Trichoderma atroviride, a maize root associated fungus, increases the parasitism rate of the fall armyworm Spodoptera frugiperda by its natural enemy Campoletis sonorensis

In agroecosystems, herbivore insects damage crops, but in the third trophic level, insects can be parasitized by natural enemies. Trichoderma spp. are common soil and root endophytic fungi that have been widely studied due to their capacity to produce antibiotics, parasitize other fungi and compete with deleterious plant microorganisms. The fall armyworm, Spodoptera frugiperda, is a serious pest of numerous crop plants. In the field, Campoletis sonorensis female wasps parasitize S. frugiperda. Considering these scenarios, it is necessary to look for ecological alternatives for S. frugiperda biocontrol. The aim of this work was to investigate whether Trichoderma atroviride associated with maize roots as part of a multitrophic interaction affects the parasitism rate of C. sonorensis on S. frugiperda. We found that larvae from maize plants whose roots were colonized by T. atroviride were stronger parasitized compared with larvae from non-inoculated plants, indicating that the fungus enhanced the natural mechanism of parasitism. This was correlated with the presence of the low-molecular weight compound 6-pentyl-2H-pyran-2-one (6-PP) released by T. atroviride from the belowground. A pharmacological test showed that 6-PP is an airborne signaling molecule that increased the parasitism rate of C. sonorensis on its enemy. This finding provides new insights into the chemical communication between fungi and insects, and likely represents an inter-kingdom signaling molecule. Furthermore, this study shows a novel role for Trichoderma in multitrophic interactions, and its secondary metabolites in pest control management, presenting an alternative for the biocontrol of S. frugiperda using the combination of T. atroviride and C. sonorensis instead of chemical insecticides.