Callosobruchus maculatus feeding triggers multilevel defenses in cowpea seeds: from germination regulation to defensive metabolite biosynthesis

Abstract

In-depth research has been conducted on plant–herbivore interactions, and most studies on resistance to insects have been focused on plants post-emergence. Currently, little is known about how seeds respond to pest feeding. Understanding how seeds defend against pests is crucial for seed security and agricultural production. Our study revealed that mild infestation by cowpea weevil (Callosobruchus maculatus), a major pest of stored pulses, activated a defense response in stored cowpea seeds. The infestation eliminated the hardseededness and upregulated the germination-prompted genes, thereby increasing the germination rate. Detailed analysis revealed that infestation induced the expression of a series of defense genes, including those involved in the jasmonic acid (JA) signaling pathway and terpenoid synthetic pathway. Transcriptomic and metabolomic analyses identified flavonoid biosynthesis as the primary response in the infested seeds. Specifically, the isoflavonoid biosynthesis was active, with increased expression of corresponding genes and accumulation of metabolites. Further Y-tube olfactometer selection experiments showed that the infested cowpea seeds attracted male insects but repelled females, indicating that pest feeding altered the volatiles emitted by cowpeas. Our findings thus elucidated the interaction between cowpea seeds and the storage pest and indicated that seeds and plants employ similar defense systems against pests. The study also provides theoretical guidance for controlling C. maculatus.