Reglucosylation of the Benzoxazinoid DIMBOA with Inversion of Stereochemical Configuration is a Detoxification Strategy in Lepidopteran Herbivores

Wouters, Felipe C.; Reichelt, Michael; Glauser, Gaëtan; Bauer, Eugen; Erb, Matthias; Gershenzon, Jonathan; Vassão, Daniel Giddings

doi:10.1002/anie.201406643

Cited by 80 publications

(83 citation statements)

References 29 publications

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“…When feeding on maize leaves, larvae of the more resistant species, S. frugiperda , S. littoralis , and S. exigua , excreted DIMBOA-Glc in the frass, while the more susceptible Mamestra brassicae and Helicoverpa armigera did not (Wouters et al 2014). In vitro assays confirmed that DIMBOA is glucosylated by S. frugiperda larval gut homogenates in the presence of UDP-glucose, suggesting the contribution of UGT enzymes.…”

Section: Metabolism Of Bxdsmentioning

confidence: 99%

Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores

et al. 2016

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Benzoxazinoids are a class of indole-derived plant chemical defenses comprising compounds with a 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one skeleton and their derivatives. These phytochemicals are widespread in grasses, including important cereal crops such as maize, wheat and rye, as well as a few dicot species, and display a wide range of antifeedant, insecticidal, antimicrobial, and allelopathic activities. Although their overall effects against insect herbivores are frequently reported, much less is known about how their modes of action specifically influence insect physiology. The present review summarizes the biological activities of benzoxazinoids on chewing, piercing-sucking, and root insect herbivores. We show how within-plant distribution modulates the exposure of different herbivore feeding guilds to these defenses, and how benzoxazinoids may act as toxins, feeding deterrents and digestibility-reducing compounds under different conditions. In addition, recent results on the metabolism of benzoxazinoids by insects and their consequences for plant-herbivore interactions are addressed, as well as directions for future research.

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Section: Metabolism Of Bxdsmentioning

confidence: 99%

Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores

et al. 2016

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“…This species is also regularly found on teosinte (de Lange et al, 2014) and appears to be well adapted to maize defenses. It is able to synthesize enzymes to counteract and detoxify DIMBOA, a toxic benzoxazinoid liberated upon herbivory (Glauser et al, 2011;Wouters et al, 2014). FAW currently occurs throughout the Americas and has recently been introduced to West Central Africa (CABI database, 2015).…”

Section: The Insectsmentioning

confidence: 99%

“…In regard to our hypothesis, maysin is possibly an alternative defense compound that has been maintained at high concentrations in cultivated maize to provide resistance against specialists. Indeed, S. frugiperda performs poorly on high maysin lines (Wiseman et al, 1992;Nuessly et al, 2007), whereas, along with D. virgifera, it is readily able to tolerate and detoxify BXDs, which appear to be more effective as a defense against the nonspecialized insects (Robert et al, 2012;Wouters et al, 2014).…”

Section: Researchmentioning

confidence: 99%

Fine‐tuning the ‘plant domestication‐reduced defense’ hypothesis: specialist vs generalist herbivores

et al. 2017

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SummaryDomesticated plants are assumed to have weakened chemical defenses. We argue, however, that artificial selection will have maintained defense traits against specialized herbivores that have coexisted with the crops throughout their domestication.We assessed the performance of eight species of insect herbivores from three feeding guilds on six European maize lines and six populations of their wild ancestor, teosinte. A metabolomics approach was used in an attempt to identify compounds responsible for observed differences in insect performance.Insects consistently performed better on maize than on teosinte. As hypothesized, this difference was greater for generalist herbivores that are normally not found on teosinte. We also found clear differences in defense metabolites among the different genotypes, but none that consistently correlated with differences in performance. Concentrations of benzoxazinoids, the main chemical defense in maize, tended to be higher in leaves of teosinte, but the reverse was true for the roots.It appears that chemical defenses that target specialized insects are still present at higher concentrations in cultivated maize than compounds that are more effective against generalists. These weakened broad-spectrum defenses in crops may explain the successes of novel pests.

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“…Glutathione S-transferases (GSTs) and UDP-glucosyltransferases (UGTs) are examples of such enzymes. In Spodoptera spp., larvae feeding on maize, which produces the toxic aglucone DIMBOA when attacked, detoxify the toxin in their guts by the addition of glucose [18]. Helicoverpa larvae uses an UGT to glycosylate the alkaloid capsaicin produced by pepper fruits [19] and M. sexta larvae glycosylate several toxic plant phenolics produced by its host plants [20].…”

Section: Introductionmentioning

confidence: 99%

Transcriptome profiling reveals differential gene expression of detoxification enzymes in a hemimetabolous tobacco pest after feeding on jasmonate-silenced Nicotiana attenuata plants

2016

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BackgroundThe evolutionary arms race between plants and insects has driven the co-evolution of sophisticated defense mechanisms used by plants to deter herbivores and equally sophisticated strategies that enable phytophagous insects to rapidly detoxify the plant’s defense metabolites. In this study, we identify the genetic determinants that enable the mirid, Tupiocoris notatus, to feed on its well-defended host plant, Nicotiana attenuata, an outstanding model for plant-insect interaction studies.ResultsWe used an RNAseq approach to evaluate the global gene expression of T. notatus after feeding on a transgenic N. attenuata line which does not accumulate jasmonic acid (JA) after herbivory, and consequently accumulates very low levels of defense metabolites. Using Illumina sequencing, we generated a de novo assembled transcriptome which resulted in 63,062 contigs (putative transcript isoforms) contained in 42,610 isotigs (putative identified genes). Differential expression analysis based on RSEM-estimated transcript abundances identified 82 differentially expressed (DE) transcripts between T. notatus fed on wild-type and the defenseless plants. The same analysis conducted with Corset-estimated transcript abundances identified 59 DE clusters containing 85 transcripts. In both analyses, a larger number of DE transcripts were found down-regulated in mirids feeding on JA-silenced plants (around 70%). Among these down-regulated transcripts we identified seven transcripts possibly involved in the detoxification of N. attenuata defense metabolite, specifically, one glutathione-S-transferase (GST), one UDP-glucosyltransferase (UGT), five cytochrome P450 (P450s), and six serine proteases. Real-time quantitative PCR confirmed the down-regulation for six transcripts (encoding GST, UGT and four P450s) and revealed that their expression was only slightly decreased in mirids feeding on another N. attenuata transgenic line specifically silenced in the accumulation of diterpene glycosides, one of the many classes of JA-mediated defenses in N. attenuata.ConclusionsThe results provide a transcriptional overview of the changes in a specialist hemimetabolous insect associated with feeding on host plants depleted in chemical defenses. Overall, the analysis reveals that T. notatus responses to host plant defenses are narrow and engages P450 detoxification pathways. It further identifies candidate genes which can be tested in future experiments to understand their role in shaping the T. notatus-N. attenuata interaction.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3348-0) contains supplementary material, which is available to authorized users.

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Reglucosylation of the Benzoxazinoid DIMBOA with Inversion of Stereochemical Configuration is a Detoxification Strategy in Lepidopteran Herbivores

Cited by 80 publications

References 29 publications

Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores

Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores

Fine‐tuning the ‘plant domestication‐reduced defense’ hypothesis: specialist vs generalist herbivores

Transcriptome profiling reveals differential gene expression of detoxification enzymes in a hemimetabolous tobacco pest after feeding on jasmonate-silenced Nicotiana attenuata plants

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