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

Gary Felton, K. Donato, R. J. Del Vecchio, S. S. Duffey

Research output: Contribution to journalArticle

310 Citations (Scopus)

Abstract

The foliage and fruit of the tomato plant Lycopersicon 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 fruitworm Heliothis zea or the beet army-worm Spodoptera 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 by o-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.

Original languageEnglish (US)
Pages (from-to)2667-2694
Number of pages28
JournalJournal of Chemical Ecology
Volume15
Issue number12
DOIs
StatePublished - Dec 1 1989

Fingerprint

Catechol Oxidase
Herbivory
Nutritive Value
Lycopersicon esculentum
catechol oxidase
foliage
Insects
Fruits
herbivore
Oxidoreductases
herbivores
fruit
Chemical activation
Fruit
insect
insects
alkylation
amino acid
tomatoes
fruits

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry

Cite this

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title = "Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores",
abstract = "The foliage and fruit of the tomato plant Lycopersicon 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 fruitworm Heliothis zea or the beet army-worm Spodoptera 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 by o-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.",
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Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. / Felton, Gary; Donato, K.; Del Vecchio, R. J.; Duffey, S. S.

In: Journal of Chemical Ecology, Vol. 15, No. 12, 01.12.1989, p. 2667-2694.

Research output: Contribution to journalArticle

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