The jasmonate pathway alters herbivore feeding behaviour: consequences for plant defences

The jasmonate pathway is a highly conserved defensive cascade in plants that regulates the induction of resistance against herbivores; however, its role in herbivore feeding behaviour remains unknown. We used a mutant tomato plant ( def -1) deficient in the production of jasmonate-related defensive proteins to test the hypothesis that genotypes with a reduced ability to induce resistance have a higher and more concentrated pattern of herbivore damage. Wild-type and def -1 plants received either damage by Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) caterpillars or no damage. After treatment, we tested for systemic responses by allowing a free roaming S. exigua caterpillar to feed on the undamaged portions of plants. Weight-gain and leaf consumption of S. exigua were highest on def -1 plants, regardless of prior herbivore damage. Def -1 plants also had fewer numbers of leaves and leaflets eaten, and fewer feeding holes, which was indicative of a more concentrated distribution of damage on mutant compared to wild-type plants. Following these results, we mimicked the amount and distribution of feeding damage that wild-type or jasmonate-deficient plants would receive on wild-type plants to test whether changes in feeding behaviour may feedback to influence the expression of induced resistance. We mimicked the distribution of damage in wild-type and jasmonate-deficient plants by allowing caterpillars to feed on either one (leaf 1 or 2) or two leaves (leaf 1 and 2). Increased herbivore damage resulted in higher proteinase inhibitor (PI) activity, a jasmonate-regulated defensive protein, and lower S. exigua performance on wild-type but not jasmonate-deficient plants. Compared to undamaged plants, a concentrated pattern of herbivore damage increased systemic resistance; these induced responses were greater on leaflets with stronger vascular connections to the damaged leaf. A more dispersed pattern of caterpillar damage altered the expression of induced responses, but the outcome depended on the specific pattern of damage. When leaf 1 was damaged and then leaf 2, the undamaged (third) leaf (which is more strongly connected to leaf 1 than 2) expressed reduced the PI activity compared to plants receiving concentrated damage to leaf 1; whereas in plants where leaf 2 was first damaged and then leaf 1, there were no differences in PI activity in leaf 3 compared to plants receiving concentrated damage to leaf 2. Thus, induction of the jasmonate pathway may not only determine the amount and distribution of feeding damage by herbivores, but this may feedback to affect the subsequent expression of plant defence.