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

A serpin gene from a parasitoid wasp disrupts host immunity and exhibits adaptive alternative splicing.
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DOI:
10.1371/journal.ppat.1011649
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发表时间:
2023-09
期刊:
影响因子:
6.7
通讯作者:
--
中科院分区:
医学1区
文献类型:
--
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选择性剪接(AS)是真核生物中蛋白质多样性的主要来源,但与基因复制(GD)相比,其进化过程知之甚少。AS和GD如何相互作用也在很大程度上未得到充分研究。通过构建PpSerpin-1(Pteromalus puparum serpin 1)在寄生蜂和其他昆虫中的进化轨迹,发现AS和GD共同贡献了serpin蛋白的多样性。这两个过程是负相关的,并在蛋白质和调控序列中表现出不同的功能。寄生蜂表现出更高的丝氨酸蛋白酶抑制剂蛋白/结构域的数量比nonparasitoids,导致更多的GD,但较少的AS在寄生蜂。AS和GD在寄生蜂寄主效应基因进化中的潜在作用进行了讨论。此外,我们发现,PpSerpin-1显示了一个外显子扩展的AS相比,其他寄生虫,和几个亚型参与黄蜂的免疫反应,已被招募到黄蜂毒液和幼虫唾液,并抑制宿主免疫。总的来说,我们的研究提供了一个例子,寄生虫的丝氨酸蛋白酶抑制剂基因如何适应寄生通过AS,并揭示了AS和GD的差异功能的昆虫丝氨酸蛋白酶抑制剂的进化及其协会与寄生的生活策略。选择性剪接(AS)和基因重复(GD)对真核生物蛋白质多样性有重要贡献,但它们与生命策略的相互作用和关联在很大程度上仍未得到充分研究。寄生虫招募不同的毒力基因来对抗宿主防御,为了解AS和GD之间的相互作用提供了一个独特的窗口。调查的PpSerpin-1基因(Pteromalus puparum serpin 1)在寄生蜂和其他昆虫的进化,我们发现AS和GD之间的负相关性,不同的序列特征,和协会的寄生生活策略。我们还展示了AS如何增强PpSerpin-1蛋白的多样性,参与寄生蜂毒液和幼虫唾液调节宿主免疫。据我们所知,这也代表了第一次在寄生蜂幼虫唾液基因的功能分析。
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. Alternative splicing (AS) and gene duplications (GD) significantly contribute to protein diversity in eukaryotes, yet their interplay and associations with life strategies remain largely understudied. Parasites recruit diverse virulence genes to counter host defenses, providing a unique window into the interplay between AS and GD. Investigating the evolution of the PpSerpin-1 gene (Pteromalus puparum serpin 1) in parasitoids and other insects, we uncovered a negative correlation between AS and GD, distinct sequence features, and associations to the parasitic life strategy. We also demonstrate how AS enhances PpSerpin-1 protein diversity, which participates in parasitoid wasp venom and larval saliva to regulate host immunity. To our knowledge, this also represents the first functional analysis of a larval salivary gene in parasitoid wasps.
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