A mode of action of glucosinolate-derived isothiocyanates: Detoxification depletes glutathione and cysteine levels with ramifications on protein metabolism in Spodoptera littoralis

Jeschke, Verena; Gershenzon, Jonathan; Vassão, Daniel Giddings

doi:10.1016/j.ibmb.2016.02.002

Cited by 73 publications

(100 citation statements)

References 75 publications

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“…Upon tissue rupture, glucosinolates are hydrolyzed by myrosinases, and the unstable aglucones spontaneously degrade to highly reactive isothiocyanates, which act as direct defenses against microbial pathogens and herbivores ( Fig. 7b; Agrawal & Kurashige, 2003;Bednarek et al, 2009;Fan et al, 2011;Jeschke et al, 2016).…”

Section: Glucosinolate Hydrolases (Myrosinases) In Plants and Insectsmentioning

confidence: 99%

Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

et al. 2019

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Summary Despite the phylogenetic distance between plants and insects, these two groups of organisms produce some secondary metabolites in common. Identical structures belonging to chemical classes such as the simple monoterpenes and sesquiterpenes, iridoid monoterpenes, cyanogenic glycosides, benzoic acid derivatives, benzoquinones and naphthoquinones are sometimes found in both plants and insects. In addition, very similar glucohydrolases involved in activating two‐component defenses, such as glucosinolates and cyanogenic glycosides, occur in both plants and insects. Although this trend was first noted many years ago, researchers have long struggled to find convincing explanations for such co‐occurrence. In some cases, identical compounds may be produced by plants to interfere with their function in insects. In others, plant and insect compounds may simply have parallel functions, probably in defense or attraction, and their co‐occurrence is a coincidence. The biosynthetic origin of such co‐occurring metabolites may be very different in insects as compared to plants. Plants and insects may have different pathways to the same metabolite, or similar sequences of intermediates, but different enzymes. Further knowledge of the ecological roles and biosynthetic pathways of secondary metabolites may shed more light on why plants and insects produce identical substances.

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Section: Glucosinolate Hydrolases (Myrosinases) In Plants and Insectsmentioning

confidence: 99%

Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

et al. 2019

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“…To functionally test how plant-derived chemicals drove gene family dynamics in S. flava , we first focused on its interactions with the glucosinolate (GSL)-myrosinase system (the "mustard oil bomb"; (40) ), which is the principal chemical defense system in the Brassicales. GSLs are amino-acid derived molecules that are hydrolyzed upon tissue damage, forming highly electrophilic and insecticidal isothiocyanates (ITCs or mustard oils) (41,42) . Ingestion of mustard oils or exposure to mustard oil vapor slows growth and is highly toxic to insects, including D. melanogaster (43,44) .…”

Section: Accelerated Duplications and Evolution Of A Key Detoxificatimentioning

confidence: 99%

Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

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SIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly ( Drosophila melanogaste r), the "wasabi fly" ( Scaptomyza flava ), that evolved to consume mustard plants including Arabidopsis thaliana . The yeast-to-mustard dietary transition remodeled the fly's gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals. Gloss et al. 2019 1ABSTRACT One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana ) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila . We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains ("blooms") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase ( Gst ) and cytochrome P450 ( Cyp450 ) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1 ) and Gst (N=5 for GstE5-8 ) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro . One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis , helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.

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“…Alternatively, reduced food intake in infected locusts may be driven by the activation of the immune system. Both their immune system and their ability to detoxify noxious food substances rely on pathways that involve the antioxidant glutathione (Habig et al ., 1974; Stahlschmidt et al ., 2015; Jeschke et al ., 2016). Consequently, competition for glutathione between these two physiological pathways could lead to impaired detoxification when the immune system is already activated (McMillan et al ., 2018).…”

Section: Discussionmentioning

confidence: 99%

Malpighamoebainfection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules

Rossi

Ott

Niven

2019

Preprint

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12Malpighian tubules, analogous to vertebrate nephrons, play a key role in insect 13 osmoregulation and detoxification. Tubules can become infected with a protozoan, 14Malpighamoeba, which damages their epithelial cells, potentially compromising their function. 15Here we quantify the impact of Malpighamoeba infection on fluid secretion and P-glycoprotein-16 dependent detoxification by Malpighian tubules of the desert locust using a modified Ramsay 17 assay. Infected tubules have a greater surface area and a higher fluid secretion rate than 18 uninfected tubules. Infection also impairs P-glycoprotein-dependent detoxification reducing 19 the net extrusion of rhodamine B per unit of surface area. However, infected tubules' increased 20 surface area and fluid secretion rate means they have similar total net extrusion per tubule to 21 uninfected tubules. Increased fluid secretion rate of infected tubules likely subjects locusts to 22 greater water stress and imposes increased energy costs. Coupled with reduced efficiency of 23 P-glycoprotein detoxification, Malpighamoeba infection is likely to reduce insect survival within 24 natural environments. 25

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A mode of action of glucosinolate-derived isothiocyanates: Detoxification depletes glutathione and cysteine levels with ramifications on protein metabolism in Spodoptera littoralis

Cited by 73 publications

References 75 publications

Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

Evolution of herbivory remodels aDrosophilagenome

Malpighamoebainfection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules

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