Herbivore identity and intensity interact to influence plant metabolic response to herbivory

Herbivore identity and intensity are important in mediating plant defense responses, but the effects of their interaction on the plant metabolome have not yet been fully explored. Here, gas chromatography mass spectrometry was utilized to detect the metabolic changes in leaves, stems and roots of the common reed Phragmites australis infested with different intensity combinations of leaf-chewing Laelia coenosa and stem piercing-sucking Dimorphopterus pallipes. The supervised partial least squares-discriminant analysis showed that feeding by the two insects distinctly changed the metabolic profiles of all plant tissues. Furthermore, different intensities of the two herbivores resulted in significantly different metabolites in leaves. Only a high intensity of D. pallipes activated a distinct metabolic profile in roots, whereas there was no difference in stem metabolites in response to different herbivore intensities. Significant combined feeding effects of the two herbivores on plant metabolic composition was only detected in leaves infested with high herbivore intensity. Generally, D. pallipes feeding had a stronger effect on metabolite contents in different tissues compared to L. coenosa feeding. There was mostly a linear relationship between responses of leaf metabolites and herbivore intensity, whereas root metabolites generally showed non-linear responses to herbivore intensity. Additionally, there were significant interactions during simultaneous feeding of the two herbivores in leaves, which tended to be antagonistic. In general, our study suggested that plant responses to herbivory vary among tissues and are affected differently based on herbivore identity and intensity, which may vary in their interactions on plant metabolites at the whole-plant level.