Plant-phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars

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 harbor a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behavior. 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 ichnoviruses-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.

学界日益认识到，植物与昆虫间的互作可由微生物共生体（microbial symbionts）介导。然而，目前仅在少数与寄生蜂相关的茧蜂病毒（bracoviruses）相关案例中，才有证据表明，源自第二营养级（trophic level）以外生物的共生体能够影响植物-昆虫间的互作。昆虫寄生蜂（parasitoid）携带有多种多样的共生体，与茧蜂病毒类似，这些共生体可被注入植食性宿主体内，以调控宿主的生理与行为。但这类共生体在以植物为基础的食物网中的功能，在很大程度上仍未得到充分研究。本研究首次提供证据表明，一类与寄生蜂相关的姬蜂病毒（ichnoviruses）类共生体，能够调控植物-昆虫互作的强度。比较蛋白质组学（proteomic）分析显示，当寄生蜂注入含有姬蜂病毒颗粒的萼液（calyx fluid）后，毛虫（caterpillar）唾液腺的组成会发生定性与定量双重改变：定性层面表现为两种病毒编码蛋白的出现，定量层面则体现为多种毛虫内源酶的丰度变化，其中包括葡萄糖氧化酶（glucose oxidase）这类激发子（elicitors）。反过来，由毛虫口腔分泌物（oral secretions）组成改变所诱导的植物表型（plant phenotypic）变化，会对植食性昆虫的生存适合度产生影响。姬蜂病毒通过调控植物对植食作用（herbivory）的响应，使其寄生蜂宿主在被寄生毛虫体内的发育时长缩短，从而为共生的寄生蜂带来益处。值得注意的是，植物介导的姬蜂病毒诱导效应，还能提升未被寄生的植食性昆虫的生存适合度——在自然环境中，这类昆虫往往与被寄生的个体共享寄主植物。本研究结合寄生蜂的病毒共生体对植物造成的生态成本，对上述发现展开了讨论。本研究揭示了食肉动物相关共生体在植物-昆虫-寄生蜂系统中所发挥的作用，为相关领域提供了极具启发性的全新发现，同时也强调了从生态学视角解读互利共生（mutualistic associations）关系的重要性。