Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity

Significance The role of herbivore-associated microbes in mediating plant–herbivore interactions has gained recent attention. We show that a parasitoid associated with its caterpillar host not only suppresses the immune system of the caterpillar but also suppresses the induced defenses of the caterpillar’s host plant. Parasitoids inject eggs into their hosts but also inject polydnaviruses that suppress the caterpillar’s immunity. Immunosuppression enables eggs to hatch and develop as larvae within caterpillars. Additionally, the polydnavirus reduces salivary glucose oxidase, the primary elicitor found in the caterpillar’s oral secretions. Caterpillars injected with polydnavirus induce lower plant defenses than untreated caterpillars. Our results reveal a dimension to the complexity of plant–herbivore interactions indicating that polydnaviruses mediate the phenotypes of the parasitoid, herbivore, and plant.
Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called “polydnaviruses.” Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered.