There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant-insect interactions are restricted to a few cases belonging to parasitoid-associated bracoviruses. Insect parasitoids harbour a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behaviour. Yet, the function of these symbionts in plant-based trophic webs remains largely overlooked. Here, we provide the first evidence of a parasitoid-associated symbiont belonging to the group of ichnoviruses which affects the strength of plant-insect interactions. A comparative proteomic analysis shows that, upon parasitoid injection of calyx fluid containing ichnovirus particles, the composition of salivary glands of caterpillars changes both qualitatively (presence of two viral-encoded proteins) and quantitatively (abundance of several caterpillar-resident enzymes, including elicitors such as glucose oxidase). In turn, plant phenotypic changes triggered by the altered composition of caterpillar oral secretions affect the performance of herbivores. Ichnovirus manipulation of plant responses to herbivory leads to benefits for their parasitoid partners in terms of reduced developmental time within the parasitized caterpillar. Interestingly, plant-mediated ichnovirus-induced effects also enhance the performances of unparasitized herbivores which in natural conditions may feed alongside parasitized ones. We discuss these findings in the context of ecological costs imposed to the plant by the viral symbiont of the parasitoid. Our results provide intriguing novel findings about the role played by carnivore-associated symbionts on plant-insect-parasitoid systems and underline the importance of placing mutualistic associations in an ecological perspective.

中文翻译：

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寄生鱼科病毒诱导的植物表型变化增强了未寄生和寄生毛虫的性能

人们越来越意识到植物和昆虫之间的相互作用可以由微生物共生体介导。尽管如此，证据表明与第二营养级以外的生物体相关的共生体影响植物-昆虫的相互作用仅限于少数属于寄生蜂相关短臂病毒的病例。昆虫寄生物拥有多种共生体，与短杆状病毒一样，它们可以被注射到它们的食草宿主中来操纵它们的生理和行为。然而，这些共生体在基于植物的营养网中的功能在很大程度上仍被忽视。在这里，我们提供了属于影响植物与昆虫相互作用强度的 ichnoviruses 组的寄生蜂相关共生体的第一个证据。比较蛋白质组学分析表明，在寄生蜂注射含有 ichnovirus 颗粒的花萼液后，毛毛虫唾液腺的组成在质量上（存在两种病毒编码蛋白）和数量上发生了变化（存在多种毛毛虫驻留酶，包括诱导子，如葡萄糖氧化酶）。反过来，由毛虫口腔分泌物组成的改变引发的植物表型变化会影响食草动物的表现。Ichnovirus 操纵植物对食草动物的反应，在减少寄生毛虫的发育时间方面为其寄生伙伴带来好处。有趣的是，植物介导的 ichnovirus 诱导的作用也增强了未寄生的食草动物的表现，这些食草动物在自然条件下可能与寄生的食草动物一起进食。我们在寄生蜂的病毒共生体强加给植物的生态成本的背景下讨论这些发现。我们的研究结果提供了关于食肉动物相关共生体在植物-昆虫-寄生物系统中所起作用的有趣的新发现，并强调了将互惠关联置于生态角度的重要性。