DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci USA

School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 07/2009; 106(27):11206-11. DOI: 10.1073/pnas.0900301106
Source: PubMed


The recent, unexpected discovery of a functional DNA methylation system in the genome of the social bee Apis mellifera underscores the potential importance of DNA methylation in invertebrates. The extent of genomic DNA methylation and its role in A. mellifera remain unknown, however. Here we show that genes in A. mellifera can be divided into 2 distinct classes, one with low-CpG dinucleotide content and the other with high-CpG dinucleotide content. This dichotomy is explained by the gradual depletion of CpG dinucleotides, a well-known consequence of DNA methylation. The loss of CpG dinucleotides associated with DNA methylation also may explain the unusual mutational patterns seen in A. mellifera that lead to AT-rich regions of the genome. A detailed investigation of this dichotomy implicates DNA methylation in A. mellifera development. High-CpG genes, which are predicted to be hypomethylated in germlines, are enriched with functions associated with developmental processes, whereas low-CpG genes, predicted to be hypermethylated in germlines, are enriched with functions associated with basic biological processes. Furthermore, genes more highly expressed in one caste than another are overrepresented among high-CpG genes. Our results highlight the potential significance of epigenetic modifications, such as DNA methylation, in developmental processes in social insects. In particular, the pervasiveness of DNA methylation in the genome of A. mellifera provides fertile ground for future studies of phenotypic plasticity and genomic imprinting.

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    • "In comparison, the fruit fly Drosophila melanogaster lacks most of the classical DNMTs and displays limited cytosine methylation (Hung et al., 1999; Lyko et al., 2000). At the same time, the honey bee Apis mellifera bears a fully functional set of DNMTs, and DNA methylation is widespread across its genome (Elango et al., 2009). Although bivalve organisms comprise more than 30000 species and constitute the second largest group of mollusks, only limited research on DNA methylation patterns has been conducted in this taxonomic group (Gavery and Roberts, 2010; Riviere et al., 2013). "
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    ABSTRACT: DNA methylation is an important epigenetic regulatory mechanism that influences genomic stability, gene activation, X-chromosome inactivation and other factors. A change in DNA methylation is usually associated with aging and cellular senescence. DNA methyltransferase 1 (DNMT1) is the most abundant DNA methyltransferase, and it plays an important role in maintaining the established methylation pattern during DNA replication in vertebrates. Although the effect of aging on DNA methylation has been well studied in vertebrates, little research has been conducted in invertebrates, especially in marine bivalves. In this study, we examined global DNA methylation levels in four groups of adult Zhikong scallop Chlamys farreri at different ages. The results showed that both the age and tissue type had a strong effect on the DNA methylation. In addition, a significant decrease in DNA methylation with aging (1–4 years) can be detected in mantle, kidney and hepatopancreas. We further measured the change in DNMT1 transcript abundance using quantitative reverse transcription PCR (qRT-PCR), which revealed that DNMT1 transcription significantly decreased with aging in mantle and hepatopancreas and strongly correlated with DNA methylation (R = 0.72). Our data provided greater insight into the aging-related decline of DNA methylation, which could aid in gaining a better understanding of the relationship between DNA me-thylation and the aging process in bivalve mollusks.
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    • "Research shows that genomic imprinting occurs in insects as well as in many other animals (Youngson & Whitelaw, 2008; Anaka et al., 2009; Elango et al., 2009). "
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    ABSTRACT: In addition to nutritional conditions experienced by individuals themselves, those experienced by their parents can affect their immune function. Here, we studied the intra- and trans-generational effects of larval diet on susceptibility to an entomopathogenic fungus, Beauveria bassiana, in the greater wax moth, Galleria mellonella. In the first part of the study, a split-brood design was used to compare the susceptibility of full-sibs raised either on low or high nutrition larval diet. In the second part of the study, a similar experimental design was employed to investigate the effects of maternal and paternal diet as well as their interaction on offspring's susceptibility. In the first part of the study, we found that individuals fed with high nutrition diet had higher mortality from infection than individuals fed with low nutrition diet. However, diet did not affect post-infection survival time. Conversely, in the second part of the study, maternal diet was found to have no significant effect on final mortality rate of offspring, but it affected survival time: larvae with high nutrition maternal diet survived fewer days after infection than larvae with low nutrition maternal diet. Paternal diet had no significant effect on offspring's susceptibility to the fungus, indicating that paternal effects are not as important as maternal effects in influencing immune function in this species. Our findings provide further indication that maternal nutrition affects immune function in insects, and suggest that the direct effects of nutrition on immunity may be different, yet parallel, to those caused by parental nutrition. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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    • "Components of this secretion, including Royalactin, Major Royal Jelly proteins, and a fatty acid Histone Deacetylase inhibitor , likely activate epidermal growth factor receptor (EGFR) signaling in the larval fat body (Kamakura 2011), which in turn activates downstream pathways that directly or indirectly affect developmental trajectories (e.g., insulin-like signaling, PI3K/TOR/S6K, Ras/Raf/MAPK; Patel et al. 2007; Kamakura 2011; Mutti et al. 2011; Wolschin et al. 2011; Badisco et al. 2013). Experimental gene knock-downs, as well as comparative transcriptome and methylome studies, performed mostly in honeybees, have revealed extensive caste-dependent changes in gene expression and epigenetic regulation (Kucharski et al. 2008; Elango et al. 2009; Bonasio et al. 2012; Shi et al. 2012; Simola, Ye, et al. 2013) for a wide range of genes, for example, hexamerins (Hoffman and Goodisman 2007; Hunt et al. 2007; Cameron et al. 2013), "
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    ABSTRACT: Developmental plasticity allows for the remarkable morphological specialization of individuals into castes in eusocial species of Hymenoptera. Developmental trajectories that lead to alternative caste fates are typically determined by specific environmental stimuli that induce larvae to express and maintain distinct gene expression patterns. While most eusocial species express two castes, queens and workers, the ant Cardiocondyla obscurior expresses diphenic females and males; this provides a unique system with four discrete phenotypes to study the genomic basis of developmental plasticity in ants. We sequenced and analyzed the transcriptomes of 28 individual C. obscurior larvae of known developmental trajectory, providing the first in-depth analysis of gene expression in eusocial insect larvae. Clustering and transcription factor binding site analyses revealed that different transcription factors and functionally distinct sets of genes are recruited during larval development to induce the four alternative trajectories. In particular, we found complex patterns of gene regulation pertaining to sphingolipid metabolism, a conserved molecular pathway involved in development, obesity and aging. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail:
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