Flavonoids mediate systemic defenses induced by root feeding in cotton

Plant-herbivore interactions dominate food web links in terrestrial settings, thereby shaping ecosystem structure and functioning. Within a given plant, both primary and secondary metabolites mediate the interplay between above- and below-ground herbivores. Here, we investigate how root feeding by larvae of the turnip moth Agrotis segetum (Lepidoptera: Noctuidae) affects development and feeding behavior of an above-ground sap-feeder i.e., the large cotton aphid Acyrthosiphon gossypii (Hemiptera: Aphididae) on cotton. We further draw upon transcriptomics, metabolomics and in-vitro bioassays to elucidate how plant metabolites mediate these interactions. Root feeding reduces A. gossypii adult survival and fecundity by 35.1%. Aphids on A. segetum-infested cotton spend 7% longer probing cells than on un-infested plants. Root and stem herbivory by A. segetum larvae alters gene transcripts and metabolites in leaves, inducing biosynthesis of three flavonoids i.e., dihydromyricetin, phloridzin and dihydroquercetin. In-vitro bioassays show that the latter two compounds markedly decrease A. gossypii adult survival and fecundity. Below-ground herbivory thus elicits biosynthesis and systemic translocation of phloridzin and dihydroquercetin, with antagonistic effects on above-ground sap-feeders. Our study sheds light on the underlying mechanisms of herbivore-triggered plant defenses in cotton and reveals the interplay between herbivore guilds across ecological realms. We discuss the implications of these findings for pest management.