Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect

Plants emit specific blends of volatile organic compounds (VOCs) that serve as multitrophic, multifunctional signals. Fungi colonizing aboveground (AG) or belowground (BG) plant structures can modify VOC patterns, thereby altering the information content for AG insects. Whether AG microbes affect the emission of root volatiles and thus influence soil insect behaviour is unknown. The endophytic fungus Neotyphodium uncinatum colonizes the aerial parts of the grass hybrid Festuca pratensis x Lolium perenne and is responsible for the presence of insect-toxic loline alkaloids in shoots and roots. We investigated whether endophyte symbiosis had an effect on the volatile emission of grass roots and if the root herbivore Costelytra zealandica was able to recognize endophyte-infected plants by olfaction. In BG olfactometer assays, larvae of C. zealandica were more strongly attracted to roots of uninfected than endophyte-harbouring grasses. Combined gas chromatography-mass spectrometry and proton transfer reaction-mass spectrometry revealed that endophyte-infected roots emitted less VOCs and more CO2. Our results demonstrate that symbiotic fungi in plants may influence soil insect distribution by changing their behaviour towards root volatiles. The well-known defensive mutualism between grasses and Neotyphodium endophytes could thus go beyond bioactive alkaloids and also confer protection by being chemically less apparent for soil herbivores.