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

Zhichao Yan, Qi Fang, Jiqiang Song, Lei Yang, Shan Xiao, Jiale Wang, Gongyin Ye

PLoS pathogens 2023 Sep

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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. Copyright: © 2023 Yan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation

Zhichao Yan, Qi Fang, Jiqiang Song, Lei Yang, Shan Xiao, Jiale Wang, Gongyin Ye. A serpin gene from a parasitoid wasp disrupts host immunity and exhibits adaptive alternative splicing. PLoS pathogens. 2023 Sep;19(9):e1011649