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

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.

Assessment of Sex-Specific Toxicity and Physiological Responses to Thymol in a Common Bean Pest Acanthoscelides obtectus Say

“…Our observation about inhibition of neurotransmitter enzyme AChE and detoxification enzyme GST by thymol in bean weevil females and males agrees with findings of other studies on physiological mechanisms of monoterpenes and essential oils toxicity ( Mojarab-Mahboubkar et al, 2015 ; Liao et al, 2016 , 2017 ; Agliassa and Maffei, 2018 ; Yang et al, 2018 ; Chen et al, 2021 ; Fouad and Abotaleb, 2021 ). Inhibition of AChE leads to accumulation of acetylcholine at nerve synapses, and thus permanent conduction of nerve impulses, ataxia, convulsions and death ( Rattan, 2010 ).…”

“…For instance, bean weevil females exposed to thyme essential oil had lower a level of damaged lipids ( Lazarević et al, 2020 ). In consistence with our results, SOD and CAT were elevated by thymol in Ephestia kuehniella larvae ( Shahriari et al, 2018 ), by carvacrol, p-cymene and γ-terpinene in S. littoralis larvae ( Agliassa and Maffei, 2018 ), by carvacrol in Lymantria dispar larvae ( Chen et al, 2021 ), by ethanolic extract of Acalypha wilkesiana leaves in Callosobruchus maculatus adults ( Oni et al, 2019 ) and by Boswellia carterii EO in adults of two Callosobruchus species ( Kiran et al, 2017 ). SOD and CAT responses to botanicals may vary depending on insect species, duration of exposure, botanical type and concentration.…”

“…EOs and EOs compounds may also decrease the activity of enzymes in the mitochondrial electron transport chain, which further provoke increase in free radicals and oxidative damage to macromolecules ( Pinho et al, 2014 ; da Cunha et al, 2015 ; Kiran et al, 2017 ; Liao et al, 2018 ). To defend from oxidative stress, insects induce various enzymatic and non-enzymatic antioxidants ( da Cunha et al, 2015 ; Kiran and Prakash, 2015a , b ; Agliassa and Maffei, 2018 ; Chen et al, 2021 ). For example, dietary α-pinene, trans-anethole and thymol elevate activities of superoxide dismutase (SOD), catalase (CAT) and glutathione S-transferase (GST) in Ephestia kuehniella Zeller larvae ( Shahriari et al, 2018 ).…”

Integrated view of plant metabolic defense with particular focus on chewing herbivores

“…We have already introduced polyphenols that exert a pro‐oxidant activity in the interior of alkaline insect guts, which can yield a large variety of chemically reactive species (Appel and Martin, 1990). Similarly, ingestion of monoterpenes and sesquiterpenes, abundant in peltate glandular trichomes of oregano ( Origanum vulgare ), caused oxidative stress in S. littoralis larvae, among others, indicated as increase in the insect antioxidant enzyme activities: catalases (CATs), superoxide dismutases (SODs), and glutathione S‐transferases (GSTs) (Agliassa and Maffei, 2018). In case of mitochondrial damage, uncontrolled release of free radicals can be causing unspecific damage to lipids, proteins, and DNA (for detailed review see Bakkali et al, 2008), which is likely to act synergistically with the presence of highly reactive mixture of phenoxyl radicals in the insect digestive tract (Appel and Martin, 1990; reviewed by Sakihama et al, 2002).…”

Origanum vulgare terpenoids modulate Myrmica scabrinodis brain biogenic amines and ant behaviour

“…Therefore, blends of the two terpenoids are mainly emitted when oregano plants respond to the presence of ants. The release of C and T mixtures is more than a generic deterrent signal [41] causing the dispel of some ant species and act as chemical cue manipulating the behavior of Myrmica ant. C and T blends not only decrease the M .…”