Epigenetic inheritance and genome regulation: Is DNA methylation linked to ploidy in haplodiploid insects?

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1785, 2014, Pages

  Glastad, Karl M ^a   Hunt, Brendan G ^a,b   Yi, Soojin V ^a   Goodisman, Michael A D ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

DNA methylome; Dosage compensation; Epigenetics; Gene regulation; Haplodiploid; Social insect

Indexed keywords

CELL ORGANELLE; CHROMOSOME; DNA; GENE EXPRESSION; GENOME; HERITABILITY; METHYLATION; MORPHOLOGY; POLYPLOIDY; SOCIAL INSECT;

ANIMAL; BIOLOGICAL MODEL; FOOD CHAIN; GRASSLAND; GROWTH, DEVELOPMENT AND AGING; HERBIVORY; INTRODUCED SPECIES; KENYA; MAMMAL; PHYSIOLOGY; SOLANUM;

ANIMALS; FOOD CHAIN; GRASSLAND; GROWTH AND DEVELOPMENT; HERBIVORY; INTRODUCED SPECIES; KENYA; MAMMALS; MODELS, BIOLOGICAL; PHYSIOLOGY; SOLANUM;

EID: 84899689010     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0411     Document Type: Article

References (48)

1. Edgar BA, Orr-Weaver TL. 2001 Endoreplication cell cycles: more for less. Cell 105, 297-306. (doi:10. 1016/S0092-8674(01)00334-8)
2. Sassone-Corsi P. 2002 Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296, 2176-2178. (doi:10.1126/science. 1070963)
3. Heimpel GE, de Boer JG. 2008 Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53, 209-230. (doi:10.1146/annurev.ento.53.103106.093441)
4. Otto SP, Jarne P. 2001 Haploids: hapless or happening? Science 292, 2441-2443. (doi:10.1126/ science.1062890)
5. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR. 1999 Ploidy regulation of gene expression. Science 285, 251-254. (doi:10.1126/science.285.5425.251)
6. Aron S, de Menten L, Van Bockstaele DR, Blank SM, Roisin Y. 2005 When hymenopteran males reinvented diploidy. Curr. Biol. 15, 824-827. (doi:10.1016/j.cub.2005.03.017)
7. Adams KL, Wendel JF. 2005 Novel patterns of gene expression in polyploid plants. Trends Genet. 21, 539-543. (doi:10.1016/j.tig.2005.07.009)
8. Otto SP. 2007 The evolutionary consequences of polyploidy. Cell 131, 452-462. (doi:10.1016/j.cell. 2007.10.022)
9. Rasch E, Cassidy J, King R. 1977 Evidence for dosage compensation in parthenogenetic Hymenoptera. Chromosoma 59, 323-340. (doi:10.1007/BF00327973)
10. Evans J, Shearman DCA, Oldroyd BP. 2004 Molecular basis of sex determination in haplodiploids. Trends Ecol. Evol. 19, 1-3. (doi:10.1016/j.tree.2003.11.001)
11. Scholes DR, Suarez AV, Paige KN. 2013 Can endopolyploidy explain body size variation within and between castes in ants? Ecol. Evol. 3, 2128-2137. (doi:10.1002/ece3.623)
12. Bonasio R, Tu S, Reinberg D. 2010 Molecular signals of epigenetic states. Science 330, 612-616. (doi:10. 1126/science.1191078)
13. Klose RJ, Bird AP. 2006 Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31, 89-97. (doi:10.1016/j.tibs.2005.12.008)
14. Suzuki MM, Bird A. 2008 DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465-476. (doi:10.1038/ nrg2341)
15. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. 2010 The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8, e1000506. (doi:10.1371/ journal.pbio.1000506)
16. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, Maleszka R. 2012 DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc. Natl Acad. Sci. USA 109, 4968-4973. (doi:10. 1073/pnas.1202392109)
17. Simola DF, Ye C, Mutti NS, Dolezal K, Bonasio R, Liebig J, Reinberg D, Berger SL. 2013 A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res. 23, 486-496. (doi:10.1101/gr.148361.112)
18. Bonasio R et al. 2012 Genome-wide and castespecific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr. Biol. 22, 1755-1764. (doi:10.1016/j.cub.2012.07.042)
19. Kucharski R, Maleszka J, Foret S, Maleszka R. 2008 Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827-1830. (doi:10.1126/science.1153069)
20. Conrad T, Akhtar A. 2012 Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat. Rev. Genet. 13, 123-134. (doi:10.1038/nrg3124)
21. Payer B, Lee JT. 2008 X chromosome dosage compensation: how mammals keep the balance. Annu. Rev. Genet. 42, 733-772. (doi:10.1146/ annurev.genet.42.110807.091711)
22. Ross KG, Vargo EL, Keller L, Trager JC. 1993 Effect of a founder event on variation in the genetic sexdetermining system of the fire ant Solenopsis invicta. Genetics 135, 843-854.
23. Ross KG, Fletcher DJC. 1985 Genetic origin of male diploidy in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae), and its evolutionary significance. Evolution 39, 888-903. (doi:10.2307/ 2408688)
24. Krieger MJB, Ross KG, Chang CWY, Keller L. 1999 Frequency and origin of triploidy in the fire ant Solenopsis invicta. Heredity 82, 142-150. (doi:10. 1038/sj.hdy.6884600)
25. Hunt BG, Glastad KM, Yi SV, Goodisman MAD. 2013 Patterning and regulatory associations of DNA methylation are mirrored by histone modifications in insects. Genome Biol. Evol. 5, 591-598. (doi:10. 1093/gbe/evt030)
26. Wurm Y et al. 2011 The genome of the fire ant Solenopsis invicta. Proc. Natl Acad. Sci. USA 108, 5679-5684. (doi:10.1073/pnas.1009690108)
27. Benjamini Y, Hochberg Y. 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. B (Methodological) 57, 289-300.
28. R Development Core Team. 2013 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
29. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005 BLAST2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676. (doi:10.1093/bioinformatics/bti610)
30. Ometto L, Shoemaker D, Ross KG, Keller L. 2011 Evolution of gene expression in fire ants: the effects of developmental stage, caste, and species. Mol. Biol. Evol. 28, 1381-1392. (doi:10.1093/molbev/ msq322)
31. Wang J, Jemielity S, Uva P, Wurm Y, Graff J, Keller L. 2007 An annotated cDNA library and microarray for large-scale gene-expression studies in the ant Solenopsis invicta. Genome Biol. 8, R9. (doi:10.1186/ gb-2007-8-1-r9)
32. Townsend J, Hartl D. 2002 Bayesian analysis of gene expression levels: statistical quantification of relative mRNA level across multiple strains or treatments. Genome Biol. 3, research0071. (doi:10.1186/gb-2002-3-12-research0071)
33. Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y-C, Shoemaker D, Keller L. 2013 A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664-668. (doi:10.1038/nature11832)
34. Smyth GK. 2005 Limma: linear models for microarray data. In Bioinformatics and computational biology solutions using R and bioconductor (eds R Gentleman, V Carey, S Dudoit, R Irizarry, W Huber), pp. 397-420. New York, NY: Springer.
35. Waterhouse RM, Zdobnov EM, Tegenfeldt F, Li J, Kriventseva EV. 2011 OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Res. 39, D283-D288. (doi:10.1093/nar/ gkq930)
36. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller L, Goodisman MAD. 2011 Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc. Natl Acad. Sci. USA 108, 15 936-15 941. (doi:10.1073/pnas.1104825108)
37. Glastad KM, Hunt BG, Yi SV, Goodisman MAD. 2011 DNA methylation in insects: on the brink of the epigenomic era. Insect Mol. Biol. 20, 553-565. (doi:10.1111/j.1365-2583.2011.01092.x)
38. Foret S, Kucharski R, Pittelkow Y, Lockett G, Maleszka R. 2009 Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genomics 10, 472. (doi:10. 1186/1471-2164-10-472)
39. Hunt BG, Glastad KM, Yi SV, Goodisman MAD. 2013 The function of intragenic DNA methylation: insights from insect epigenomes. Integr. Comp. Biol. 53, 319-328. (doi:10.1093/icb/ict003)
40. Smith CR, Toth AL, Suarez AV, Robinson GE. 2008 Genetic and genomic analyses of the division of labour in insect societies. Nat. Rev. Genet. 9, 735-748. (doi:10.1038/nrg2429)
41. Nanty L, Carbajosa G, Heap GA, Ratnieks F, van Heel DA, Down TA, Rakyan VK. 2011 Comparative methylomics reveals gene-body H3K36me3 in Drosophila predicts DNA methylation and CpG landscapes in other invertebrates. Genome Res. 21, 1841-1850. (doi:10.1101/gr.121640.111)
42. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S. 2011 CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479, 74-79. (doi:10.1038/ nature10442)
43. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S. 2008 Histone H2A. Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125-129. (doi:10.1038/nature07324)
44. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. 2007 Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61-69. (doi:10.1038/ ng1929)
45. Gelbart ME, Kuroda MI. 2009 Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136, 1399-1410. (doi:10.1242/dev.029645)
46. Wang Z, Zhang J. 2011 Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc. Natl Acad. Sci. USA 108, E67-E76. (doi:10.1073/pnas.1100059108)
47. Talia SD, Skotheim JM, Bean JM, Siggia ED, Cross FR. 2007 The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448, 947-951. (doi:10.1038/nature06072)
48. Huh I, Zeng J, Park T, Yi S. 2013 DNA methylation and transcriptional noise. Epigenet. Chromat. 6, 9. (doi:10.1186/1756-8935-6-9)