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Characterizing the infection-induced transcriptome of Nasonia vitripennis reveals a preponderance of taxonomically-restricted immune genes.

ABSTRACT: The innate immune system in insects consists of a conserved core signaling network and rapidly diversifying effector and recognition components, often containing a high proportion of taxonomically-restricted genes. In the absence of functional annotation, genes encoding immune system proteins can thus be difficult to identify, as homology-based approaches generally cannot detect lineage-specific genes. Here, we use RNA-seq to compare the uninfected and infection-induced transcriptome in the parasitoid wasp Nasonia vitripennis to identify genes regulated by infection. We identify 183 genes significantly up-regulated by infection and 61 genes significantly down-regulated by infection. We also produce a new homology-based immune catalog in N. vitripennis, and show that most infection-induced genes cannot be assigned an immune function from homology alone, suggesting the potential for substantial novel immune components in less well-studied systems. Finally, we show that a high proportion of these novel induced genes are taxonomically restricted, highlighting the rapid evolution of immune gene content. The combination of functional annotation using RNA-seq and homology-based annotation provides a robust method to characterize the innate immune response across a wide variety of insects, and reveals significant novel features of the Nasonia immune response.

SUBMITTER: Sackton TB

PROVIDER: S-EPMC3873987 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Characterizing the infection-induced transcriptome of Nasonia vitripennis reveals a preponderance of taxonomically-restricted immune genes.

Sackton Timothy B TB Werren John H JH Clark Andrew G AG

PloS one 20131227 12

The innate immune system in insects consists of a conserved core signaling network and rapidly diversifying effector and recognition components, often containing a high proportion of taxonomically-restricted genes. In the absence of functional annotation, genes encoding immune system proteins can thus be difficult to identify, as homology-based approaches generally cannot detect lineage-specific genes. Here, we use RNA-seq to compare the uninfected and infection-induced transcriptome in the para ...[more]

PMID: 24386321

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Project description:The parasitoid wasp Nasonia vitripennis is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over exons, primarily in the 5' regions of genes. It is also elevated near the sites of translational initiation and termination, with reduced levels in 5' and 3' UTRs. Methylated genes have higher median expression levels and lower expression variation across development stages than non-methylated genes. There is no difference in frequency of differential splicing between methylated and non-methylated genes, and as yet no established role for methylation in regulating alternative splicing in Nasonia. Phylogenetic comparisons indicate that many genes maintain methylation status across long evolutionary time scales. Nasonia methylated genes are more likely to be conserved in insects, but even those that are not conserved show broader expression across development than comparable non-methylated genes. Finally, examination of duplicated genes shows that those paralogs that have lost methylation in the Nasonia lineage following gene duplication evolve more rapidly, show decreased median expression levels, and increased specialization in expression across development. Methylation of Nasonia genes signals constitutive transcription across developmental stages, whereas non-methylated genes show more dynamic developmental expression patterns. We speculate that loss of methylation may result in increased developmental specialization in evolution and acquisition of methylation may lead to broader constitutive expression.

Dataset Information

Characterizing the infection-induced transcriptome of Nasonia vitripennis reveals a preponderance of taxonomically-restricted immune genes.

Publications

Characterizing the infection-induced transcriptome of Nasonia vitripennis reveals a preponderance of taxonomically-restricted immune genes.

Similar Datasets

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