Genome-wide and single-base resolution DNA methylomes of the Pacific oyster Crassostrea gigas provide insight into the evolution of invertebrate CpG methylation

BMC Genomics

Guofan Zhang⁴  Ximing Guo²  Xiaodong Fang¹  Huayong Que⁴  Jie Meng⁴  Fucun Wu⁴  Linlin Zhang⁴  Haigang Qi⁴  Fei Xu⁴  Huimin Cai¹  Lijun Jin³  Li Li⁴  Jinmin Lian³  Qiye Li⁵  Xiaotong Wang⁴ 

[1] BGI-Shenzhen, Shenzhen, China;Haskin Shellfish Research Laboratory, Institute of Marine and Coastal Sciences, Rutgers University, Port Norris, NJ 08349, USA;China National GeneBank, BGI-Shenzhen, Shenzhen, China;Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China;Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

关键词: Gene age;    Genome-wide;    DNA methylation;    Crassostrea gigas;    Oyster;    Mollusca;   

Others  :  1127223
DOI  :  10.1186/1471-2164-15-1119

 received in 2014-07-15, accepted in 2014-12-09,  发布年份 2014

【 摘 要 】

Background

Studies of DNA methylomes in a wide range of eukaryotes have revealed both conserved and divergent characteristics of DNA methylation among phylogenetic groups. However, data on invertebrates particularly molluscs are limited, which hinders our understanding of the evolution of DNA methylation in metazoa. The sequencing of the Pacific oyster Crassostrea gigas genome provides an opportunity for genome-wide profiling of DNA methylation in this model mollusc.

Results

Homologous searches against the C. gigas genome identified functional orthologs for key genes involved in DNA methylation: DNMT1, DNMT2, DNMT3, MBD2/3 and UHRF1. Whole-genome bisulfite sequencing (BS-seq) of the oyster’s mantle tissues revealed that more than 99% methylation modification was restricted to cytosines in CpG context and methylated CpGs accumulated in the bodies of genes that were moderately expressed. Young repeat elements were another major targets of CpG methylation in oysters. Comparison with other invertebrate methylomes suggested that the 5’-end bias of gene body methylation and the negative correlation between gene body methylation and gene length were the derived features probably limited to the insect lineage. Interestingly, phylostratigraphic analysis showed that CpG methylation preferentially targeted genes originating in the common ancestor of eukaryotes rather than the oldest genes originating in the common ancestor of cellular organisms.

Conclusions

Comparative analysis of the oyster DNA methylomes and that of other animal species revealed that the characteristics of DNA methylation were generally conserved during invertebrate evolution, while some unique features were derived in the insect lineage. The preference of methylation modification on genes originating in the eukaryotic ancestor rather than the oldest genes is unexpected, probably implying that the emergence of methylation regulation in these 'relatively young’ genes was critical for the origin and radiation of eukaryotes.

【 授权许可】

   
2014 Wang et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR: Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 2006, 126:1189-1201.
• [2]Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S: CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 2011, 479:74-79.
• [3]Bird AP: Gene number, noise reduction and biological complexity. Trends Genet 1995, 11:94-100.
• [4]Wolffe AP, Matzke MA: Epigenetics: regulation through repression. Science 1999, 286:481-486.
• [5]Zemach A, McDaniel IE, Silva P, Zilberman D: Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 2010, 328:916-919.
• [6]Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, Ukomadu C, Sadler KC, Pradhan S, Pellegrini M, Jacobsen SE: Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 2010, 107:8689-8694.
• [7]Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo Q-M: Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
• [8]Xiang H, Zhu J, Chen Q, Dai F, Li X, Li M, Zhang H, Zhang G, Li D, Dong Y, Zhao L, Lin Y, Cheng D, Yu J, Sun J, Zhou X, Ma K, He Y, Zhao Y, Guo S, Ye M, Guo G, Li Y, Li R, Zhang X, Ma L, Kristiansen K, Guo Q, Jiang J, Beck S, et al.: Single base-resolution methylome of the silkworm reveals a sparse epigenomic map. Nat Biotechnol 2010, 28:516-520.
• [9]Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R: The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 2010, 8:e1000506.
• [10]Bonasio R, Li Q, Lian J, Mutti NS, Jin L, Zhao H, Zhang P, Wen P, Xiang H, Ding Y, Jin Z, Shen SS, Wang Z, Wang W, Wang J, Berger SL, Liebig J, Zhang G, Reinberg D: Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr Biol 2012, 22:1755-1764.
• [11]Li Y, Zhu J, Tian G, Li N, Li Q, Ye M, Zheng H, Yu J, Wu H, Sun J, Zhang H, Chen Q, Luo R, Chen M, He Y, Jin X, Zhang Q, Yu C, Zhou G, Sun J, Huang Y, Zheng H, Cao H, Zhou X, Guo S, Hu X, Li X, Kristiansen K, Bolund L, Xu J, et al.: The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol 2010, 8:e1000533.
• [12]Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S: Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 2006, 39:61-69.
• [13]Yang X, Han H, De Carvalho DD, Lay FD, Jones PA, Liang G: Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell 2014, 26:577-590.
• [14]Gavery MR, Roberts SB: DNA methylation patterns provide insight into epigenetic regulation in the Pacific oyster (Crassostrea gigas). BMC Genomics 2010, 11:483. BioMed Central Full Text
• [15]Fneich S, Dheilly N, Adema C, Rognon A, Reichelt M, Bulla J, Grunau C, Cosseau C: 5-methyl-cytosine and 5-hydroxy-methyl-cytosine in the genome of Biomphalaria glabrata, a snail intermediate host of Schistosoma mansoni. Parasit Vectors 2013, 6:167. BioMed Central Full Text
• [16]Riviere G, Wu G-C, Fellous A, Goux D, Sourdaine P, Favrel P: DNA methylation is crucial for the early development in the oyster C. gigas. Marine Biotechnol 2013, 15:739-753.
• [17]Gavery MR, Roberts SB: Predominant intragenic methylation is associated with gene expression characteristics in a bivalve mollusc. Peer J 2013, 1:e215.
• [18]Sun Y, Hou R, Fu X, Sun C, Wang S, Wang C, Li N, Zhang L, Bao Z: Genome-wide analysis of DNA methylation in five tissues of Zhikong scallop, Chlamys farreri. PLoS One 2014, 9:e86232.
• [19]Fleury E, Huvet A, Lelong C, De Lorgeril J, Boulo V, Gueguen Y, Bachère E, Tanguy A, Moraga D, Fabioux C: Generation and analysis of a 29,745 unique Expressed Sequence Tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase. BMC Genomics 2009, 10:341. BioMed Central Full Text
• [20]Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H, Xiong Z, Que H, Xie Y, Holland PW, Paps J, Zhu Y, Wu F, Chen Y, Wang J, Peng C, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z, Zhu Q, Feng Y, Mount A, Hedgecock D, et al.: The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.
• [21]Olson CE, Roberts SB: Genome-wide profiling of DNA methylation and gene expression in Crassostrea gigas male gametes. Front Physiol 2014, 5:224.
• [22]Goll MG, Bestor TH: Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005, 74:481-514.
• [23]Law JA, Jacobsen SE: Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 2010, 11:204-220.
• [24]Hendrich B, Tweedie S: The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet 2003, 19:269-277.
• [25]Kennedy VS, Breisch LL: Maryland’s oysters: research and management. Maryland: University of Maryland College Park; 1981.
• [26]Suzuki MM, Bird A: DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008, 9:465-476.
• [27]Sarda S, Zeng J, Hunt BG, Yi SV: The evolution of invertebrate gene body methylation. Mol Biol Evol 2012, 29:1907-1916.
• [28]Foret S, Kucharski R, Pittelkow Y, Lockett GA, Maleszka R: Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genomics 2009, 10:472. BioMed Central Full Text
• [29]Domazet-Loso T, Brajkovic J, Tautz D: A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet 2007, 23:533-539.
• [30]Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, Chen Z, Childers CP, Glastad KM, Gokhale K, Gowin J, Gronenberg W, Hermansen RA, Hu H, Hunt BG, Huylmans AK, Khalil SM, Mitchell RD, Munoz-Torres MC, Mustard JA, Pan H, Reese JT, Scharf ME, Sun F, Vogel H, Xiao J, Yang W, Yang Z, Yang Z, Zhou J, et al.: Molecular traces of alternative social organization in a termite genome. Nat Commun 2014, 5:3636.
• [31]Gelfman S, Cohen N, Yearim A, Ast G: DNA-methylation effect on cotranscriptional splicing is dependent on GC architecture of the exon–intron structure. Genome Res 2013, 23:789-799.
• [32]Li-Byarlay H, Li Y, Stroud H, Feng S, Newman TC, Kaneda M, Hou KK, Worley KC, Elsik CG, Wickline SA, Jacobsen SE, Ma J, Robinson GE: RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee. Proc Natl Acad Sci U S A 2013, 110:12750-12755.
• [33]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
• [34]Birney E, Clamp M, Durbin R: GeneWise and Genomewise. Genome Res 2004, 14:988-995.
• [35]Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M: Pfam: the protein families database. Nucleic Acids Res 2014, 42:D222-D230.
• [36]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
• [37]Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628.
• [38]Robinson MD, Oshlack A: A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11:R25. BioMed Central Full Text
• [39]Hayatsu H, Tsuji K, Negishi K: Does urea promote the bisulfite-mediated deamination of cytosine in DNA? Investigation aiming at speeding-up the procedure for DNA methylation analysis. Nucleic Acids Symp Ser 2006, 50:69-70.
• [40]Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J: SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25:1966-1967.
• [41]Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I: Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001, 125:279-284.
• [42]Domazet-Loso T, Tautz D: Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa. BMC Biol 2010, 8:66. BioMed Central Full Text
• [43]Beißbarth T, Speed TP: GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 2004, 20:1464-1465.