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

Antonino Cusumano,Erik H Poelman,Fabrice Legeai,Serge Urbach,Marc Ravallec,Anne‐Nathalie Volkoff,Marcel Dicke

doi:10.1111/mec.16072

Abstract

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.

Highlights

Plants are at the basis of most terrestrial food webs and interact with various organisms in nature, including herbivorous and carnivorous insects (Schoonhoven et al, 2005; Stam et al, 2014; Turlings & Erb, 2018)
We investigated: (1) whether ichnoviruses are responsible for the majority of the changes occurring in the salivary glands of naturally parasitized caterpillars by using a comparative proteomic approach, (2) whether the performance of unparasitized caterpillars increased when feeding on plants previously treated with insect saliva collected from caterpillars that had been injected with parasitoid calyx fluid containing the ichnovirus
Insect parasitoids have been shown to interact with the plant by influencing plant responses to herbivory as a consequence of the parasitisation of the attacking herbivore (Cuny et al, 2019; Kaplan et al, 2016; Ode et al, 2016; Poelman, Gols et al, 2011; Poelman, Zheng et al, 2011; Tan et al, 2019, 2020)

Summary

| INTRODUCTION

Plants are at the basis of most terrestrial food webs and interact with various organisms in nature, including herbivorous and carnivorous insects (Schoonhoven et al, 2005; Stam et al, 2014; Turlings & Erb, 2018). Bracovirus-mediated changes in plant quality benefit the growth of the caterpillar in which the parasitoid larvae develop, increasing the fitness of the offspring of the bracovirus-injecting parasitoid female (Tan et al, 2018) These discoveries have opened a novel scenario in plant-insect interactions showing that, third-trophic level symbionts do not come directly in contact with the plant, they can still induce changes in plant phenotype, mediated by their effects on the infected caterpillars. We investigated: (1) whether ichnoviruses are responsible for the majority of the changes occurring in the salivary glands of naturally parasitized caterpillars by using a comparative proteomic approach, (2) whether the performance of unparasitized caterpillars increased when feeding on plants previously treated with insect saliva collected from caterpillars that had been injected with parasitoid calyx fluid containing the ichnovirus. | 4569 and (3) whether parasitoid offspring benefitted from plant-mediated ichnovirus-induced manipulation

| MATERIALS AND METHODS

| RESULTS

Findings

| DISCUSSION