Exposure to herbivore-induced plant volatiles primes JA-dependent gossypol defenses in cotton

Herbivore-induced plant volatiles (HIPVs) are known to prime neighboring plants for enhanced defense, but the molecular basis for this phenomenon remains poorly understood, particularly in cotton. Here, we demonstrate for cotton plants that exposure to volatiles induced by the cotton bollworm (Helicoverpa armigera Hübner; CBW), enhances resistance against subsequent CBW attack, as evidenced in both laboratory and semi-field trials. While HIPV exposure alone did not elicit direct defense activation, it primed the jasmonic acid (JA) signaling pathway, leading to accelerated induction of JA biosynthesis genes and elevated JA accumulation upon herbivory. That this primed resistance is JA-dependent, was confirmed by treating HIPV-exposed plants with JA biosynthesis inhibitors, which completely abolished the priming effects. We further found that HIPV-primed plants exhibited significantly higher accumulation of the key defensive metabolite gossypol following larval feeding. The role of gossypol-reliant defenses was confirmed by using a glandless cotton mutant (gl2gl2gl3gl3) deficient in gossypol and related terpenoid aldehydes. The combined results reveal that CBW-induced volatiles prime anti-herbivore resistance in cotton by potentiating the JA signaling pathway, which in turn enhances gossypol biosynthesis upon actual herbivore attack. This new insight into the physio-ecological mechanisms underlying airborne defense priming in cotton also highlights its potential application in sustainable pest management.