Spodoptera littoralis detoxifies neurotoxic 3-nitropropanoic acid by conjugation with amino acids

Novoselov, Alexey L.; Becker, Tobias; Pauls, Gerhard; Reuß, Stephan H. von; Boland, Wilhelm

doi:10.1016/j.ibmb.2015.05.013

Cited by 12 publications

(14 citation statements)

References 34 publications

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“…These are typical products of phase II detoxification reactions that increase polarity and facilitate excretion. While glucose (Ahmad and Hopkins, 1993;Ahn et al, 2011;Luque et al, 2002;Sasai et al, 2009;Wouters et al, 2014) and amino acid (Konno et al, 1996;Nijhout, 1975;Novoselov et al, 2015;Stauber et al, 2012) conjugates are well known in insects, phosphate metabolites of plant defenses are without precedent.…”

Section: Most Identified Salicinoid Metabolites Are Products Of Phasementioning

confidence: 99%

“…After initial ester cleavage of salicinoids in the gut lumen, the phase II conjugation reactions must take place within cells because these reactions require intracellular enzymes and high energy cellular intermediates, such as UDPG and glutathione, and would not be favored under the typical pH environment of the insect gut. The probable location is the epithelial cells lining the gut lumen, site of many metabolic reactions associated with nutrient digestion, assimilation and detoxification (Appel and Martin, 1990;Novoselov et al, 2015). After conjugation, the polar products can be transported back into the gut lumen for excretion or loaded in the hemolymph.…”

Section: Localization and Transport Of Salicinoid Metabolites In Gypsmentioning

confidence: 99%

“…In addition, they may possess altered target sites that are no longer susceptible to the toxic action of the defense compound (Zhen et al, 2012), or may sequester compounds in a way that avoids intoxication (Opitz and Müller, 2009). Yet most attention has been paid to metabolic transformations that allow herbivores to detoxify defenses and excrete the resulting metabolites (Heckel, 2014;Novoselov et al, 2015). Research on herbivore detoxification of plant defense compounds and insecticides is based on the vast literature on drug metabolism in humans and other animals.…”

Section: Introductionmentioning

confidence: 99%

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Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

Boeckler

Paetz

Feibicke

et al. 2016

Insect Biochemistry and Molecular Biology

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The survival of insect herbivores on chemically defended plants may often depend on their ability to metabolize these defense compounds. However, only little knowledge is available on how insects actually process most plant defense compounds. We investigated the metabolism of salicinoids, a major group of phenolic glycosides in poplar and willow species, by a generalist herbivore, the gypsy moth (Lymantria dispar). Seven salicinoid metabolites identified in gypsy moth caterpillar feces were mostly conjugates with glucose, cysteine or glycine. Two of the glucosides were phosphorylated, a feature not previously reported for insect metabolites of plant defense compounds. The origins of these metabolites were traced to specific moieties of three major poplar salicinoids ingested, salicin, salicortin and tremulacin. Based on the observed metabolite patterns we were able to deduce the initial steps of salicinoid breakdown in L. dispar guts, which involves cleavage of ester bonds. The conjugated molecules were effectively eliminated within 24 h after ingestion. Some of the initial breakdown products (salicin and catechol) demonstrated negative effects on insect growth and survival in bioassays on artificial diets. Gypsy moth caterpillars with prior feeding experience on salicinoid-containing poplar foliage converted salicinoids to the identified metabolites more efficiently than caterpillars pre-fed an artificial diet. The majority of the metabolites we identified were also produced by other common poplar-feeding insects. The conversion of plant defenses like salicinoids to a variety of water-soluble sugar, phosphate and amino acid conjugates and their subsequent excretion fits the general detoxification strategy found in insect herbivores and other animals.

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Section: Most Identified Salicinoid Metabolites Are Products Of Phasementioning

confidence: 99%

Section: Localization and Transport Of Salicinoid Metabolites In Gypsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

Boeckler

Paetz

Feibicke

et al. 2016

Insect Biochemistry and Molecular Biology

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“…derived from glycine 48, alanine 49 and glutamic acid 50, the amides are excreted via the malphigian tubules over the hind gut of the insects. 149 In (leguminous) plants, the ability to detoxify 3-NPA 1 via oxidation probably evolved to protect sensitive tissue from intoxication. 16,150 This oxidation is catalyzed by 3-NPA oxidase, which delivers malonate semialdehyde 33, nitrite, nitrate and hydrogen peroxide (Fig.…”

Section: Detoxication Of 3-npamentioning

confidence: 99%

A tale of four kingdoms – isoxazolin-5-one- and 3-nitropropanoic acid-derived natural products

et al. 2017

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Covering up to September 2016This review reports on natural compounds that derive from the isoxazolinone ring as well as the 3-nitropropanoic acid (3-NPA) moiety. These structural elements occur in compounds that have been identified in plants, insects, bacteria and fungi. In particular, plants belonging to the family of legumes produce such compounds. In the case of insects, isoxazolin-5-one and 3-NPA derivatives were found in leaf beetles of the subtribe Chrysomelina. A number of these natural products have been synthesized so far. In the case of the single compound 3-NPA, several synthetic strategies have been reported and some of the most efficient routes are reviewed. The toxicity of 3-NPA results from its ability to bind covalently to the catalytic center of succinate dehydrogenase causing irreversible inhibition of mitochondrial respiration. As a motif that is produced by many species of plants, leaf beetles and fungi, different detoxification mechanisms for 3-NPA have evolved in different species. These mechanisms are based on amide formation of 3-NPA with amino acids, reduction to β-alanine, ester formation or oxidation to malonic acid semialdehyde. The biosynthetic pathways of 3-NPA and isoxazolin-5-one moieties have been studied in fungi, plants and leaf beetles. In the case of fungi, 3-NPA derives from aspartate, while leaf beetles use essential amino acids such as valine as ultimate precursors. In the case of plants, it is supposed that malonate serves as a precursor of 3-NPA, as indicated by feeding of C-labeled precursors to Indigofera spicata. In other leguminous plants it is suggested that asparagine is incorporated into compounds that derive from isoxazolin-5-one, which was indicated byC-labeled compounds as well. In the case of leaf beetles it was demonstrated that detection of radioactivity after C-labeling from a few precursors is not sufficient to unravel biosynthetic pathways.

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“…3-Nitropropionic acid and its glucose esters have been identified in many members of the legume plant family (Fabaceae) and in certain fungi as a defense against herbivores (Chomcheon et al 2005 ; Francis et al 2013 ; Parry et al 2011 ). Some insect herbivores can detoxify 3-NPA (Johnson et al 2001 ; Majak et al 1998 ; Novoselov et al 2015 ). To date, Chrysomelina leaf beetles are the only insects in which 3-NPA and its derivatives have been described as allomones.…”

Section: Introductionmentioning

confidence: 99%

Two Defensive Lines in Juvenile Leaf Beetles; Esters of 3-nitropropionic Acid in the Hemolymph and Aposematic Warning

et al. 2016

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Juveniles of the leaf beetles in subtribe Chrysomelina have efficient defense strategies against predators. When disturbed, they transiently expose volatile deterrents in large droplets from nine pairs of defensive glands on their back. Here, we report on an additional line of defense consisting of the non-volatile isoxazolin-5-one glucoside and its 3-nitropropanoyl ester in the larval hemolymph. Because isoxazolin-5-one derivatives were not detectable in related leaf beetle taxa, they serve as a diagnostic marker for the Chrysomelina subtribe. Conjugation of isotopically labelled 3-nitropropionic acid to isoxazolin-5-one glucoside in vivo demonstrates its function as a carrier for the 3-nitropropanoyl esters. The previous identification of characteristic glucosides as precursors of the volatile deterrents underlines the general importance of glucosides for sequestration from food plants, and the subsequent transport in the hemolymph to the defense system. The combination of repellent volatiles with non-volatile toxic compounds in the hemolymph has the potential to create synergistic effects since the odorant stimulus may help predators learn to avoid some foods. The combination of the two defense lines has the advantage, that the hemolymph toxins provide reliable and durable protection, while the repellents may vary after a host plant change.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-016-0684-0) contains supplementary material, which is available to authorized users.

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Spodoptera littoralis detoxifies neurotoxic 3-nitropropanoic acid by conjugation with amino acids

Cited by 12 publications

References 34 publications

Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

A tale of four kingdoms – isoxazolin-5-one- and 3-nitropropanoic acid-derived natural products

Two Defensive Lines in Juvenile Leaf Beetles; Esters of 3-nitropropionic Acid in the Hemolymph and Aposematic Warning

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