Dataset Information

Whole-genome DNA methylation profile of the jewel wasp (Nasonia vitripennis).

ABSTRACT: The epigenetic mark of DNA methylation, the addition of a methyl (CH3) group to a cytosine residue, has been extensively studied in many mammalian genomes and, although it is commonly found at the promoter regions of genes, it is also involved in a number of different biological functions. In other complex animals, such as social insects, DNA methylation has been determined to be involved in caste differentiation and to occur primarily in gene bodies. The role of methylation in nonsocial insects, however, has not yet been explored thoroughly. Here, we present the whole-genome DNA methylation profile of the nonsocial hymenopteran, the jewel wasp (Nasonia vitripennis). From high-throughput sequencing of bisulfite-converted gDNA extracted from male Nasonia thoraces, we were able to determine which cytosine residues are methylated in the entire genome. We found that an overwhelming majority of methylated sites (99.7%) occur at cytosines followed by a guanine in the 3' direction (CpG sites). Additionally, we found that a majority of methylation in Nasonia occurs within exonic regions of the genome (more than 62%). Overall, methylation is sparse in Nasonia, occurring only at 0.18% of all sites and at 0.63% of CpGs. Our analysis of the Nasonia methylome revealed that in contrast to the methylation profile typically seen in mammals, methylation is sparse and is constrained primarily to exons. This methylation profile is more similar to that of the social hymenopteran species, the honey bee (Apis mellifera). In presenting the Nasonia methylome, we hope to promote future investigation of the regulatory function of DNA methylation in both social and nonsocial hymenoptera.

SUBMITTER: Beeler SM

PROVIDER: S-EPMC3962478 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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Whole-genome DNA methylation profile of the jewel wasp (Nasonia vitripennis).

Beeler Suzannah M SM Wong Garrett T GT Zheng Jennifer M JM Bush Eliot C EC Remnant Emily J EJ Oldroyd Benjamin P BP Drewell Robert A RA

G3 (Bethesda, Md.) 20140320 3

The epigenetic mark of DNA methylation, the addition of a methyl (CH3) group to a cytosine residue, has been extensively studied in many mammalian genomes and, although it is commonly found at the promoter regions of genes, it is also involved in a number of different biological functions. In other complex animals, such as social insects, DNA methylation has been determined to be involved in caste differentiation and to occur primarily in gene bodies. The role of methylation in nonsocial insects ...[more]

PMID: 24381191

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Project description:BackgroundNasonia vitripennis is an emerging insect model system with haplodiploid genetics. It holds a key position within the insect phylogeny for comparative, evolutionary and behavioral genetic studies. The draft genomes for N. vitripennis and two sibling species were published in 2010, yet a considerable amount of transcriptiome data have since been produced thereby enabling improvements to the original (OGS1.2) annotated gene set. We describe and apply the EvidentialGene method used to produce an updated gene set (OGS2). We also carry out comparative analyses showcasing the usefulness of the revised annotated gene set.ResultsThe revised annotation (OGS2) now consists of 24,388 genes with supporting evidence, compared to 18,850 for OGS1.2. Improvements include the nearly complete annotation of untranslated regions (UTR) for 97 % of the genes compared to 28 % of genes for OGS1.2. The fraction of RNA-Seq validated introns also grow from 85 to 98 % in this latest gene set. The EST and RNA-Seq expression data provide support for several non-protein coding loci and 7712 alternative transcripts for 4146 genes. Notably, we report 180 alternative transcripts for the gene lola. Nasonia now has among the most complete insect gene set; only 27 conserved single copy orthologs in arthropods are missing from OGS2. Its genome also contains 2.1-fold more duplicated genes and 1.4-fold more single copy genes than the Drosophila melanogaster genome. The Nasonia gene count is larger than those of other sequenced hymenopteran species, owing both to improvements in the genome annotation and to unique genes in the wasp lineage. We identify 1008 genes and 171 gene families that deviate significantly from other hymenopterans in their rates of protein evolution and duplication history, respectively. We also provide an analysis of alternative splicing that reveals that genes with no annotated isoforms are characterized by shorter transcripts, fewer introns, faster protein evolution and higher probabilities of duplication than genes having alternative transcripts.ConclusionsGenome-wide expression data greatly improves the annotation of the N. vitripennis genome, by increasing the gene count, reducing the number of missing genes and providing more comprehensive data on splicing and gene structure. The improved gene set identifies lineage-specific genomic features tied to Nasonia's biology, as well as numerous novel genes. OGS2 and its associated search tools are available at http://arthropods.eugenes.org/EvidentialGene/nasonia/ , www.hymenopteragenome.org/nasonia/ and waspAtlas: www.tinyURL.com/waspAtlas . The EvidentialGene pipeline is available at https://sourceforge.net/projects/evidentialgene/ .

Project description:The extraordinary range in the degree of sexual dimorphism (SD) among animal species is widely perceived to be caused in part by differences in patterns of sexual selection, but sex-specific adaptations and sex chromosome differences also play a role. Studies in insects have discovered a substantial number of sex-biased genes, but little is known about the epigenetic basis of SD. The degree and genome-wide distribution of sex-biased expression become interesting questions in hymenoptera species with haplodiploid sex-determination. To study the genetic and epigenetic architecture of SD and understand the conservation and evolution of sex-biased expression in a haplodiploid system that lacks sex chromosomes, we performed RNA-seq and whole-genome bisulfite sequencing in female and male adult samples of two parasitoid wasp species, Nasonia vitripennis and Nasonia giraulti. More than 75% of the expressed genes displayed significantly sex-biased expression. Both the number and the degree of sex-biased genes are higher than insects like Drosophila melanogaster, which have sex-chromosome mediated sex determination. Females from the two Nasonia species have far more similar expression profiles than does the contrast between the two sexes within either species. Interestingly, the extremely male- and female-biased genes are enriched for totally different functional categories: male-biased genes are highly enriched for key enzymes in sex-pheromone synthesis; female-biased genes are enriched for nuclear-located genes that are responsible for epigenetic regulation of gene expression. Unlike gene expression profiles, DNA methylomes are more similar within species, and no stable differentially methylated genes have been found between the two sexes, suggesting that DNA methylation is not directly responsible for the molecular basis of SD. However, methylation status does influence sex-biased expression: 80% of female-biased genes are methylated, which is more than two-fold higher than the genome average (30%); almost all male-biased and sex-specific genes are non-methylated, which is consistent with the fact that methylated genes have house-keeping functions and a broader expression breadth. Evolutionarily, male-biased genes have greater sequence divergence between the two species, and they are more likely to have a functional paralog in the Nasonia genome. Sex-specific genes have significantly higher non-synonymous substitution rates and dN/dS ratios. In addition, local clusters of sex-biased genes in the genome may have epigenetic properties similar to the sex chromosome. In summary, Nasonia accomplish a striking degree of sex-differential expression through a difference in ploidy along with associated differences in methylations status.

Dataset Information

Whole-genome DNA methylation profile of the jewel wasp (Nasonia vitripennis).

Publications

Whole-genome DNA methylation profile of the jewel wasp (Nasonia vitripennis).

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