Abstract
Epigenetic phenomena have been widely characterized in the genomes of vertebrates and DNA methylation is a key mechanism of epigenetic regulation. The DNA methylation systems of invertebrates and vertebrates show several notable differences. However, the evolutionary implications of those differences only recently began to be revealed. Our study investigated the recurrence of sex-specific methylation, as previously described for the species Drosophila willistoni, in other species of the Sophophora subgenus that present close evolutionary relationship. The MSRE and Southern blot techniques were used to analyze rDNA of some species of the willistoni, melanogaster, saltans and obscura groups of Drosophila and the results suggested that differential DNA methylation between sexes only occurs in Drosophila tropicalis and D. insularis, two sibling species of the willistoni subgroup. However, only using the MSRE technique we could detect sex-specific patterns of DNA methylation in all species of willistoni subgroup. These results indicate that DNA methylation may present important differences, even between closely related species, shedding new light on this Neotropical species complex.
Similar content being viewed by others
References
Ashburner M (1989) Drosophila: A laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Ayala FJ, Tracey ML, Hedgecock D, Richmond RC (1974) Genetic differentiation during the speciation process in Drosophila. Evolution 28:576–592
Bhutkar A, Schaeffer SW, Russo SM, XU M, Smith TF, Gelbart WM (2008) Chromosomal rearrangement inferred from comparisons of 12 Drosophila Genomes. Genetics 179:1657–1680
Bird AP, Taggart MH, Macleod D (1981) Loss of rDNA methylation accompanies the onset of ribosomal gene activity in early development of X. laevis. Cell 26:381–390
Burdick AB (1954) New medium of reproductive quality stable at room temperature. Dros Inf Serv 28:170
Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman T, Kellis M, Gelbart W et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218
Field LM, Lyko F, Mandrioli M, Prantera G (2004) DNA methylation in insects. Insect Mol Biol 13:109–115
Fisher O, Siman-Tov R, Ankri S (2004) Characterization of cytosine methylated regions and 5-cytosine DNA methyltransferase (Ehmeth) in the protozoan parasite Entamoeba histolytica. Nucleic Acids Res 32:287–297
Garcia RN, D’Ávila MF, Loreto ELS, Panzera Y, Heredia FO, Valente VLS (2007) First evidence of methylation in the genome of Drosophila willistoni. Genetica 131:91–105
Ghoshal K, Majumder S, Datta J, Motiwala T, Bai S, Sharma SM, Frankel W, Jacob ST (2004) Role of human ribosomal RNA (rRNA) promoter methylation and of methyl-CpG-binding protein MBD2 in the suppression of rRNA gene expression. J Biol Chem 279:6783–6793
Gleason JM, Griffith EC, Powell JR (1998) A molecular phylogeny of the Drosophila willistoni group: Conflicts between species concepts? Evolution 52:1093–1103
Gowher H, Leismann O, Jeltsch A (2000) DNA of Drosophila melanogaster contains 5-methylcytosine. EMBO 19:6918–6923
Gruenbaum Y, Naveh-Many T, Cedar H, Razin A (1981) Sequence specificity of methylation in higher plant DNA. Nature 292:860–862
Hung MS, Karthikeyan N, Huang B, Koo HC, Kiger J, Shen CKJ (1999) Drosophila proteins related to vertebrade DNA (5-cytosine) methyltransferases. Proc Nat Acad Sci USA 96:11940–11945
Jablonka E (2004) Epigenetic epidemiology. Int J Epidemiol 33:929–935
Khosla S, Dean W, Brown D, Reik W, Feil R (2001) Culture of preimplantation mouse embryos affects development and the expression of imprinted genes. Biol Reprod 64:918–926
Kunert N, Marhold J, Stach D, Lyko F (2003) A Dnmt2-like protein mediates DNA methylation in Drosophila. Development 130:5083–5090
Lodhi MA, Ye GN, Weeden NF, Reisch BI (1994) A simple and efficient method for DNA extraction from grapevine cultivars and Vitis species. Plant Mol Biol Rep 12:6–13
Lyko F (2001) DNA methylation learns to fly. Trends Genet 17:169–172
Lyko F, Ramsahoye BH, Jaenisch R (2000) DNA methylation in Drosophila melanogaster. Nature 408:538–540
Mandrioli M, Borsatti F (2006) DNA methylation of fly genes and transposons. Cell Mol Life Sci 63:1933–1936
Markow TA, O’Grady PM (2005) Evolutionary Genetics of Reproductive Behavior in Drosophila: Connecting the Dots. Annu Rev Genet 39:263–291
Marques EK, Napp M, Winge H, Cordeiro AR (1966) A corn meal, soybean flour, wheat germ medium for Drosophila. Dros Inf Serv 41:187
McStay B, Grummt I (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Bi 24:131–157
Nur U (1990) Heterochromatinization and euchromatinization of whole genomes in scale insects (Coccoidea: Homoptera). Development Suppl: 29–34
O’Grady PM, Kidwell MG (2002) Phylogeny of the subgenus Sophophora (Diptera: Drosophilidae) based on combined analysis of nuclear and mitochondrial sequences. Mol Phylogenet Evol 22:442–453
O’Grady PM, Clark JB, Kidwell MG (1998) Phylogeny of the Drosophila saltans Species Group Based on Combined Analysis of Nuclear and Mitochondrial DNA Sequences. Mol Biol Evol 15:656–664
Powell JR (1997) Progress and prospects in evolutionary biology: the drosophila model. Oxford University Press, New York
Robe LJ, Cordeiro J, Loreto ELS, Valente VLS (2010) Taxonomic boundaries, phylogenetic relationships and biogeography of the Drosophila willistoni subgroup (Diptera: Drosophilidae). Genetica doi: 10.1007/s10709-009-9432-5
Salzberg A, Fisher O, Siman-Tov R, Ankri S (2004) Identification of methylated sequences in genomic DNA of adult Drosophila melanogaster. Biochem Biophys Res Commun 322:465–469
Santoro R, Grummt I (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell 8:719–725
Santoro R, Grummt I (2005) Epigenetic mechanism of rDNA gene silencing: temporal order of NoRC-mediated histone modification, chromatin remodelling, and DNA methylation. Mol Cell Biol 25:2539–2546
Sassi AK, Herédia FO, Loreto ELS, Valente VLS, Rohde C (2005) Transposable elements P and gypsy in natural populations of Drosophila willistoni. Gen Mol Biol 4:734–739
Schaeffer SW, Bhutkar A, McAllister BF, Matsuda M, Matzkin LM, O’Grady PM, Rohde C, Valente VL, Aguadé M, Anderson WW et al (2008) Polytene chromosomal maps of 11 Drosophila species: The order of genomic scaffolds inferred from genetic and physical maps. Genetics 179:1601–1655
Tautz D, Hancock J, Webb D, Tautz C, Dover G (1988) Complete sequences of the rRNA genes of Drosophila melanogaster. Mol Biol Evol 5:366–376
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
Tweedie S, Ng HH, Barlow AL, Turner BM, Hendrich B, Bird A (1999) Vestiges of a methylation system in Drosophila melanogaster? Nat Genet 23:389–390
Vicario S, Moriyama EN, Powell JR (2007) Codon usage in twelve species of Drosophila. BMC Evol Biol 7:226–242
Weinhold B (2006) Epigenetics: the science of change. Environ Health Persp 114:A160–A167
Acknowledgments
We would like to thank Dr. Raul Godoy-Herrera, of University of Chile, for strains of D. subobscura; Dr. Muneo Matsuda, of the Kyorin University–Tokyo, for strains of D. pseudoobscura; Dr. Elgion Loreto, of Universidade Federal de Santa Maria–Brazil, for D. sechellia strains and Dr. Hermes J. Schmitz for stimulating discussions about evolution. We would also thank two anonymous referees for helpful comments and suggestions. This study was supported by grants and fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
D’Ávila, M.F., Garcia, R.N., Panzera, Y. et al. Sex-specific methylation in Drosophila: an investigation of the Sophophora subgenus. Genetica 138, 907–913 (2010). https://doi.org/10.1007/s10709-010-9473-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-010-9473-9