Belowground mutualists modulate growth and aboveground defense in potato: insights from mycorrhizal and entomopathogenic nematode interactions

Soil application of entomopathogenic nematodes enhanced the growth and modulated the aboveground defenses in potato plants, while interactions with mycorrhizal fungi shaped the volatile emissions and herbivory, underscoring the nematodes as primary drivers in multi-mutualistic systems. Plants frequently engage with multiple belowground mutualists simultaneously, yet the outcomes of such multi-partner associations for plant traits and herbivore resistance remain poorly understood. In this study, we investigated the independent and combined effects of arbuscular mycorrhizal fungi (AMF; Rhizophagus irregularis) and entomopathogenic nematodes (EPNs; Steinernema carpocapsae and Heterorhabditis bacteriophora) on the growth and defense phenotype of potato (Solanum tuberosum) plants. Using a fully factorial experimental design, we assessed the plant height, foliar phenolic content, constitutive volatile organic compound (VOC) emissions, and leaf damage by chewing herbivores. We found that EPNs alone enhanced plant height and reduced flavonoid concentrations, consistent with a potential shift in growth-defense allocation. AMF inoculation had no significant main effects on any measured trait but interacted with EPNs in a species-specific manner. Notably, mycorrhization increased VOC emission only in the presence of H. bacteriophora, while co-inoculation with AMF and S. carpocapsae significantly reduced herbivore damage-a response not observed in either single-symbiont treatment. These findings highlight the non-additive and context-dependent nature of belowground mutualist interactions, with distinct outcomes governed by the identity of the EPN. To our knowledge, this is among the first documented cases where aboveground herbivory is attenuated through a context-specific interaction between two root-associated mutualists. Overall, our results highlight the ecological significance of considering species-specific, multi-mutualist interactions in shaping plant traits and suggest that combining functionally distinct symbionts may offer a novel approach to enhancing crop resilience in sustainable agriculture.