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      Plant organ cultures as masked mycotoxin biofactories: Deciphering the fate of zearalenone in micropropagated durum wheat roots and leaves

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          Abstract

          “Masked mycotoxins” senso strictu are conjugates of mycotoxins resulting from metabolic pathways activated by the interplay between pathogenic fungi and infected plants. Zearalenone, an estrogenic mycotoxin produced by Fusarium spp, was the first masked mycotoxin ever described in the literature, but its biotransformation has been studied to a lesser extent if compared to other compounds such as deoxynivalenol. We presented herein the first application of organ and tissue culture techniques to study the metabolic fate of zearalenone in durum wheat, using an untargeted HR-LCMS approach. A complete, quick absorption of zearalenone by uninfected plant organs was noticed, and its biotransformation into a large spectrum of phase I and phase II metabolites has been depicted. Therefore, wheat organ tissue cultures can be effectively used as a biocatalytic tool for the production of masked mycotoxins, as well as a replicable model for the investigation of the interplay between mycotoxins and wheat physiology.

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          Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin.

          Zearalenone (ZEA) is a mycotoxin produced mainly by fungi belonging to the genus Fusarium in foods and feeds. It is frequently implicated in reproductive disorders of farm animals and occasionally in hyperoestrogenic syndromes in humans. There is evidence that ZEA and its metabolites possess oestrogenic activity in pigs, cattle and sheep. However, ZEA is of a relatively low acute toxicity after oral or interperitoneal administration in mice, rat and pig. The biotransformation for ZEA in animals involves the formation of two metabolites alpha-zearalenol (alpha-ZEA) and beta-zearalenol (beta-ZEA) which are subsequently conjugated with glucuronic acid. Moreover, ZEA has also been shown to be hepatotoxic, haematotoxic, immunotoxic and genotoxic. The exact mechanism of ZEA toxicity is not completely established. This paper gives an overview about the acute, subacute and chronic toxicity, reproductive and developmental toxicity, carcinogenicity, genotoxicity and immunotoxicity of ZEA and its metabolites. ZEA is commonly found on several foods and feeds in the temperate regions of Europe, Africa, Asia, America and Oceania. Recent data about the worldwide contamination of foods and feeds by ZEA are considered in this review. Due to economic losses engendered by ZEA and its impact on human and animal health, several strategies for detoxifying contaminated foods and feeds have been described in the literature including physical, chemical and biological process. Dietary intakes of ZEA were reported from few countries from the world. The mean dietary intakes for ZEA have been estimated at 20 ng/kgb.w./day for Canada, Denmark and Norway and at 30 ng/kgb.w./day for the USA. The Joint FAO/WHO Expert Committee on Food Additives (JECFA) established a provisional maximum tolerable daily intake (PMTDI) for ZEA of 0.5 microg/kg of body weight.
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            Masked mycotoxins: determination of a deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromatography-tandem mass spectrometry.

            Conjugated mycotoxins, in which the toxin is usually bound to a more polar substance like glucose, are referred to as masked mycotoxins, as these substances escape routine detection methods but can release their toxic precursors after hydrolysis. This is the first report on the natural occurrence of a glucoside of deoxynivalenol (DON) in Fusarium-infected wheat and maize. To obtain appropriate standards, we chemically synthesized deoxynivalenol-3-beta-D-glucopyranoside (DON-3-glucoside) and deoxynivalenol-15-beta-D-glucopyranoside (DON-15-glucoside). The synthesis products were characterized by liquid chromatography-tandem mass spectrometry. The DON-glucosides showed different collision-induced dissociation (CID) fragmentation behaviors and could therefore be distinguished. Wheat plants were either treated with DON (n = 52) or with Fusarium spp. (n = 4) at anthesis, and after harvest, wheat ears were analyzed for DON and DON-glucosides. All 56 treated wheat samples contained DON and a DON-glucoside with the same retention time, molecular mass, and CID fragmentation behavior as the synthetic DON-3-glucoside. Moreover, the DON-glucoside was also found in two out of three analyzed naturally DON-contaminated maize and in five out of five naturally contaminated wheat samples, in a range from 4 to 12% of the DON concentration. To further confirm the identity of the DON-glucoside, the compound was isolated from wheat extracts and characterized as DON-3-glucoside with NMR. The results of this study indicate the importance to consider both DON and DON-3-glucoside with regard to food and feed safety.
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              Irrigation of root vegetables with treated wastewater: evaluating uptake of pharmaceuticals and the associated human health risks.

              To meet mounting water demands, treated wastewater has become an important source of irrigation. Thus, contamination of treated wastewater by pharmaceutical compounds (PCs) and the fate of these compounds in the agricultural environment are of increasing concern. This field study aimed to quantify PC uptake by treated wastewater-irrigated root crops (carrots and sweet potatoes) grown in lysimeters and to evaluate potential risks. In both crops, the nonionic PCs (carbamazepine, caffeine, and lamotrigine) were detected at significantly higher concentrations than ionic PCs (metoprolol, bezafibrate, clofibric acid, diclofenac, gemfibrozil, ibuprofen, ketoprofen, naproxen, sulfamethoxazole, and sildenafil). PCs in leaves were found at higher concentrations than in the roots. Carbamazepine metabolites were found mainly in the leaves, where the concentration of the metabolite 10,11-epoxycarbamazepine was significantly higher than the parent compound. The health risk associated with consumption of wastewater-irrigated root vegetables was estimated using the threshold of toxicological concern (TTC) approach. Our data show that the TTC value of lamotrigine can be reached for a child at a daily consumption of half a carrot (∼60 g). This study highlights that certain PCs accumulated in edible organs at concentrations above the TTC value should be categorized as contaminants of emerging concern.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: SoftwareRole: Validation
                Role: ConceptualizationRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: ConceptualizationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 November 2017
                2017
                : 12
                : 11
                : e0187247
                Affiliations
                [1 ] Department of Food and Drug, University of Parma, Parma, Italy
                [2 ] Deparment of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
                [3 ] Barilla G.R. F.lli SpA, Advanced Laboratory Research, Parma, Italy
                Universita degli Studi di Pisa, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0716-8394
                Article
                PONE-D-17-16646
                10.1371/journal.pone.0187247
                5690627
                29145415
                52a9abd9-84c6-4362-9c39-9124bdb74454
                © 2017 Righetti et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 May 2017
                : 17 October 2017
                Page count
                Figures: 5, Tables: 2, Pages: 17
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolic Pathways
                Xenobiotic Metabolism
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Wheat
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Plant Pathogens
                Plant Fungal Pathogens
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Arabidopsis Thaliana
                Research and Analysis Methods
                Model Organisms
                Arabidopsis Thaliana
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Brassica
                Arabidopsis Thaliana
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
                Arabidopsis Thaliana
                Biology and Life Sciences
                Plant Science
                Plant Physiology
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolic Pathways
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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