Abstract
DNA methyltransferases (DNMTs) are an enzyme family that catalyzes the transfer of a methyl group to DNA for a wide variety of biological functions. To determine whether the number and composition of the Dnmt gene family affects the 5-methylcytosine (5mc) ratio at the genome level, genome-wide 5mc ratios from three marine animals, the mangrove killifish (Kryptolebias marmoratus), an intertidal copepod (Tigriopus japonicus), and a monogonont rotifer (Brachionus koreanus), were analyzed in each organism after the cloning of Dnmt genes. Lineage- and teleost-specific gene evolution was observed in the vertebrate Dnmt3 gene family, while unique gene expansion was found in the T. japonicus Dnmt1 gene family. However, the rotifer did not have any apparent homologue of Dnmt1 or Dnmt3 in its genome. This gene information was highly supportive of genome-wide 5mc levels in the three marine animals. Therefore, the absence or presence of the Dnmt gene family could be an important evolutionary parameter of how this could affect genome-wide epigenetic metabolism.
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Allen MD, Grummitt CG, Hilcenko C, Min SY, Tonkin LM, Johnson CM, Freund SM, Bycroft M, Warren AJ (2006) Solution structure of the nonmethyl-CpG-binding CXXC domain of the leukaemia-associated MLL histone methyltransferase. EMBO J 25:4503–4512
Bachman KE, Rountree MR, Baylin SB (2001) Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 276:32282–32287
Bañuelos S, Saraste M, Djinović Carugo K (1998) Structural comparisons of calponin homology domains: implications for actin binding. Structure 6:1419–1431
Bestor TH (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9:2395–2402
Callebaut I, Courvalin JC, Mornon JP (1999) The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation. FEBS Lett 446:189–193
Campos C, Valente LM, Fernandes JM (2012) Molecular evolution of zebrafish dnmt3 genes and thermal plasticity of their expression during embryonic development. Gene 500:93–100
Capuano F, Mülleder M, Kok R, Blom HJ, Ralser M (2014) Cytosine DNA methylation is found in Drosophila melanogaster but absent in Saccharomyces cerevisiae, Schizosaccharomyces pombe, and other yeast species. Anal Chem 86:3697–3702
Chen T, Ueda Y, Dodge JE, Wang Z, Li E (2003) Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol Cell Biol 23:5594–5605
Chen T, Mally A, Ozden S, Chipman JK (2010) Low doses of the carcinogen furan alter cell cycle and apoptosis gene expression in rat liver independent of DNA methylation. Environ Health Perspect 118:1597–1602
Cheng X (1995) Structure and function of DNA methyltransferases. Annu Rev Biophys Biomol Struct 24:293–318
Choi BJ, Yoon JH, Choi WS, Kim O, Nam SW, Lee JY, Park WS (2013) GKN1 and miR-185 are associated with CpG island methylator phenotype in gastric cancers. Mol Cell Toxicol 9:227–233
Gao F, Liu X, Wu XP, Wang XL, Gong D, Lu H, Xia Y, Song Y, Wang J, Du J, Liu S, Han X, Tang Y, Yang H, Jin Q, Zhang X, Liu M (2012) Differential DNA methylation in discrete developmental stages of the parasitic nematode Trichinella spiralis. Genome Biol 13:R100
Glastad KM, Hunt BG, Yi SV, Goodisman MA (2011) DNA methylation in insects: on the brink of the epigenomic era. Insect Mol Biol 20:553–565
Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481–514
Hung M-S, Karthikeyan N, Huang B, Koo HC, Kiger J, Shen CJ (1999) Drosophila proteins related to vertebrate DNA (5-cytosine) methyltransferases. Proc Natl Acad Sci USA 96:11940–11945
Hwang D-S, Suga K, Sakakura Y, Park HG, Hagiwara A, Rhee J-S, Lee J-S (2013) Complete mitochondrial genome of the monogonont rotifer, Brachionus koreanus (Rotifera, Brachionidae). Mitochondrial DNA 25:29–30
Hwang D-S, Lee B-Y, Kim H-S, Lee M-C, Kyung D-H, Om A-S, Rhee J-S, Lee J-S (2014) Genome-wide identification of nuclear receptor (NR) superfamily genes in the copepod Tigriopus japonicus. BMC Genomics 15:993
Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333:1300–1303
Iyer LM, Tahiliani M, Rao A, Aravind L (2009) Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle 8:1698–1710
Jabbari K, Cacciò S, Païs de Barros JP, Desgrès J, Bernardi G (1997) Evolutionary changes in CpG and methylation levels in the genome of vertebrates. Gene 205:109–118
Jaenisch R (1997) DNA methylation and imprinting: why bother? Trends Genet 13:323–329
Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33S:245–254
Jeltsch A, Nellen W, Lyko F (2006) Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem Sci 31:306–308
Jeong C-B, Kim B-M, Lee J-S, Rhee J-S (2014) Genome-wide identification of whole ATP-binding cassette (ABC) transporters in the intertidal copepod Tigriopus japonicus. BMC Genomics 15:651
Jeong C-B, Kim B-M, Choi H-J, Baek I, Souissi S, Park HG, Lee J-S, Rhee J-S (2015) Genome-wide identification and transcript profile of the whole cathepsin superfamily in the intertidal copepod Tigriopus japonicus. Dev Comp Immunol 53:1–12
Jung S-O, Lee Y-M, Park T-J, Park HG, Hagiwara A, Leung KMY, Dahms H-W, Lee W, Lee J-S (2006) The complete mitochondrial genome of the intertidal copepod Tigriopus sp. (Copepoda, Harpactidae) from Korea and phylogenetic considerations. J Exp Mar Biol Ecol 333:251–262
Khoddami V, Cairns BR (2013) Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 31:458–464
Kiani J, Grandjean V, Liebers R, Tuorto F, Ghanbarian H, Lyko F, Cuzin F, Rassoulzadegan M (2013) RNA-mediated epigenetic heredity requires the cytosine methyltransferase Dnmt2. PLoS Genet 9:e1003498
Kim H-S, Lee B-Y, Won E-J, Han J, Hwang D-S, Park HG, Lee J-S (2015) Identification of xenobiotic biodegradation and metabolism-related genes in the copepod Tigriopus japonicus whole transcriptome analysis. Mar Genomics. doi:10.1016/j.margen
Lee J-S, Rhee J-S, Kim R-O, Hwang D-S, Han J, Choi B-S, Park GS, Kim I-C, Park HG, Lee Y-M (2010) The copepod Tigriopus japonicus genomic DNA information (574 Mb) and molecular anatomy. Mar Environ Res 69:S21–S23
Lee J-S, Kim R-O, Rhee J-S, Han J, Hwang D-S, Choi B-S, Lee CJ, Yoon Y-D, Lim J-S, Lee Y-M, Park GS, Hagiwara A, Choi I-Y (2011) Sequence analysis of genomic DNA (680 Mb) by GS-FLX-Titanium sequencer in the monogonont rotifer Brachionus ibericus. Hydrobiologia 662:65–75
Lee B-Y, Kim H-S, Hwang D-S, Won E-J, Choi B-S, Choi I-Y, Park HG, Rhee J-S, Lee J-S (2015) Whole transcriptome analysis of the monogonont rotifer Brachionus koreanus provides molecular resources for developing biomarkers of carbohydrate metabolism. Comp Biochem Physiol D 14:33–41
Meyer A, Schartl M (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11:699–704
Ohno S (1970) Evolution by gene duplication. Springer, New York
Okano M, Xie S, Li E (1998) Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19:219–220
Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257
Raddatz G, Guzzardo PM, Olova N, Fantappié MR, Rampp M, Schaefer M, Reik W, Hannon GJ, Lyko F (2013) Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proc Natl Acad Sci USA 110:8627–8631
Rai K, Jafri IF, Chidester S, James SR, Karpf AR, Cairns BR, Jones DA (2010) Dnmt3 and G9a cooperate for tissue-specific development in zebrafish. J Biol Chem 285:4110–4121
Rhee J-S, Lee J-S (2014) Whole genome data for omics-based research on the self-fertilizing fish Kryptolebias marmoratus. Mar Pollut Bull 85:532–541
Rountree MR, Bachman KE, Baylin SB (2000) DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25:269–277
Tweedie S, Charlton J, Clark V, Bird A (1997) Methylation of genomes and genes at the invertebrate-vertebrate boundary. Mol Cell Biol 17:1469–1475
Urieli-Shoval S, Gruenbaum Y, Sedat J, Razin A (1982) The absence of detectable methylated bases in Drosophila melanogaster DNA. FEBS Lett 146:148–152
Vandegehuchte MB, Lemière F, Janssen CR (2009) Quantitative DNA-methylation in Daphnia magna and effects of multigeneration Zn exposure. Comp Biochem Physiol C 150:343–348
Varriale A, Bernardi G (2006) DNA methylation and body temperature in fishes. Gene 385:111–121
Wojciechowski M, Rafalski D, Kucharski R, Misztal K, Maleszka J, Bochtler M, Maleszka R (2014) Insights into DNA hydroxymethylation in the honeybee from in-depth analyses of TET dioxygenase. Open Biol 4:8
Yan H, Bonasio R, Simola DF, Liebig J, Berger SL, Reinberg D (2015) DNA methylation in social insects: how epigenetics can control behavior and longevity. Annu Rev Entomol 60:435–452
Yi S (2012) Birds do it, bees do it, worms and ciliates do it too: DNA methylation from unexpected corners of the tree of life. Genome Biol 13:174
Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919
Acknowledgments
We thank three anonymous reviewers for their helpful comments and also thank Prof. Hans-U. Dahms for his comments on the revised manuscript. This work was supported by a grant by the Marine Biotechnology Program (PJT200620, Genome analysis of marine organisms and development of functional application) funded by the Ministry of Oceans and Fisheries, Korea, to Jae-Seong Lee.
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The fish were reared in accordance with the Animal Welfare Ethical Committee of the Sungkyunkwan University.
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Kim, BM., Mirbahai, L., Mally, A. et al. Correlation between the DNA methyltransferase (Dnmt) gene family and genome-wide 5-methylcytosine (5mC) in rotifer, copepod, and fish. Genes Genom 38, 13–23 (2016). https://doi.org/10.1007/s13258-015-0333-y
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DOI: https://doi.org/10.1007/s13258-015-0333-y