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

Abstract

ORCID ID: 0000-0003-4940-288X (S.S.). 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 Tobacco mosaic virusinfected tobacco (Nicotiana tabacum) leaves in which a hypersensitive response (HR) was induced and identified as loliolide, which has been identified as a b-carotene metabolite. When applied to tomato (Solanum lycopersicum) leaves, loliolide decreased the survival rate of the two-spotted spider mite, Tetranychus urticae, egg deposition by the same pest, and the survival rate of larvae of the common cutworm Spodoptera litura without exhibiting toxicity against these herbivores. Endogenous loliolide levels increased not only with an infestation by S. litura 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. Suppressor of zeaxanthin-less (szl), an Arabidopsis (Arabidopsis thaliana) mutant with a point mutation in a key gene of the b-carotene metabolic pathway, exhibited the decreased accumulation of endogenous loliolide and increased susceptibility to infestation by the western flower thrip (Frankliniella occidentalis). A pretreatment with loliolide decreased susceptibility to thrips in the JA-insensitive Arabidopsis mutant coronatine-insensitive1. Exogenous loliolide did not restore reduced electrolyte leakage in szl 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.

α-Ionone, an Apocarotenoid, Induces Plant Resistance to Western Flower Thrips, Frankliniella occidentalis, Independently of Jasmonic Acid

“…To examine the effects of apocarotenoids on herbivores, we released adult female western flower thrips onto micro-tom tomato (Solanum lycopersicum) leaves that were treated with β-cyclocitral, α-ionone, or β-ionone. Since loliolide effectively decreased the susceptibility to western flower thrips at 300 µM when applied to Arabidopsis leaves [5], we used concentrations of 300 µM or lower for β-cyclocitral, α-ionone, and β-ionone. The treatment with α-ionone at 300 µM decreased the number of eggs laid by the pest (Figure 1; p < 0.05, F = 2.800).…”

“…Molecules 2019, 24, x FOR PEER REVIEW 2 of 10 carotene [5,[8][9][10]. The degradation of α-and β-carotenes also results in the production of other apocarotenoids, such as β-cyclocitral, α-ionone, and β -ionone [11].…”

“…The above results suggested that reductions in the survival of western flower thrips and egg deposition by the same pest on tomato leaves were due to host defense responses induced by exogenously applied α-ionone. To gain insights into the α-ionone-induced defense mechanism, we analyzed the induction kinetics of herbivore-responsive tomato genes, such as those encoding proteinase inhibitor II (SlPin2) [21], leucine aminopeptidase (SlLapA1) [22], acidic chitinase (SlChi3) [23], basic chitinase (SlChi9) [23], basic β-1,3-glucanase (SlGluB), and cell-wall invertase (SlLin5) [5]. Tomato plants were exposed to α-ionone vapor for 24 h, and the expression levels of these marker genes in the treated leaves were examined by real-time PCR.…”

“…We recently demonstrated that loliolide induced resistance to multiple herbivore pests, such as the two-spotted spider mite (Tetranychus urticae), western flower thrips (Frankliniella occidentalis), and common cutworm (Spodoptera litura), through the activation of JA-independent defense responses [5]. Loliolide has also been shown to function as an allelochemical in plant-plant communications [6,7].…”

“…Loliolide has also been shown to function as an allelochemical in plant-plant communications [6,7]. Loliolide is produced via the chemical or enzymatic degradation process of α-carotene and β-carotene [5,[8][9][10]. The degradation of αand β-carotenes also results in the production of other apocarotenoids, such as β-cyclocitral, α-ionone, and β -ionone [11].…”