Characterizing the Infection-Induced Transcriptome of Nasonia vitripennis Reveals a Preponderance of Taxonomically-Restricted Immune Genes

Timothy B Sackton,John H Werren,Andrew G Clark,François Leulier

doi:10.1371/journal.pone.0083984

Timothy B Sackton, John H Werren + Show 2 more

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https://doi.org/10.1371/journal.pone.0083984

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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.

Highlights

Host-pathogen coevolution is one of the major drivers of adaptive evolution across a wide variety of organisms: genes encoding proteins involved in the immune response are among the most common targets of positive selection in numerous taxa, including mammals [1,2] and insects [3,4,5,6,7]
There is growing evidence that the protein-coding repertoire of the innate immune system is rapidly evolving in insects [5,8,9,10,11], even though comparative genomic analysis reveals the existence of a conserved core of immune signaling pathways in most insects [12,13,14,15]
With the substantial increase in predicted gene number and gene quality obtained with the Official Gene Set V2.0 (OGSv2) gene set, it is clear that an updated annotation of infection responsive genes would be valuable

Summary

Introduction

Host-pathogen coevolution is one of the major drivers of adaptive evolution across a wide variety of organisms: genes encoding proteins involved in the immune response are among the most common targets of positive selection in numerous taxa, including mammals [1,2] and insects [3,4,5,6,7]. There is growing evidence that the protein-coding repertoire of the innate immune system is rapidly evolving in insects [5,8,9,10,11], even though comparative genomic analysis reveals the existence of a conserved core of immune signaling pathways in most insects [12,13,14,15] This trend is apparent among genes encoding proteins involved in recognition of pathogens and among genes encoding pathogen killing molecules such as antimicrobial peptides (AMPs), based on the few cases that have been well characterized to date. These ‘‘taxonspecific’’ immunity genes likely represent both genes that evolve so rapidly that their homology to other genes is obscured and de novo evolution of immunity genes within taxa

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