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      Metabolism of plant-derived toxins from its insect host increases the success of the entomopathogenic fungus Beauveria bassiana

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          Abstract

          Beauveria bassiana is a soil fungus that parasitizes a large number of arthropod species, including numerous crop pests, causing white muscardine disease and is therefore used as a biological insecticide. However, some insects, such as the cabbage aphid ( Brevicoryne brassicae), defend themselves chemically by sequestering dietary pro-toxins (glucosinolates) from their Brassicales host plants. Glucosinolates are accumulated by cabbage aphids and activated to form toxic isothiocyanates when under attack. While isothiocyanate formation protects aphids against most attackers, B. bassiana is still able to infect the cabbage aphid under natural conditions. We therefore investigated how this fungus is able to circumvent the chemical defense system of the cabbage aphid. Here, we describe how B. bassiana infection activates the cabbage aphid defense system, but the resulting toxins are metabolized by B. bassiana via the mercapturic acid pathway, of which the first step is catalyzed by glutathione- S-transferases of low substrate specificity. This detoxification pathway enhances B. bassiana growth when isothiocyanates are present in natural concentrations, and so appears to be an important factor in fungal parasitization of these chemically defended aphids.

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          Most cited references68

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          Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics.

          Xenobiotic resistance in insects has evolved predominantly by increasing the metabolic capability of detoxificative systems and/or reducing xenobiotic target site sensitivity. In contrast to the limited range of nucleotide changes that lead to target site insensitivity, many molecular mechanisms lead to enhancements in xenobiotic metabolism. The genomic changes that lead to amplification, overexpression, and coding sequence variation in the three major groups of genes encoding metabolic enzymes, i.e., cytochrome P450 monooxygenases (P450s), esterases, and glutathione-S-transferases (GSTs), are the focus of this review. A substantial number of the adaptive genomic changes associated with insecticide resistance that have been characterized to date are transposon mediated. Several lines of evidence suggest that P450 genes involved in insecticide resistance, and perhaps insecticide detoxification genes in general, may share an evolutionary association with genes involved in allelochemical metabolism. Differences in the selective regime imposed by allelochemicals and insecticides may account for the relative importance of regulatory or structural mutations in conferring resistance.
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            Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana.

            The glucosinolate content of various organs of the model plant Arabidopsis thaliana (L.) Heynh., Columbia (Col-0) ecotype, was analyzed at different stages during its life cycle. Significant differences were noted among organs in both glucosinolate concentration and composition. Dormant and germinating seeds had the highest concentration (2.5-3.3% by dry weight), followed by inflorescences, siliques (fruits), leaves and roots. While aliphatic glucosinolates predominated in most organs, indole glucosinolates made up nearly half of the total composition in roots and late-stage rosette leaves. Seeds had a very distinctive glucosinolate composition. They possessed much higher concentrations of several types of aliphatic glucosinolates than other organs, including methylthioalkyl and, hydroxyalkyl glucosinolates and compounds with benzoate esters than other organs. From a developmental perspective, older leaves had lower glucosinolate concentrations than younger leaves, but this was not due to decreasing concentrations in individual leaves with age (glucosinolate concentration was stable during leaf expansion). Rather, leaves initiated earlier in development simply had much lower rates of glucosinolate accumulation per dry weight gain throughout their lifetimes. During seed germination and leaf senescence, there were significant declines in glucosinolate concentration. The physiological and ecological significance of these findings is briefly discussed.
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              Disarming the mustard oil bomb.

              Plants are attacked by a broad array of herbivores and pathogens. In response, plants deploy an arsenal of defensive traits. In Brassicaceae, the glucosinolate-myrosinase complex is a sophisticated two-component system to ward off opponents. However, this so-called "mustard oil bomb" is disarmed by a glucosinolate sulfatase of a crucifer specialist insect, diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Sulfatase activity of this enzyme largely prevents the formation of toxic hydrolysis products arising from this plant defense system. Importantly, the enzyme acts on all major classes of glucosinolates, thus enabling diamondback moths to use a broad range of cruciferous host plants.
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                Author and article information

                Contributors
                vassao@ice.mpg.de
                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group UK (London )
                1751-7362
                1751-7370
                21 July 2023
                21 July 2023
                October 2023
                : 17
                : 10
                : 1693-1704
                Affiliations
                [1 ]Max Planck Institute for Chemical Ecology, Department of Biochemistry, ( https://ror.org/02ks53214) Jena, Germany
                [2 ]Max Planck Institute for Chemical Ecology, Department of Natural Product Biosynthesis, ( https://ror.org/02ks53214) Jena, Germany
                [3 ]Max Planck Institute for Chemical Ecology, Department of Evolutionary Neuroethology, ( https://ror.org/02ks53214) Jena, Germany
                [4 ]Max Planck Institute of Geoanthropology, Department of Archaeology, ( https://ror.org/00js75b59) Jena, Germany
                Author information
                http://orcid.org/0000-0001-9861-6097
                http://orcid.org/0000-0002-6691-6500
                http://orcid.org/0000-0002-1812-1551
                http://orcid.org/0000-0001-8455-9298
                Article
                1480
                10.1038/s41396-023-01480-3
                10504261
                37479887
                c4c88a75-22f8-421a-9e30-6a695602fdd3
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 14 March 2023
                : 7 July 2023
                : 13 July 2023
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100004189, Max-Planck-Gesellschaft (Max Planck Society);
                Categories
                Article
                Custom metadata
                © International Society for Microbial Ecology 2023

                Microbiology & Virology
                metabolomics,fungal ecology,transcriptomics,applied microbiology
                Microbiology & Virology
                metabolomics, fungal ecology, transcriptomics, applied microbiology

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