Flood-Induced Insect Resistance in Maize Involves Flavonoid-Dependent Salicylic Acid Induction

Plants have evolved the ability to respond to a diverse range of biotic and abiotic stresses. Often, combining these stresses multiplies the challenge for the plants, but occasionally the combined stress can induce unexpected synergistic defences. In maize, combined flooding and herbivory induces a salicylic acid (SA)-dependent defence against Spodoptera frugiperda (fall armyworm). In this study we used RNAseq and metabolic profiling to show that flavonoids are involved in maize response to combined flooding and herbivory. To assess the role of flavonoids in flood-induced S. frugiperda resistance, we analyzed the maize idf mutant that has compromised expression of chalcone synthase, the first enzyme in flavonoid biosynthesis. This flavonoid-deficient mutant was compromised both in flood-induced S. frugiperda resistance and in SA accumulation. These data revealed an unexpected requirement for flavonoids in SA induction. In contrast to idf, the flavonoid 3' hydroxylase mutant, pr1, showed enhanced SA accumulation after combinatorial treatment, which closely correlated with elevated levels of select flavonoids and the dihydroflavonol reductase, anthocyaninless1 (a1) mutant, was unaffected in its SA-induction. These data indicate that specific flavonoids likely play a role in flood-induced SA accumulation and S. frugiperda resistance.