Fungi from the black cutworm Agrotis ipsilon oral secretions mediate plant–insect interactions

It is well known that the interactions of insect herbivores and their host plant can be mediated by microbes. Our central hypothesis is that herbivore-associated fungi might directly or indirectly affect plant–insect interactions. In this study, we identified five orally secreted fungi from field-collected black cutworm, Agrotis ipsilon, including Aspergillus parasiticus, Aspergillus niger, Geotrichum candidum, Fusarium subglutinans, and Mucor circinelloides f. lusitanicus. We found that caterpillars inoculated with F. subglutinans or M. circinelloides f. lusitanicus induced higher defense responses in plants, but with different patterns between different plants. These herbivore-induced defense responses reduced the growth of caterpillars. However, direct application of fungi to mechanically wounded tomato did not induce JA-related defense responses. The application of regurgitant from fungi-inoculated or non-inoculated caterpillars, suggested that regurgitant might be responsible for the fungi-mediated defense response in plants against caterpillar attack. Furthermore, both F. subglutinans and M. circinelloides f. lusitanicus benefited caterpillar growth when they fed on detached tomato leaves, but had no influence when caterpillars fed on artificial diet. Our finding suggests that insect-associated fungi could influence plant–insect interactions by indirectly mediating plant defense responses, and directly affecting caterpillar performance on host plants.