The temporal pattern of neighboring plant defense response to herbivore-specific plant volatiles

Plants damaged by herbivores with different diet breadth (specialist or generalist) can emit species-specific herbivore-induced plant volatiles (HIPVs). Yet, it remains elusive whether receiver neighboring plants prime their defense responses differentially according to the danger level of the impending insect herbivores of distinct diet breadth, and how effective is defense priming in terms of plant fitness when the actual threats occur as predicted. We investigated how neighboring plants exhibit their defense and their ultimate fitness. We found that the receiver tomato plants exposed to specialist species (Tuta absoluta)-induced volatiles initiated quicker and more vigorous defense responses than the case of generalist (Helicoverpa armigera). The plants exposed to specialist-induced volatiles are more timely to upregulate defense gene expression, increasing trypsin proteinase inhibitor and peroxidas activity and chlorogenic acid accumulation, entailing costs in term of soluble protein content, and inhibiting insect herbivore growth, than the plants exposed to generalist-induced volatiles. Moreover, the plants exposed to specialist-induced volatiles induced higher levels of jasmonic acid compared with those exposed to generalist-induced volatiles. However, the defense priming did not allow the plants exposed to specialist-induced volatiles to obtain fitness benefit in terms of plant growth upon actual herbivore attack, but it did for the plants exposed to generalist-induced volatiles. In conclusion, plants trigger faster and more vigorous defense priming against specialists, but the expectation of benefits is disappointed, compared with the case of generalists. The findings enhance our understanding on plant defense priming mediated by insect herbivore species-specific volatile signals in plant-arthropod communities.