How do insect herbivores cope with the extreme oxidative stress of phototoxic host plants?

Abstract

Plants of the Asteraceae and Hypericaceae possess secondary compounds that induce photooxidation in insect herbivores that consume them. One of the well-established modes of action of these substances is peroxidation of membrane lipids. Some herbivores counteract these defences by avoidance of light and tissues rich in phototoxins or the ability to detoxify these secondary substances. The cytochrome P-450 polysubstrate monooxygenase systems involved, the metabolic products, and a new putative toxin pump have been described. Dietary antioxidants (β-carotene, vitamin E, ascorbate) are additional defences against phototoxicity. They reduce mortality in herbivores exposed to phototoxins and some specialist herbivores have high constitutive levels. Adapted specialist insects also have higher constitutive levels of superoxide dismutase (SOD) and respond to phototoxins in their diet by the induction of catalase (CAT), glutathione reductase (GR), and increased levels of reduced glutathione (GSH). Artificial inhibition of the enzymes SOD and CAT had little effect on phototoxicity but inhibition of GSH synthesis in herbivores enhanced photooxidative effects of administered phototoxins on lipid peroxidation. While insects have many mechanisms to overcome plant photooxidants, the Asteraceae appear to have adopted a strategy of counterattack. We suggest and provide preliminary evidence that a second group of secondary substances, the sesquiterpene lactones, occurring in the Asteraceae can attack key antioxidant defences to synergise phototoxins. © 1995 Wiley-Liss, Inc.

Reconfiguration of the immune system network during food limitation in the caterpillarManduca sexta

“…Although GSH is not typically thought of as part of the immune response, it plays a key role in buffering animals against both pathogen toxins (Aucoin et al, 1995) and the oxidative stress that can be generated by PO activity (Clark et al, 2010). We include it here as a likely component of 'infection tolerance' (Stahlschmidt et al, 2015).…”

A Pharm-Ecological Perspective of Terrestrial and Aquatic Plant-Herbivore Interactions

“…Some PSMs are known to have highly specific targets such as the inhibition of Na + /K + ATPase by cardenolides (Petschenka et al 2012) and cardiac glycosides (Holzinger et al 1996) and inhibition of succinate dehyrogenase by papyriferic acid from birch (Forbey et al, 2011;McLean et al, 2009). Other PSMs interact with nutrients to cause broad pharmacological responses such as oxidative stress (Aucoin et al, 1995) or work synergistically with other PSMs to elicit responses (Guillet et al, 2000;Wen et al 2006). Others may exert their effects indirectly through multiple pathways.…”

Cytotoxicity and drug potentiating activity of phenylheptatriyne

“…Previous work with PHT demonstrated phototoxicity in insect models to be inhibited by increased activity of endogenous superoxide dismutase (SOD) and when supplemented with the lipid soluble antioxidants, a-tocopherol and /Lcarotene (Aucoin et al, 1995). Insects also show effects of lipid peroxidation if glutathione (GSH) is inhibited before administering PHT and irradiating with UVA.…”

“…The cytotoxicity of fatty acids and photoexcited PHT is inhibited in systems enriched with certain enzymatic and nonenzymatic antioxidants Aucoin et al, 1995). PHT phototoxicity is inhibited by increased superoxide dismutase (SOD) activity and exogenous or-tocopherol and fi-carotene (Aucoin et al, 1995).…”

“…PHT phototoxicity is inhibited by increased superoxide dismutase (SOD) activity and exogenous or-tocopherol and fi-carotene (Aucoin et al, 1995). Insects that specialize on phototoxic host plants possess high constitutive levels of the lipid soluble antioxidants but also over-express enzymes involved in the detoxifícation of highly reactive, oxygen species.…”