al.  Establishing, maintaining and modifying DNA methylation patterns in plants and animals , 2010, Nature Reviews Genetics.

[25]  Wei Lu,et al.  Identification of a Functional Genetic Variant at 16q12.1 for Breast Cancer Risk: Results from the Asia Breast Cancer Consortium , 2010, PLoS genetics.

[26]  Marco Biasini,et al.  Toward the estimation of the absolute quality of individual protein structure models , 2010, Bioinform..

[27]  Geoffrey J. Barton,et al.  Java bioinformatics analysis web services for multiple sequence alignment—JABAWS:MSA , 2011, Bioinform..

[28]  Geoffrey I. Webb,et al.  Efficient large-scale protein sequence comparison and gene matching to identify orthologs and co-orthologs , 2011, Nucleic acids research.

[29]  Jeremy D. DeBarry,et al.  MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity , 2012, Nucleic acids research.

[30]  Songnian Hu,et al.  EvolView, an online tool for visualizing, annotating and managing phylogenetic trees , 2012, Nucleic Acids Res..

[31]  Wei Tang,et al.  Draft genome of the kiwifruit Actinidia chinensis , 2013, Nature Communications.

[32]  S. Chen,et al.  Genome-wide analysis of DNA methylation in soybean. , 2013, Molecular plant.

[33]  Sean R. Eddy,et al.  nhmmer: DNA homology search with profile HMMs , 2013, Bioinform..

[34]  S. Zhong,et al.  Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening , 2013, Nature Biotechnology.

[35]  M. Matzke,et al.  RNA-directed DNA methylation: an epigenetic pathway of increasing complexity , 2014, Nature Reviews Genetics.

[36]  Yunbo Luo,et al.  Genome-wide identification of cytosine-5 DNA methyltransferases and demethylases in Solanum lycopersicum. , 2014, Gene.

[37]  Robert J. Schmitz,et al.  Covering your bases: inheritance of DNA methylation in plant genomes. , 2014, Molecular plant.

[38]  Peer Bork,et al.  SMART: recent updates, new developments and status in 2015 , 2014, Nucleic Acids Res..

[39]  J. Giovannoni,et al.  A DEMETER-like DNA demethylase governs tomato fruit ripening , 2015, Proceedings of the National Academy of Sciences.

[40]  Thomas J. Hardcastle,et al.  DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis , 2015, Genes & development.

[41]  Songnian Hu,et al.  Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees , 2016, Nucleic Acids Res..

[42]  S. Wan,et al.  Genome-Wide Identification and Comparative Analysis of Cytosine-5 DNA Methyltransferase and Demethylase Families in Wild and Cultivated Peanut , 2016, Front. Plant Sci..

[43]  T. Schwede,et al.  Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology , 2017, Scientific Reports.

[44]  S. Gori,et al.  A different vision of dyslexia: Local precedence on global perception , 2017, Scientific Reports.

[45]  Juan C. Sánchez-DelBarrio,et al.  DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. , 2017, Molecular biology and evolution.

[46]  Torsten Schwede,et al.  The SWISS-MODEL Repository—new features and functionality , 2016, Nucleic Acids Res..

[47]  Jian‐Kang Zhu,et al.  Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit , 2017, Proceedings of the National Academy of Sciences.

[48]  Torsten Schwede,et al.  SWISS-MODEL: homology modelling of protein structures and complexes , 2018, Nucleic Acids Res..

[49]  Yehua He,et al.  TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface , 2018 .

[50]  J. Elmore,et al.  Transcriptome profiles in peripheral white blood cells at the time of artificial insemination discriminate beef heifers with different fertility potential , 2018, BMC Genomics.

[51]  Charles David,et al.  A manually annotated Actinidia chinensis var. chinensis (kiwifruit) genome highlights the challenges associated with draft genomes and gene prediction in plants , 2018, BMC Genomics.

[52]  Sudhir Kumar,et al.  MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. , 2018, Molecular biology and evolution.

[53]  Z. Fei,et al.  A MYB/bHLH complex regulates tissue-specific anthocyanin biosynthesis in the inner pericarp of red-centered kiwifruit Actinidia chinensis cv. Hongyang. , 2019, The Plant journal : for cell and molecular biology.