Origanum vulgare Terpenoids Induce Oxidative Stress and Reduce the Feeding Activity of Spodoptera littoralis.

Chiara Agliassa,Massimo Maffei

doi:10.3390/ijms19092805

Chiara Agliassa, Massimo Maffei

Open Access

https://doi.org/10.3390/ijms19092805

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Abstract

Terpenoids are toxic compounds produced by plants as a defense strategy against insect herbivores. We tested the effect of Origanum vulgare terpenoids on the generalist herbivore Spodoptera littoralis and the response of the plant to herbivory. Terpenoids were analyzed by GC-FID and GC-MS and quantitative gene expression (qPCR) was evaluated on selected plant genes involved in both terpene biosynthesis. The insect detoxification response to terpenes was evaluated by monitoring antioxidant enzymes activity and expression of insect genes involved in terpene detoxification. O. vulgare terpenoid biosynthesis and gene expression was modulated by S. littoralis feeding. The herbivore-induced increased level of terpenoids (particularly carvacrol and p-cymene) interacted with the herbivore by decreasing larval survival and growth rate. The assimilation by S. littoralis of more than 50% of ingested terpenes correlated with the possible toxic effects of O. vulgare terpenoids. In choice test experiments, carvacrol and γ-terpinene mediated the larval feeding preferences, wherease the prolonged feeding on O. vulgare terpenoids (particularly on γ-terpinene) exerted relevant antinutritional effects on larvae. S. littoralis was found to react to O. vulgare terpenoids by increasing its antioxidant enzymes activities and gene expression, although this was not sufficient to sustain the toxicity of O. vulgare terpenoids.

Highlights

Terpenoids constitute the largest and most heterogeneous class of secondary metabolites, and include monoterpenes and sesquiterpenes as volatile constituents [1,2]
After several trials we found that the 2nd and 3rd instar larvae showed a higher sensitivity to O. vulgare terpenoids; we used these two instar stages for all tests and measurements were performed during transition from one instar to the one
The feeding activity of the generalist S. littoralis increased the expression of O. vulgare DXS, a gene involved in the early steps of terpenoid biosynthesis for the mevalonate-independent (MEP)-pathway gene, the product of which is considered to catalyze one of the rate-limiting steps of this pathway [33] as well as GPPS, whose overproduction is expected to result in increased production of monoterpene end products [34]

Summary

Introduction

Terpenoids constitute the largest and most heterogeneous class of secondary metabolites, and include monoterpenes and sesquiterpenes as volatile constituents [1,2] These volatile terpenoids can act both as constitutive and herbivory-induced (Herbivore-Induced Plant Volatiles, HIPVs) defense compounds. Phytophagous insects represent one of the major causes of biotic stress for plants [12] and herbivore attack can cause both quantitative and qualitative changes in the composition of HIPVs [2,13,14,15] Monoterpenes such as thymol and carvacrol show LD50 values of 25 and 43 μg·larvae−1, respectively, when tested on early four-instar Spodoptera litura and the LD50 of these monoterpenes increases with the larval development [16]. The mode of action of these monoterpenes on herbivores is not fully understood, they have been found to elicit insect detoxification enzymes [21,25,26] and other mechanisms of tolerance [27]

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