BACKGROUND: Epigenetic modification of DNA via methylation is one of the key inventions in eukaryotic evolution. It provides a source for the switching of gene activities, the maintenance of stable phenotypes and the integration of environmental and genomic signals. Although this process is widespread among eukaryotes, both the patterns of methylation and their relevant biological roles not only vary noticeably in different lineages, but often are poorly understood. In addition, the evolutionary origins of DNA methylation in multicellular organisms remain enigmatic. Here we used a new 'epigenetic' model, the social honey bee Apis mellifera, to gain insights into the significance of methylated genes. RESULTS: We combined microarray profiling of several tissues with genome-scale bioinformatics and bisulfite sequencing of selected genes to study the honey bee methylome. We find that around 35% of the annotated honey bee genes are expected to be methylated at the CpG dinucleotides by a highly conserved DNA methylation system. We show that one unifying feature of the methylated genes in this species is their broad pattern of expression and the associated 'housekeeping' roles. In contrast, genes involved in more stringently regulated spatial or temporal functions are predicted to be un-methylated. CONCLUSION: Our data suggest that honey bees use CpG methylation of intragenic regions as an epigenetic mechanism to control the levels of activity of the genes that are broadly expressed and might be needed for conserved core biological processes in virtually every type of cell. We discuss the implications of our findings for genome-scale regulatory network structures and the evolution of the role(s) of DNA methylation in eukaryotes. Our findings are particularly important in the context of the emerging evidence that environmental factors can influence the epigenetic settings of some genes and lead to serious metabolic and behavioural disorders.
BACKGROUND: Epigenetic modification of DNA via methylation is one of the key inventions in eukaryotic evolution. It provides a source for the switching of gene activities, the maintenance of stable phenotypes and the integration of environmental and genomic signals. Although this process is widespread among eukaryotes, both the patterns of methylation and their relevant biological roles not only vary noticeably in different lineages, but often are poorly understood. In addition, the evolutionary origins of DNA methylation in multicellular organisms remain enigmatic. Here we used a new 'epigenetic' model, the social honey beeApis mellifera, to gain insights into the significance of methylated genes. RESULTS: We combined microarray profiling of several tissues with genome-scale bioinformatics and bisulfite sequencing of selected genes to study the honey bee methylome. We find that around 35% of the annotated honey bee genes are expected to be methylated at the CpG dinucleotides by a highly conserved DNA methylation system. We show that one unifying feature of the methylated genes in this species is their broad pattern of expression and the associated 'housekeeping' roles. In contrast, genes involved in more stringently regulated spatial or temporal functions are predicted to be un-methylated. CONCLUSION: Our data suggest that honey bees use CpG methylation of intragenic regions as an epigenetic mechanism to control the levels of activity of the genes that are broadly expressed and might be needed for conserved core biological processes in virtually every type of cell. We discuss the implications of our findings for genome-scale regulatory network structures and the evolution of the role(s) of DNA methylation in eukaryotes. Our findings are particularly important in the context of the emerging evidence that environmental factors can influence the epigenetic settings of some genes and lead to serious metabolic and behavioural disorders.
Authors: Luciano Di Croce; Veronica A Raker; Massimo Corsaro; Francesco Fazi; Mirco Fanelli; Mario Faretta; Francois Fuks; Francesco Lo Coco; Tony Kouzarides; Clara Nervi; Saverio Minucci; Pier Giuseppe Pelicci Journal: Science Date: 2002-02-08 Impact factor: 47.728
Authors: Jo Vandesompele; Katleen De Preter; Filip Pattyn; Bruce Poppe; Nadine Van Roy; Anne De Paepe; Frank Speleman Journal: Genome Biol Date: 2002-06-18 Impact factor: 13.583
Authors: Chris R Smith; Christopher D Smith; Hugh M Robertson; Martin Helmkampf; Aleksey Zimin; Mark Yandell; Carson Holt; Hao Hu; Ehab Abouheif; Richard Benton; Elizabeth Cash; Vincent Croset; Cameron R Currie; Eran Elhaik; Christine G Elsik; Marie-Julie Favé; Vilaiwan Fernandes; Joshua D Gibson; Dan Graur; Wulfila Gronenberg; Kirk J Grubbs; Darren E Hagen; Ana Sofia Ibarraran Viniegra; Brian R Johnson; Reed M Johnson; Abderrahman Khila; Jay W Kim; Kaitlyn A Mathis; Monica C Munoz-Torres; Marguerite C Murphy; Julie A Mustard; Rin Nakamura; Oliver Niehuis; Surabhi Nigam; Rick P Overson; Jennifer E Placek; Rajendhran Rajakumar; Justin T Reese; Garret Suen; Shu Tao; Candice W Torres; Neil D Tsutsui; Lumi Viljakainen; Florian Wolschin; Jürgen Gadau Journal: Proc Natl Acad Sci U S A Date: 2011-01-31 Impact factor: 11.205
Authors: Yannick Wurm; John Wang; Oksana Riba-Grognuz; Miguel Corona; Sanne Nygaard; Brendan G Hunt; Krista K Ingram; Laurent Falquet; Mingkwan Nipitwattanaphon; Dietrich Gotzek; Michiel B Dijkstra; Jan Oettler; Fabien Comtesse; Cheng-Jen Shih; Wen-Jer Wu; Chin-Cheng Yang; Jerome Thomas; Emmanuel Beaudoing; Sylvain Pradervand; Volker Flegel; Erin D Cook; Roberto Fabbretti; Heinz Stockinger; Li Long; William G Farmerie; Jane Oakey; Jacobus J Boomsma; Pekka Pamilo; Soojin V Yi; Jürgen Heinze; Michael A D Goodisman; Laurent Farinelli; Keith Harshman; Nicolas Hulo; Lorenzo Cerutti; Ioannis Xenarios; Dewayne Shoemaker; Laurent Keller Journal: Proc Natl Acad Sci U S A Date: 2011-01-31 Impact factor: 11.205
Authors: Robert Parker; Andony P Melathopoulos; Rick White; Stephen F Pernal; M Marta Guarna; Leonard J Foster Journal: PLoS One Date: 2010-06-15 Impact factor: 3.240