Compatibility of mycorrhiza-induced resistance with viral and bacterial entomopathogens in the control of Spodoptera exigua in tomato.

BACKGROUND: Arbuscular mycorrhizal fungi (AMF) are soil-borne microorganisms that establish mutualistic associations with roots of most terrestrial plants. This symbiosis results in nutritional and defensive benefits to the host plant, usually conferring protection against biotic stresses, but its indirect impact on third trophic levels is still unknown. In the present work, we explore whether the symbiosis of tomato plants with Funneliformis mosseae (and/or exposition to herbivory) influences the interaction of the generalist pest Spodoptera exigua (Lepidoptera: Noctuidae) with bacterial (Bacillus thuringiensis) and viral (baculovirus, SeMNPV) natural entomopathogens. RESULTS: Symbiosis with AMF and previous herbivory reduces the relative growth of S. exigua, increases its susceptibility to a sublethal dose of B. thuringiensis and has positive or neutral impact on the lethality of SeMNPV. Reduction of the phenoloxidase activity, a marker of the insect immune response, was associated with the larval feeding on plant material previously exposed to herbivory but not to the AMF. In addition, no changes in the insect gut microbiota could be associated with the observed changes in larval growth and susceptibility to the entomopathogens. CONCLUSION: Our findings provide the first evidence of compatibility of AMF symbiosis in tomato with the use of bacterial and viral entomopathogens, contributing to the development of novel approaches to combine the beneficial effect of AMF and entomopathogens in biological pest control. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?

In response to insect herbivory, plants mobilize various defenses. Defense responses include the release of herbivore-induced plant volatiles (HIPVs) that can serve as signals to alert undamaged tissues and to attract natural enemies of the herbivores. Some HIPVs can have a direct negative impact on herbivore survival, but it is not well understood by what mechanisms. Here, we tested the hypothesis that exposure to HIPVs renders insects more susceptible to natural pathogens. Exposure of the caterpillars of the noctuid Spodoptera exigua to indole and linalool, but not exposure to (Z)-3-hexenyl acetate, increased the susceptibility to Spodoptera exiguamultiple nucleopolyhedrovirus (SeMNPV). We also found that exposure to indole, but not exposure to linalool or (Z)-3-hexenyl acetate, increased the pathogenicity of Bacillus thuringiensis Additional experiments revealed significant changes in microbiota composition after forty-eight hours of larval exposure to indole. Overall, these results provide evidence that certain HIPVs can strongly enhance the susceptibility of caterpillars to pathogens, possibly through effects on the insect gut microbiota. These findings suggest a novel mechanism by which HIPVs can protect plants from herbivorous insects.IMPORTANCE Multitrophic interactions involving insect pests, their natural enemies, microorganisms, and plant hosts are increasingly being recognized as relevant factors in pest management. In response to herbivory attacks, plants activate a wide range of defenses that aim to mitigate the damage. Attacked plants release herbivore-induced plant volatiles (HIPVs), which can act as priming signals for other plants and attract natural enemies of herbivores, and which may have a direct negative impact on herbivore survival. In the present work, we show that exposure of the insects to the induced volatiles could increase the insects' susceptibility to the entomopathogens naturally occurring in the plant environment. These findings suggest a novel role for plant volatiles by influencing insect interactions with natural pathogens, probably mediated by alterations in the insect microbiota composition. In addition, this work provides evidence for selectable plant traits (production of secondary metabolites) that can have an influence on the ecology of the pests and could be relevant in the improvement of pest management strategies using natural entomopathogens.