Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance

Abstract

Jasmonic acid (JA) plays an important role in the induction of herbivore resistance in many plants. However, JA-independent herbivore resistance has been suggested. An herbivore-resistance-inducing substance was isolated from <i>Tobacco mosaic virus</i>-infected tobacco (<i>Nicotiana tabacum</i>) leaves in which a hypersensitive response (HR) was induced and identified as loliolide, which has been identified as a β-carotene metabolite. When applied to tomato (<i>Solanum lycopersicum</i>) leaves, loliolide decreased the survival rate of the two-spotted spider mite, <i>Tetranychus urticae</i>, egg deposition by the same pest, and the survival rate of larvae of the common cutworm <i>Spodoptera litura</i> without exhibiting toxicity against these herbivores. Endogenous loliolide levels increased not only with an infestation by <i>S</i> <i>litura</i> larvae, but also with the exogenous application of their oral secretions in tomato. A microarray analysis identified cell-wall-associated defense genes as loliolide-responsive tomato genes, and exogenous JA application did not induce the expression of these genes. <i>Suppressor of zeaxanthin</i>-<i>less</i> (<i>szl</i>), an Arabidopsis (<i>Arabidopsis thaliana</i>) mutant with a point mutation in a key gene of the β-carotene metabolic pathway, exhibited the decreased accumulation of endogenous loliolide and increased susceptibility to infestation by the western flower thrip (<i>Frankliniella occidentalis</i>). A pretreatment with loliolide decreased susceptibility to thrips in the JA-insensitive Arabidopsis mutant <i>coronatine</i>-<i>insensitive1</i> Exogenous loliolide did not restore reduced electrolyte leakage in <i>szl</i> in response to a HR-inducing bacterial strain. These results suggest that loliolide functions as an endogenous signal that mediates defense responses to herbivores, possibly independently of JA, at least in tomato and Arabidopsis plants.