A serpin gene from a parasitoid wasp disrupts host immunity and exhibits adaptive alternative splicing

PLoS Pathog. 2023 Sep 11;19(9):e1011649. doi: 10.1371/journal.ppat.1011649. eCollection 2023 Sep.

Abstract

Alternative splicing (AS) is a major source of protein diversity in eukaryotes, but less is known about its evolution compared to gene duplication (GD). How AS and GD interact is also largely understudied. By constructing the evolutionary trajectory of the serpin gene PpSerpin-1 (Pteromalus puparum serpin 1) in parasitoids and other insects, we found that both AS and GD jointly contribute to serpin protein diversity. These two processes are negatively correlated and show divergent features in both protein and regulatory sequences. Parasitoid wasps exhibit higher numbers of serpin protein/domains than nonparasitoids, resulting from more GD but less AS in parasitoids. The potential roles of AS and GD in the evolution of parasitoid host-effector genes are discussed. Furthermore, we find that PpSerpin-1 shows an exon expansion of AS compared to other parasitoids, and that several isoforms are involved in the wasp immune response, have been recruited to both wasp venom and larval saliva, and suppress host immunity. Overall, our study provides an example of how a parasitoid serpin gene adapts to parasitism through AS, and sheds light on the differential features of AS and GD in the evolution of insect serpins and their associations with the parasitic life strategy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing
  • Animals
  • Eukaryota
  • Larva / genetics
  • Serpins* / genetics
  • Wasps* / genetics

Substances

  • Serpins

Grants and funding

This work was supported by the Key Program of National Natural Science Foundation of China (NSFC) (grant no. 31830074 to G.Y.Y.), NSFC (grant no. 31701843 to Z.C.Y.), the Regional Joint Fund for Innovation and Development of NSFC (grant no. U21A20225 to G.Y.Y.), NSFC (grant no. 32072480 to Q.F. and no. 32001964 to L.Y.), Natural Science Foundation of Hainan Province (grant no. 323QN262 to Y.Z.C.), Natural Science Foundation of Zhejiang Province (grant No. LTGN23C140001 to F. Q.), and Major International (Regional) Joint Research Project of NSFC (grant no. 31620103915 to G.Y.Y.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.