Phenolic Compounds in Red Oak and Sugar Maple Leaves Have Prooxidant Activities in the Midgut Fluids of Malacosoma disstria and Orgyia leucostigma Caterpillars

Abstract

Phenolic compounds are generally believed to be key components of the oxidative defenses of plants against pathogens and herbivores. However, phenolic oxidation in the gut fluids of insect herbivores has rarely been demonstrated, and some phenolics could act as antioxidants rather than prooxidants. We compared the overall activities of the phenolic compounds in red oak (Quercus rubra) and sugar maple (Acer saccharum) leaves in the midgut fluids of two caterpillar species, Malacosoma disstria (phenolic-sensitive) and Orgyia leucostigma (phenolic-tolerant). Three hypotheses were examined: (1) ingested sugar maple leaves produce higher levels of semiquinone radicals (from phenolic oxidation) in caterpillar midgut fluids than do red oak leaves; (2) O. leucostigma maintains lower levels of phenolic oxidation in its midgut fluids than does M. disstria; and (3) phenolic compounds in tree leaves have overall prooxidant activities in the midgut fluids of caterpillars. Sugar maple leaves had significantly lower ascorbate: phenolic ratios than did red oak leaves, suggesting that phenolics in maple would oxidize more readily than those in oak. As expected, semiquinone radicals were at higher steady-state levels in the midgut fluids of both caterpillar species when they fed on sugar maple than on red oak, consistent with the first hypothesis. Higher semiquinone radical levels were also found in M. disstria than in O. leucostigma, consistent with the second hypothesis. Finally, semiquinone radical formation was positively associated with two markers of oxidation (protein carbonyls and total peroxides). These results suggest that the complex mixtures of phenolics in red oak and sugar maple leaves have overall prooxidant activities in the midgut fluids of M. disstria and O. leucostigma caterpillars. We conclude that the oxidative defenses of trees vary substantially between species, with those in sugar maple leaves being especially active, even in phenolic-tolerant herbivore species.

Influence of plant resistance traits in selectiveness and species strength in a tropical plant‐herbivore network

“…Th e resistance value of tannins results from their oxidative activation inside alkaline insect guts ( Ahmad, 1992 ;Appel, 1993 ;Summers and Felton, 1994 ), resulting in cytotoxic effects in their tissues ( Felton et al, 1992 ;Hagerman et al, 2003 ;Barbehenn and Constabel, 2011 ). Specifi cally, the oxidative stress generated by hydrogen peroxide production in the lumen causes lesions in the midgut epithelium ( Barbehenn et al, 2005 ).…”

Cytogenetic, cytotoxic and GC–MS studies on concrete and absolute oils from Taif rose, Saudi Arabia

“…Permeabilization of the outer and inner mitochondrial membranes causes cell death by necrosis and apoptosis (Armstrong 2006;Hussain 2009). Although reduced forms of phytophenolics are powerful antioxidants, the phenoxyl radical produced through antioxidation reactions is a potential prooxidant which may exhibit cytotoxic activity when the life time of a radical is prolonged (Sakihama et al 2002;Burt 2004;Barbehenn et al 2005). In our study phenyl ethanol, one of the phenolic constitutes, comprised of about 33 and 37 % of total volume of the absolute and concrete oil, respectively.…”

Evaluating Ascorbate Oxidase as a Plant Defense Against Leaf-Chewing Insects Using Transgenic Poplar

“…Fourth instars (N=9) fed on the leaf disks for 18-22 hr (18°C), following which the levels of semiquinone radicals in midgut contents, were measured with EPR spectrometry. Sample preparation and EPR analyses were performed as described previously (Barbehenn et al 2005a). Briefly, midgut contents were dissected, weighed in a tared centrifuge tubes containing 300 µl of pH 10 carbonate buffer (containing 10% dimethylsulfoxide), dispersed, and then centrifuged.…”

“…Tree-feeding caterpillars often ingest high levels of phenolic compounds, and an ascorbate-based antioxidant system is central to the defense of caterpillars against the oxidation of these phenolics caused by the high pH of the midgut (Felton and Duffey 1992;Barbehenn et al 2001). In the absence of sufficient ascorbate in the midgut contents, phenolic oxidation produces elevated levels of reactive oxygen species (ROS), including semiquinone radicals, peroxides, and hydroxyl radicals (Barbehenn et al , 2005a. The production of ROS is associated with oxidative damage to nutrients in the gut lumen and oxidative stress in gut tissues (Summers and Felton 1994;Barbehenn et al 2005a).…”

“…In the absence of sufficient ascorbate in the midgut contents, phenolic oxidation produces elevated levels of reactive oxygen species (ROS), including semiquinone radicals, peroxides, and hydroxyl radicals (Barbehenn et al , 2005a. The production of ROS is associated with oxidative damage to nutrients in the gut lumen and oxidative stress in gut tissues (Summers and Felton 1994;Barbehenn et al 2005a). Thus, AO might act synergistically with phenolics to increase their pro-oxidant effects on herbivores.…”