Root exudates from maize plants with high levels of foliar herbivory alters beneficial plant fungus growth

Abstract

Plant roots have developed complex interactions with microbes to resist stressful growth conditions. Therefore, root exudation is important for determining rhizosphere microbial community structure. However, the shoot/root dynamics of metabolites at different degrees of herbivory and their effects on the growth of rhizosphere microorganisms remain poorly explored. Here, we identified some of the chemical components that coordinate the interactions between maize (Zea mays) plants, the chewing insect Spodoptera frugiperda, and the rhizosphere fungus Trichoderma atroviride. The results showed that during herbivory the leaf area and biomass parameters decreased proportionally with the number of pests feeding on the shoots, and phenotypic alterations in maize were correlated with changes in the root exudation of compounds. Bioassays with root exudates from leaves with mechanical damage and oral secretions of S. frugiperda suggested that Trichoderma specifically responds to the presence of larvae in maize plants. Furthermore, the degree of herbivory modulated the content of non-structural carbohydrates (NSCs), the anti-herbivore compound 6-methoxy-2-benzoxazolin-2-one (MBOA), and the reactive oxygen species H2O2 in the root exudates, which affected the growth of T. atroviride in a dose-dependent manner. These results revealed that foliar herbivory and the degree of damage can modulate, at least in part, three fundamental aspects of multitrophic interactions: (i) both the leaf area and biomass of the plant host, (ii) root exudates, and (iii) T. atroviride growth.