DNA methylation in insects: On the brink of the epigenomic era

Insect Molecular Biology

Volumn 20, Issue 5, 2011, Pages 553-565

  Glastad, K M ^a   Hunt, B G ^a   Yi, S V ^a   Goodisman, M A D ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

comparative genomics; DNA methylation; epigenetics

Indexed keywords

ANIMAL; DNA METHYLATION; EPIGENETICS; INSECT; METABOLISM; MOLECULAR EVOLUTION; REVIEW;

ANIMALS; DNA METHYLATION; EPIGENOMICS; EVOLUTION, MOLECULAR; INSECTS;

ANIMALIA; HEXAPODA; MAMMALIA; VERTEBRATA;

EID: 80052964166     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2011.01092.x     Document Type: Review

References (143)

1. Aapola, U., Liiv, I., and, Peterson, P., (2002) Imprinting regulator DNMT3L is a transcriptional repressor associated with histone deacetylase activity. Nucleic Acids Res 30: 3602-3608. (Pubitemid 34919216)
2. Albalat, R., (2008) Evolution of DNA-methylation machinery: DNA methyltransferases and methyl-DNA binding proteins in the amphioxus Branchiostoma floridae. Dev Genes Evol 218: 691-701.
3. Ast, G., (2004) How did alternative splicing evolve? Nat Rev Genet 5: 773-782. (Pubitemid 39336361)
4. Bai, S.M., Ghoshal, K., Datta, J., Majumder, S., Yoon, S.O., and, Jacob, S.T., (2005) DNA methyltransferase 3b regulates nerve growth factor-induced differentiation of PC12 cells by recruiting histone deacetylase 2. Mol Cell Biol 25: 751-766. (Pubitemid 40096595)
5. Barberan-Soler, S., and, Zahler, A.M., (2008) Alternative splicing regulation during C. elegans development: splicing factors as regulated targets. PLoS Genet 4: e1000001.
6. Barchuk, A.R., Cristino, A.S., Kucharski, R., Costa, L.F., Simoes, Z.L.P., and, Maleszka, R., (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol 7: 70.
7. Baylin, S.B., Herman, J.G., Graff, J.R., Vertino, P.M., and, Issa, J.P., (1998) Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res 72: 141-196. (Pubitemid 27435555)
8. Ben-Porath, I., and, Cedar, H., (2001) Epigenetic crosstalk. Mol Cell 8: 933-935. (Pubitemid 34031796)
9. Berger, S.L., Kouzarides, T., Shiekhattar, R., and, Shilatifard, A., (2009) An operational definition of epigenetics. Genes Dev 23: 781-783.
10. Bestor, T.H., (1990) DNA methylation-evolution of a bacterial immune function into a regulator of gene-expression and genome structure in higher eukaryotes. Philos Trans R Soc B Biol Sci 326: 179-187.
11. Bestor, T.H., (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9: 2395-2402.
12. Bird, A.P., (1980) DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res 8: 1499-1504.
13. Bird, A.P., (1995) Gene number, noise-reduction and biological complexity. Trends Genet 11: 94-100.
14. Bird, A.P., Taggart, M.H., and, Smith, B.A., (1979) Methylated and unmethylated DNA compartments in the sea urchin genome. Cell 17: 889-901. (Pubitemid 9252298)
15. Bock, C., and, Lengauer, T., (2008) Computational epigenetics. Bioinformatics 24: 1-10.
16. Bogdanovic, O., and, Veenstra, G.J.C., (2009) DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118: 549-565.
17. Bonasio, R., Tu, S., and, Reinberg, D., (2010a) Molecular signals of epigenetic states. Science 330: 612-616.
18. Bonasio, R., Zhang, G., Ye, C., Mutti, N.S., Fang, X., Qin, N., et al,. (2010b) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068-1071.
19. Boyes, J., and, Bird, A., (1991) DNA methylation inhibits transcription indirectly via a Methyl-cpg binding-protein. Cell 64: 1123-1134. (Pubitemid 121001199)
20. Chen, T.P., Ueda, Y., Dodge, J.E., Wang, Z.J., and, 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. (Pubitemid 36951325)
21. Cheong, J., Yamada, Y., Yamashita, R., Irie, T., Kanai, A., Wakaguri, H., et al,. (2006) Diverse DNA methylation statuses at alternative promoters of human genes in various tissues. DNA Res 13: 155-167. (Pubitemid 44726366)
22. Clouaire, T., and, Stancheva, I., (2008) Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin? Cell Mol Life Sci 65: 1509-1522.
23. Clouaire, T., Heras, J., Merusi, C., and, Stancheva, I., (2010) Recruitment of MBD1 to target genes requires sequence-specific interaction of the MBD domain with methylated DNA. Nucleic Acids Res 38: 4620-4634.
24. Colbourne, J.K., Pfrender, M.E., Gilbert, D., Thomas, W.K., Tucker, A., Oakley, T.H., et al,. (2011) The ecoresponsive genome of Daphnia pulex. Science 331: 555-561.
25. Duret, L., and, Mouchiroud, D., (2000) Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol Biol Evol 17: 68-74. (Pubitemid 30056993)
26. Ehrlich, M., Gamasosa, M.A., Huang, L.H., Midgett, R.M., Kuo, K.C., McCune, R.A., et al,. (1982) Amount and distribution of 5-methylcytosine in human DNA from different types of tissues or cells. Nucleic Acids Res 10: 2709-2721.
27. Elango, N., and, Yi, S.V., (2008) DNA methylation and structural and functional bimodality of vertebrate promoters. Mol Biol Evol 25: 1602-1608. (Pubitemid 352019845)
28. Elango, N., and, Yi, S.V., (2011) Functional relevance of CpG island length for regulation of gene expression. Genetics 187: 1077-1083.
29. Elango, N., Kim, S.H., Vigoda, E., and, Yi, S.V., (2008) Mutations of different molecular origins exhibit contrasting patterns of regional substitution rate variation. PLoS Comput Biol 4: e1000015.
30. Elango, N., Hunt, B.G., Goodisman, M.A.D., and, Yi, S.V., (2009) DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci USA 106: 11206-11211.
31. Evans, J.D., and, Wheeler, D.E., (2001) Gene expression and the evolution of insect polyphenisms. BioEssays 23: 62-68. (Pubitemid 32100502)
32. Fatemi, M., Pao, M.M., Jeong, S., Gal-Yam, E.N., Egger, G., Weisenberger, D.J., et al,. (2005) Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic Acids Res 33: e176.
33. Feng, Q., and, Zhang, Y., (2001) The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 15: 827-832. (Pubitemid 32295063)
34. Feng, S.H., Cokus, S.J., Zhang, X.Y., Chen, P.Y., Bostick, M., Goll, M.G., et al,. (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107: 8689-8694.
35. Field, L.M., (2000) Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). Biochem J 349: 863-868. (Pubitemid 30609419)
36. Field, L.M., Crick, S.E., and, Devonshire, A.L., (1996) Polymerase chain reaction-based identification of insecticide resistance genes and DNA methylation in the aphid Myzus persicae (Sulzer). Insect Mol Biol 5: 197-202. (Pubitemid 126439994)
37. Foret, S., Kucharski, R., Pittelkow, Y., Lockett, G.A., and, Maleszka, R., (2009) Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genomics 10: 472.
38. Fraga, M.F., Ballestar, E., Paz, M.F., Ropero, S., Setien, F., Ballestart, M.L., et al,. (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102: 10604-10609. (Pubitemid 41061601)
39. Fuks, F., Hurd, P.J., Deplus, R., and, Kouzarides, T., (2003) The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 31: 2305-2312. (Pubitemid 37442098)
40. Futscher, B.W., Oshiro, M.M., Wozniak, R.J., Holtan, N., Hanigan, C.L., Duan, H., et al,. (2002) Role for DNA methylation in the control of cell type-specific maspin expression. Nat Genet 31: 175-179.
41. Gaunt, M.W., and, Miles, M.A., (2002) An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19: 748-761. (Pubitemid 34521306)
42. Geiman, T.M., Sankpal, U.T., Robertson, A.K., Zhao, Y.X., Zhao, Y.M., and, Robertson, K.D., (2004) DNMT3B interacts with hSNF2H chromatin remodeling enzyme, HDACs 1 and 2, and components of the histone methylation system. Biochem Biophys Res Commun 318: 544-555. (Pubitemid 38553814)
43. Goll, M.G., and, Bestor, T.H., (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514. (Pubitemid 40995515)
44. Goll, M.G., Kirpekar, F., Maggert, K.A., Yoder, J.A., Hsieh, C.L., Zhang, X.Y., et al,. (2006) Methylation of tRNA(AsP) by the DNA methyltransferase homolog Dnmt2. Science 311: 395-398. (Pubitemid 43132667)
45. Grimaldi, D., and, Engel, M., (2005) Evolution of the Insects. Cambridge University Press, Cambridge.
46. Haig, D., (2000) The kinship theory of genomic imprinting. Annu Rev Ecol Syst 31: 9-32. (Pubitemid 32139451)
47. Haines, T.R., Rodenhiser, D.I., and, Ainsworth, P.J., (2001) Allele-specific non-CpG methylation of the Nf1 gene during early mouse development. Dev Biol 240: 585-598. (Pubitemid 34056513)
48. Hata, K., Okano, M., Lei, H., and, Li, E., (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129: 1983-1993. (Pubitemid 34874213)
49. Hendrich, B., and, Bird, A., (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18: 6538-6547. (Pubitemid 28500543)
50. Hendrich, B., and, Tweedie, S., (2003) The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet 19: 269-277. (Pubitemid 36507009)
51. Hung, M.S., Karthikeyan, N., Huang, B.L., Koo, H.C., Kiger, J., and, Shen, C.K.J., (1999) Drosophila proteins related to vertebrate DNA (5-cytosine) methyltransferases. Proc Natl Acad Sci USA 96: 11940-11945. (Pubitemid 29502837)
52. Hunt, B.G., Brisson, J.A., Yi, S.V., and, Goodisman, M.A.D., (2010) Functional conservation of DNA methylation in the pea aphid and the honeybee. Genome Biol Evol 2: 719-728.
53. Illingworth, R., Kerr, A., DeSousa, D., Jorgensen, H., Ellis, P., Stalker, J., et al,. (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6: e22.
54. International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8: e1000313.
55. Jablonka, E., and, Regev, A., (1995) Gene number, methylation and biological complexity. Trends Genet 11: 383-384.
56. Jaenisch, R., and, Bird, A., (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33: 245-254. (Pubitemid 36278835)
57. Jair, K.W., Bachman, K.E., Suzuki, H., Ting, A.H., Rhee, I., Yen, R.W.C., et al,. (2006) De novo CpG island methylation in human cancer cells. Cancer Res 66: 682-692. (Pubitemid 43165930)
58. Javierre, B.M., Fernandez, A.F., Richter, J., Al-Shahrour, F., Martin-Subero, J.I., Rodriguez-Ubreva, J., et al,. (2010) Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res 20: 170-179.
59. Jones, P.A., and, Baylin, S.B., (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428. (Pubitemid 34587077)
60. Jones, P.L., Veenstra, G.J.C., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N., et al,. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19: 187-191. (Pubitemid 28248804)
61. Jurkowski, T.P., Meusburger, M., Phalke, S., Helm, M., Nellen, W., Reuter, G., et al,. (2008) Human DNMT2 methylates tRNA(Asp) molecules using a DNA methyltransferase-like catalytic mechanism. RNA 14: 1663-1670.
62. Kangaspeska, S., Stride, B., Metivier, R., Polycarpou-Schwarz, M., Ibberson, D., Carmouche, R.P., et al,. (2008) Transient cyclical methylation of promoter DNA. Nature 452: 112-115. (Pubitemid 351355094)
63. Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., et al,. (2007) Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet 16: 2272-2280. (Pubitemid 47423893)
64. Kirkness, E.F., Haas, B.J., Sun, W., Braig, H.R., Perotti, M.A., Clark, J.M., et al,. (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 107: 12168-12173.
65. Klose, R.J., and, Bird, A.P., (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31: 89-97. (Pubitemid 43221841)
66. Krauss, V., Eisenhardt, C., and, Unger, T., (2009) The genome of the stick insect Medauroidea extradentata is strongly methylated within genes and repetitive DNA. PLoS One 4: e7223.
67. Kronauer, D.J.C., (2008) Genomic imprinting and kinship in the social Hymenoptera: what are the predictions? J Theor Biol 254: 737-740.
68. Kronforst, M.R., Gilley, D.C., Strassmann, J.E., and, Queller, D.C., (2008) DNA methylation is widespread across social Hymenoptera. Curr Biol 18: R287-R288. (Pubitemid 351458687)
69. Kucharski, R., Maleszka, J., Foret, S., and, Maleszka, R., (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830. (Pubitemid 351451590)
70. Li, E., Beard, C., and, Jaenisch, R., (1993) Role for DNA methylation in genomic imprinting. Nature 366: 362-365. (Pubitemid 23349366)
71. Li, Y.R., Zhu, J.D., Tian, G., Li, N., Li, Q.B., Ye, M.Z., et al,. (2010) The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol 8: e1000533.
72. Lister, R., Pelizzola, M., Dowen, R.H., Hawkins, R.D., Hon, G., Tonti-Filippini, J., et al,. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
73. Lockett, G.A., Helliwell, P., and, Maleszka, R., (2010) Involvement of DNA methylation in memory processing in the honey bee. Neuroreport 21: 812-816.
74. Lopezrodas, G., Brosch, G., Georgieva, E.I., Sendra, R., Franco, L., and, Loidl, P., (1993) Histone deacetylase-a key enzyme for the binding of regulatory proteins to chromatin. FEBS Lett 317: 175-180. (Pubitemid 23045784)
75. Lyko, F., Foret, S., Kucharski, R., Wolf, S., Falckenhayn, C., and, Maleszka, R., (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8: e1000506.
76. Maleszka, R., (2008) Epigenetic integration of environmental and genomic signals in honey bees. Epigenetics 3: 188-192.
77. Mandrioli, M., (2007) A new synthesis in epigenetics: towards a unified function of DNA methylation from invertebrates to vertebrates. Cell Mol Life Sci 64: 2522-2524. (Pubitemid 350035615)
78. Mandrioli, M., and, Volpi, N., (2003) The genome of the lepidopteran Mamestra brassicae has a vertebrate-like content of methyl-cytosine. Genetica 119: 187-191. (Pubitemid 37365118)
79. Marais, G., (2003) Biased gene conversion: implications for genome and sex evolution. Trends Genet 19: 330-338. (Pubitemid 36694616)
80. Margueron, R., and, Reinberg, D., (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11: 285-296.
81. Marhold, J., Rothe, N., Pauli, A., Mund, C., Kuehle, K., Brueckner, B., et al,. (2004) Conservation of DNA methylation in dipteran insects. Insect Mol Biol 13: 117-123. (Pubitemid 38522241)
82. Maunakea, A.K., Nagarajan, R.P., Bilenky, M., Ballinger, T.J., D'Souza, C., Fouse, S.D., et al,. (2010) Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466: 253-257.
83. Mayer, W., Niveleau, A., Walter, J., Fundele, R., and, Haaf, T., (2000) Embryogenesis-demethylation of the zygotic paternal genome. Nature 403: 501-502. (Pubitemid 30082186)
84. Merlo, A., Herman, J.G., Mao, L., Lee, D.J., Gabrielson, E., Burger, P.C., et al,. (1995) 5′ CpG island methylation is associated with transcriptional silencing of the tumor-suppressor p16/CDKN2/MTS1 in human cancers. Nat Med 1: 686-692.
85. Metivier, R., Gallais, R., Tiffoche, C., Le Peron, C., Jurkowska, R.Z., Carmouche, R.P., et al,. (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature 452: 45-50. (Pubitemid 351355084)
86. Miller, C.A., and, Sweatt, J.D., (2007) Covalent modification of DNA regulates memory formation. Neuron 53: 857-869. (Pubitemid 46367557)
87. Moczek, A.P., and, Snell-Rood, E.C., (2008) The basis of bee-ing different: the role of gene silencing in plasticity. Evol Dev 10: 511-513.
88. Monk, M., Boubelik, M., and, Lehnert, S., (1987) Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ-cell lineages during mouse embryo development. Development 99: 371-382. (Pubitemid 17048855)
89. Nasonia Genome Working Group (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343-348.
90. Okamura, K., Matsumoto, K., and, Nakai, K., (2010) Gradual transition from mosaic to global DNA methylation patterns during deuterostome evolution. BMC Bioinformatics 11: S2.
91. Okano, M., Bell, D.W., Haber, D.A., and, Li, E., (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257. (Pubitemid 29519904)
92. Okitsu, C.Y., and, Hsieh, C.L., (2007) DNA methylation dictates histone H3K4 methylation. Mol Cell Biol 27: 2746-2757. (Pubitemid 46581362)
93. O'Neill, R.J.W., O'Neill, M.J., and, Graves, J.A.M., (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68-72. (Pubitemid 28240255)
94. Ono, M., Swanson, J.J., Field, L.M., Devonshire, A.L., and, Siegfried, B.D., (1999) Amplification and methylation of an esterase gene associated with insecticide-resistance in greenbugs, Schizaphis graminum (Rondani) (Homoptera: Aphididae). Insect Biochem Mol Biol 29: 1065-1073.
95. Ooi, S.K.T., and, Bestor, T.H., (2008) The colorful history of active DNA demethylation. Cell 133: 1145-1148. (Pubitemid 351852922)
96. Ott, J., (1979) Detection of rare major genes in lipid-levels. Hum Genet 51: 79-91. (Pubitemid 9242115)
97. Pal, C., Papp, B., and, Lercher, M.J., (2006) An integrated view of protein evolution. Nat Rev Genet 7: 337-348.
98. Queller, D.C., (2003) Theory of genomic imprinting conflict in social insects. BMC Evol Biol 3: 23.
99. Rae, P.M.M., and, Steele, R.E., (1979) Absence of cytosine methylation at C-C-G-G and G-C-G-C sites in the rDNA coding regions and intervening sequences of Drosophila and the rDNA of other higher insects. Nucleic Acids Res 6: 2987-2995. (Pubitemid 9222557)
100. Regev, A., Lamb, M., and, Jablonka, E., (1998) The role of DNA methylation in invertebrates: developmental regulation or genome defense? Mol Biol Evol 15: 880-891. (Pubitemid 28321886)
101. Reik, W., and, Walter, J., (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2: 21-32. (Pubitemid 33674766)
102. Rountree, M.R., and, Selker, E.U., (1997) DNA methylation inhibits elongation but not initiation of transcription in Neurospora crassa. Genes Dev 11: 2383-2395. (Pubitemid 27408535)
103. Savard, J., Tautz, D., Richards, S., Weinstock, G.M., Gibbs, R.A., Werren, J.H., et al,. (2006) Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res 16: 1334-1338. (Pubitemid 44664675)
104. Saxonov, S., Berg, P., and, Brutlag, D.L., (2006) A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci USA 103: 1412-1417. (Pubitemid 43191179)
105. Schaefer, M., and, Lyko, F., (2010) Lack of evidence for DNA methylation of Invader4 retroelements in Drosophila and implications for Dnmt2-mediated epigenetic regulation. Nat Genet 42: 920-921.
106. Sharif, J., Endo, T.A., Toyoda, T., and, Koseki, H., (2010) Divergence of CpG island promoters: a consequence or cause of evolution? Dev Growth Differ 52: 545-554.
107. Shen, J.C., Rideout, W.M., and, Jones, P.A., (1994) The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucleic Acids Res 22: 972-976. (Pubitemid 24162157)
108. Shimizu, T.S., Takahashi, K., and, Tomita, M., (1997) CpG distribution patterns in methylated and non-methylated species. Gene 205: 103-107. (Pubitemid 28029603)
109. Simmen, M.W., Leitgeb, S., Charlton, J., Jones, S.J.M., Harris, B.R., Clark, V.H., et al,. (1999) Nonmethylated transposable elements and methylated genes in a chordate genome. Science 283: 1164-1167.
110. Simpson, V.J., Johnson, T.E., and, Hammen, R.F., (1986) Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucleic Acids Res 14: 6711-6719.
111. Smith, C.D., Zimin, A., Holt, C., Abouheif, E., Benton, R., Cash, E., et al,. (2011) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci USA 108: 5673-5678.
112. Smith, C.R., Toth, A.L., Suarez, A.V., and, Robinson, G.E., (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9: 735-748.
113. Smith, C.R., Smith, C.D., Robertson, H.M., Helmkampf, M., Zimin, A., Yandell, M., et al,. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108: 5667-5672.
114. Soma, S., and, Rao, S.R.V., (1992) 5-Methylcytosine content in Gryllotalpa fossor (Orthoptera). Genome 35: 163-166.
115. Strassmann, J.E., and, Queller, D.C., (2007) Insect societies as divided organisms: the complexities of purpose and cross-purpose. Proc Natl Acad Sci USA 104: 8619-8626. (Pubitemid 47175455)
116. Suen, G., Teiling, C., Li, L., Holt, C., Abouheif, E., Bornberg-Bauer, E., et al,. (2011) The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet 7: e1002007.
117. Suzuki, M.M., and, Bird, A., (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9: 465-476. (Pubitemid 351693975)
118. Suzuki, M.M., Kerr, A.R.W., De Sousa, D., and, Bird, A., (2007) CpG methylation is targeted to transcription units in an invertebrate genome. Genome Res 17: 625-631. (Pubitemid 46715513)
119. Tamaru, H., and, Selker, E.U., (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277-283. (Pubitemid 33097798)
120. Tribolium Genome Sequencing Consortium (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949-955.
121. Tweedie, S., Ng, H.H., Barlow, A.L., Turner, B.M., Hendrich, B., and, Bird, A., (1999) Vestiges of a DNA methylation system in Drosophila melanogaster? Nat Genet 23: 389-390.
122. Urieli-Shoval, S., Gruenbaum, Y., Sedat, J., and, Razin, A., (1982) The absence of detectable methylated bases in Drosophila melanogaster DNA. FEBS Lett 146: 148-152.
123. Vandegehuchte, M.B., Lemiere, F., and, Janssen, C.R., (2009) Quantitative DNA-methylation in Daphnia magna and effects of multigeneration Zn exposure. Comp Biochem Physiol C Toxicol Pharmacol 150: 343-348.
124. Vanyushin, F., (2005) Methylation of adenine residues in DNA of eukaryotes. Mol Biol 39: 557-566.
125. Vire, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., et al,. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874. (Pubitemid 43255707)
126. Walsh, T.K., Brisson, J.A., Robertson, H.M., Gordon, K., Jaubert-Possamai, S., Tagu, D., et al,. (2010) A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum. Insect Mol Biol 19: 215-228.
127. Wang, Y., and, Leung, F., (2009) In silico prediction of two classes of honeybee genes with CpG deficiency or CpG enrichment and sorting according to gene ontology classes. J Mol Evol 68: 700-705.
128. Wang, Y., Jorda, M., Jones, P.L., Maleszka, R., Ling, X., Robertson, H.M., et al,. (2006) Functional CpG methylation system in a social insect. Science 314: 645-647. (Pubitemid 44646387)
129. Watt, F., and, Molloy, P.L., (1988) Cytosine methylation prevents binding to DNA of a hela-cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 2: 1136-1143.
130. Weaver, N., (1966) Physiology of caste determination. Annu Rev Entomol 11: 79-102.
131. Weber, M., Hellmann, I., Stadler, M.B., Ramos, L., Paabo, S., Rebhan, M., et al,. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457-466. (Pubitemid 46514772)
132. Wheeler, D.E., (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128: 13-34.
133. Wilkins, J.F., and, Haig, D., (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4: 359-368. (Pubitemid 36538360)
134. Wolffe, A.P., and, Matzke, M.A., (1999) Epigenetics: regulation through repression. Science 286: 481-486.
135. Wu, S.C., and, Zhang, Y., (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11: 607-620.
136. Wurm, Y., Wang, J., Riba-Grognuz, O., Corona, M., Nygaard, S., Hunt, B.G., et al,. (2011) The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci USA 108: 5679-5684.
137. Xiang, H., Zhu, J.D., Chen, Q., Dai, F.Y., Li, X., Li, M.W., et al,. (2010) Single base-resolution methylome of the silkworm reveals a sparse epigenomic map. Nat Biotechnol 28: 516-520.
138. Yi, S.V., and, Goodisman, M.A.D., (2009) Computational approaches for understanding the evolution of DNA methylation in animals. Epigenetics 4: 551-556.
139. Yoder, J.A., Walsh, C.P., and, Bestor, T.H., (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13: 335-340. (Pubitemid 27309911)
140. Young, J.I., Hong, E.P., Castle, J.C., Crespo-Barreto, J., Bowman, A.B., Rose, M.F., et al,. (2006) Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc Natl Acad Sci USA 103: 1656-1656.
141. Zemach, A., McDaniel, I.E., Silva, P., and, Zilberman, D., (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-919.
142. Zeng, J., and, Yi, S.V., (2010) DNA methylation and genome evolution in honeybee: gene length, expression, functional enrichment covary with the evolutionary signature of DNA methylation. Genome Biol Evol 2: 770-780.
143. Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., and, Henikoff, S., (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39: 61-69. (Pubitemid 46026502)