Genome-wide and Caste-Specific DNA Methylomes of the Ants Camponotus floridanus and Harpegnathos saltator

被引:293
作者
Bonasio, Roberto [2 ,3 ]
Li, Qiye [5 ,6 ]
Lian, Jinmin [5 ]
Mutti, Navdeep S. [7 ]
Jin, Lijun [5 ]
Zhao, Hongmei [5 ]
Zhang, Pei [5 ]
Wen, Ping [5 ]
Xiang, Hui [8 ]
Ding, Yun [8 ]
Jin, Zonghui [5 ]
Shen, Steven S. [2 ,3 ,4 ]
Wang, Zongji [5 ,6 ]
Wang, Wen [8 ]
Wang, Jun [5 ,9 ,10 ]
Berger, Shelley L. [1 ]
Liebig, Juergen [7 ]
Zhang, Guojie [5 ]
Reinberg, Danny [2 ,3 ]
机构
[1] Univ Penn, Sch Med, Philadelphia, PA 19104 USA
[2] NYU, Sch Med, Howard Hughes Med Inst, New York, NY 10016 USA
[3] NYU, Sch Med, Dept Biochem, New York, NY 10016 USA
[4] NYU, Sch Med, Ctr Hlth Informat & Bioinformat, New York, NY 10016 USA
[5] BGI Shenzhen, Shenzhen 518083, Peoples R China
[6] S China Univ Technol, Sch Biosci & Bioengn, Guangzhou 510006, Guangdong, Peoples R China
[7] Arizona State Univ, Sch Life Sci, Tempe, AZ 85287 USA
[8] Chinese Acad Sci, State Key Lab Genet Resources & Evolut, Kunming Inst Zool, Kunming 650223, Yunnan, Peoples R China
[9] Univ Copenhagen, Dept Biol, DK-2100 Copenhagen, Denmark
[10] Univ Copenhagen, Novo Nordisk Fdn Ctr Basic Metab Res, DK-2100 Copenhagen, Denmark
关键词
CPG METHYLATION; INTRAGENOMIC CONFLICT; RNA; CONSERVATION; DIVERGENCE; PATTERNS; SYSTEM; PLANTS;
D O I
10.1016/j.cub.2012.07.042
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Background: Ant societies comprise individuals belonging to different castes characterized by specialized morphologies and behaviors. Because ant embryos can follow different developmental trajectories, epigenetic mechanisms must play a role in caste determination. Ants have a full set of DNA methyltransferases and their genomes contain methylcytosine. To determine the relationship between DNA methylation and phenotypic plasticity in ants, we obtained and compared the genome-wide methylonnes of different castes and developmental stages of Camponotus floridanus and Harpegnathos saltator. Results: In the ant genomes, methylcytosines are found both in symmetric CG dinucleotides (CpG) and non-CpG contexts and are strongly enriched at exons of active genes. Changes in exonic DNA methylation correlate with alternative splicing events such as exon skipping and alternative splice site selection. Several genes exhibit caste-specific and developmental changes in DNA methylation that are conserved between the two species, including genes involved in reproduction, telomere maintenance, and noncoding RNA metabolism. Several loci are methylated and expressed monoallelically, and in some cases, the choice of methylated allele depends on the caste. Conclusions: These first ant methylomes and their intra- and interspecies comparison reveal an exonic methylation pattern that points to a connection between DNA methylation and splicing. The presence of monoallelic DNA methylation and the methylation of non-CpG sites in all samples suggest roles in genome regulation in these social insects, including the intriguing possibility of parental or caste-specific genomic imprinting.
引用
收藏
页码:1755 / 1764
页数:10
相关论文
共 49 条
  • [1] Barlow D.P., 2007, EPIGENETICS
  • [2] PROCESS OF QUEEN-WORKER DIFFERENTIATION IN THE HONEYBEE
    BEETSMA, J
    [J]. BEE WORLD, 1979, 60 (01) : 24 - 39
  • [3] DNA methylation patterns and epigenetic memory
    Bird, A
    [J]. GENES & DEVELOPMENT, 2002, 16 (01) : 6 - 21
  • [4] Emerging topics in epigenetics: ants, brains, and noncoding RNAs
    Bonasio, Roberto
    [J]. BLAVATNIK AWARDS FOR YOUNG SCIENTISTS 2011, 2012, 1260 : 14 - 23
  • [5] Molecular Signals of Epigenetic States
    Bonasio, Roberto
    Tu, Shengjiang
    Reinberg, Danny
    [J]. SCIENCE, 2010, 330 (6004) : 612 - 616
  • [6] Genomic Comparison of the Ants Camponotus floridanus and Harpegnathos saltator
    Bonasio, Roberto
    Zhang, Guojie
    Ye, Chaoyang
    Mutti, Navdeep S.
    Fang, Xiaodong
    Qin, Nan
    Donahue, Greg
    Yang, Pengcheng
    Li, Qiye
    Li, Cai
    Zhang, Pei
    Huang, Zhiyong
    Berger, Shelley L.
    Reinberg, Danny
    Wang, Jun
    Liebig, Juergen
    [J]. SCIENCE, 2010, 329 (5995) : 1068 - 1071
  • [7] Intragenomic conflict over queen determination favours genomic imprinting in eusocial Hymenoptera
    Dobata, Shigeto
    Tsuji, Kazuki
    [J]. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2012, 279 (1738) : 2553 - 2560
  • [8] Conservation and divergence of methylation patterning in plants and animals
    Feng, Suhua
    Cokus, Shawn J.
    Zhang, Xiaoyu
    Chen, Pao-Yang
    Bostick, Magnolia
    Goll, Mary G.
    Hetzel, Jonathan
    Jain, Jayati
    Strauss, Steven H.
    Halpern, Marnie E.
    Ukomadu, Chinweike
    Sadler, Kirsten C.
    Pradhan, Sriharsa
    Pellegrini, Matteo
    Jacobsen, Steven E.
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (19) : 8689 - 8694
  • [9] DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees
    Foret, Sylvain
    Kucharski, Robert
    Pellegrini, Matteo
    Feng, Suhua
    Jacobsen, Steven E.
    Robinson, Gene E.
    Maleszka, Ryszard
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2012, 109 (13) : 4968 - 4973
  • [10] Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes
    Foret, Sylvain
    Kucharski, Robert
    Pittelkow, Yvonne
    Lockett, Gabrielle A.
    Maleszka, Ryszard
    [J]. BMC GENOMICS, 2009, 10 : 472