Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores

Abstract

The foliage and fruit of the tomato plantLycopersicon esculentum contains polyphenol oxidases (PPO) and peroxidases (POD) that are compartmentally separated from orthodihydroxyphenolic substrates in situ. However, when leaf tissue is damaged by insect feeding, the enzyme and phenolic substrates come in contact, resulting in the rapid oxidation of phenolics to orthoquinones. When the tomato fruitwormHeliothis zea or the beet army-wormSpodoptera exigua feed on tomato foliage, a substantial amount of the ingested chlorogenic acid is oxidized to chlorogenoquinone by PPO in the insect gut. Additionally, the digestive enzymes of the fruitworm have the potential to further activate foliar oxidase activity in the gut. Chlorogenoquinone is a highly reactive electrophilic molecule that readily binds cova-lently to nucleophilic groups of amino acids and proteins. In particular, the -SH and -NH2 groups of amino acids are susceptible to binding or alkylation. In experiments with tomato foliage, the relative growth rate of the fruitworm was negatively correlated with PPO activity. As the tomato plant matures, foliar PPO activity may increase nearly 10-fold while the growth rate of the fruitworm is severely depressed. In tomato fruit, the levels of PPO are highest in small immature fruit but are essentially negligible in mature fruit. The growth rate of larvae on fruit was also negatively correlated with PPO activity, with the fastest larval growth rate occurring when larvae fed on mature fruit. The reduction in larval growth is proposed to result from the alkylation of amino acids/protein byo-quinones, and the subsequent reduction in the nutritive quality of foliage. This alkylation reduces the digestibility of dietary protein and the bioavailability of amino acids. We believe that this mechanism of digestibility reduction may be extrapolatable to other plant-insect systems because of the ubiquitous cooccurrence of PPO and phenolic substrates among vascular plant species.

Plant Leucine Aminopeptidases Moonlight as Molecular Chaperones to Alleviate Stress-induced Damage

“…Many defense proteins exert their effects within the insect gut by inhibiting the activity of digestive enzymes or reducing the quality of the leaf diet by removing essential amino acids or cross-linking proteins (61)(62)(63)(64). Lepidopteran midguts are alkaline (65), and due to LAP-A hyperstability within insect digestive track and frass and its alkaline pH optima (30,66), it has been proposed that LAP-A may degrade peptides within the insect midgut (30,32).…”

Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees

“…in the midgut of caterpillars), some phenolics, such as ellagitannins, auto-oxidize into quinones that are highly reactive and also toxic compounds (Barbehenn et al 2006). Quinones form covalent bonds with nucleophilic moieties of biomolecules, such as the functional groups of amino acids and proteins, making them indigestible (Felton et al 1989). The oxidation of phenolics may also occur by enzymatic reactions catalyzed by plant polyphenol oxidases (PPOs) and peroxidases (PODs) (Felton et al 1989;Felton and Duffey 1991;Bi and Felton 1995).…”

Polyphenoloxidase Silencing Affects Latex Coagulation in Taraxacum Species

“…PPOs are found throughout the plant kingdom (Mayer and Harel, 1979;Vaughn and Duke, 1984;Mayer, 1987;Vaughn et al, 1988;Sherman et al, 1991), and they probably play a role in defense against pathogens and herbivores (Vö rö s et al., 1957;Felton et al, 1989;Duffey and Felton, 1991;Constabel and Ryan, 1998;Stout et al, 1999;Gatehouse, 2002). They are plastid-localized copper metalloenzymes that catalyze the oxidation of o-diphenols to o-diquinones (diphenolase activity; EC 1.10.3.2) and, in some species, also the o-hydroxylation of monophenols (monophenolase activity; EC 1.14.18.1; Vaughn et al, 1988;Mayer, 2006).…”