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Elisabeth Varga
Department of Food Chemistry and Toxicology, Faculty of Chemistry, University of Vienna, Währinger Straße 40, 1090 Vienna, Austria

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Journal article
Published: 06 July 2021 in Science of The Total Environment
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Prymnesium parvum is a bloom forming haptophyte that has been responsible for numerous fish kill events across the world. The toxicity of P. parvum has been attributed to the production of large polyketide compounds, collectively called prymnesins, which based on their structure can be divided into A-, B- and C-type. The polyketide chemical nature of prymnesins indicates the potential involvement of polyketide synthases (PKSs) in their biosynthesis. However, little is known about the presence of PKSs in P. parvum as well as the potential molecular trade-offs of toxin biosynthesis. In the current study, we generated and analyzed the transcriptomes of nine P. parvum strains that produce different toxin types and have various cellular toxin contents. Numerous type I PKSs, ranging from 37 to 109, were found among the strains. Larger modular type I PKSs were mainly retrieved from strains with high cellular toxin levels and eight consensus transcripts were present in all nine strains. Gene expression variance analysis revealed potential molecular trade-offs associated with cellular toxin quantity, showing that basic metabolic processes seem to correlate negatively with cellular toxin content. These findings point towards the presence of metabolic costs for maintaining high cellular toxin quantity. The detailed analysis of PKSs in P. parvum is the first step towards better understanding the molecular basis of the biosynthesis of prymnesins and contributes to the development of molecular tools for efficient monitoring of future blooms.

ACS Style

Konstantinos Anestis; Gurjeet Singh Kohli; Sylke Wohlrab; Elisabeth Varga; Thomas Ostenfeld Larsen; Per Juel Hansen; Uwe John. Polyketide synthase genes and molecular trade-offs in the ichthyotoxic species Prymnesium parvum. Science of The Total Environment 2021, 795, 148878 .

AMA Style

Konstantinos Anestis, Gurjeet Singh Kohli, Sylke Wohlrab, Elisabeth Varga, Thomas Ostenfeld Larsen, Per Juel Hansen, Uwe John. Polyketide synthase genes and molecular trade-offs in the ichthyotoxic species Prymnesium parvum. Science of The Total Environment. 2021; 795 ():148878.

Chicago/Turabian Style

Konstantinos Anestis; Gurjeet Singh Kohli; Sylke Wohlrab; Elisabeth Varga; Thomas Ostenfeld Larsen; Per Juel Hansen; Uwe John. 2021. "Polyketide synthase genes and molecular trade-offs in the ichthyotoxic species Prymnesium parvum." Science of The Total Environment 795, no. : 148878.

Journal article
Published: 04 March 2021 in Toxins
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The human intestine is regularly exposed to ingested food contaminants, such as fungal and bacterial toxins, which have been described to co-occur in a mixed diet. Thus, it is of utmost importance to understand possible interactions between contaminants of different origin. Hence, we investigated the single and combined effects of one of the most abundant mycotoxins, deoxynivalenol (DON; 0.1 to 10 µg/mL), and the bacterial toxin cereulide (CER; 1 to 100 ng/mL) on differentiated human Caco-2 (C2BBe1) cells cultured in a transwell system. We tested the capacity of the two toxins to alter the intestinal integrity and further investigated the uptake of both compounds and the formation of selected DON metabolites. CER alone (10 and 100 ng/mL) and in combination with DON (10 ng/mL CER with 1 µg/mL DON) was found to alter the barrier function by increasing the transepithelial electrical resistance and the expression of the tight junction protein claudin-4. For the first time, DON-3-sulfate was identified as a metabolite of human intestinal cells in vitro. Moreover, co-incubation of CER and DON led to an altered ratio between DON and DON-3-sulfate. Hence, we conclude that co-exposure to CER and DON may alter the intestinal barrier function and biotransformation of intestinal cells.

ACS Style

Julia Beisl; Elisabeth Varga; Dominik Braun; Benedikt Warth; Monika Ehling-Schulz; Giorgia Del Favero; Doris Marko. Assessing Mixture Effects of Cereulide and Deoxynivalenol on Intestinal Barrier Integrity and Uptake in Differentiated Human Caco-2 Cells. Toxins 2021, 13, 189 .

AMA Style

Julia Beisl, Elisabeth Varga, Dominik Braun, Benedikt Warth, Monika Ehling-Schulz, Giorgia Del Favero, Doris Marko. Assessing Mixture Effects of Cereulide and Deoxynivalenol on Intestinal Barrier Integrity and Uptake in Differentiated Human Caco-2 Cells. Toxins. 2021; 13 (3):189.

Chicago/Turabian Style

Julia Beisl; Elisabeth Varga; Dominik Braun; Benedikt Warth; Monika Ehling-Schulz; Giorgia Del Favero; Doris Marko. 2021. "Assessing Mixture Effects of Cereulide and Deoxynivalenol on Intestinal Barrier Integrity and Uptake in Differentiated Human Caco-2 Cells." Toxins 13, no. 3: 189.

Journal article
Published: 01 January 2021 in Journal of Biological Chemistry
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Brassinosteroids (BRs) are steroid hormones of plants that coordinate fundamental growth and development processes. Their homeostasis is controlled by diverse means, including glucosylation of the bioactive BR brassinolide (BL), which is catalyzed by the UDP-glycosyltransferases UGT73C5 and UGT73C6 and occurs mainly at the C-23 position, Additional evidence had suggested that the resultant BL-23-O-glucoside (BL-23-O-Glc) can be malonylated, but the physiological significance of and enzyme required for this reaction had remained unknown. Here we show that in Arabidopsis thaliana malonylation of BL-23-O-Glc is catalyzed by the acyltransferase PMAT1, which is also known to malonylate phenolic glucosides and lipid amides. Loss of PMAT1 abolished BL-23-O-malonylglucoside formation and enriched BL-23-O-Glc, showing that the enzyme acts on the glucoside. An over-expression of PMAT1 in plants where UGT73C6 was also over-expressed, and thus BL-23-O-Glc formation was promoted, enhanced the symptoms of BR-deficiency of UGT73C6oe plants, providing evidence that PMAT1 contributes to BL inactivation. Based on these results a model is proposed in which PMAT1 acts in the conversion of both endogenous and xenobiotic glucosides, to adjust metabolic homeostasis in spatial and temporal modes.

ACS Style

Sufu Gan; Wilfried Rozhon; Elisabeth Varga; Jyotirmoy Halder; Franz Berthiller; Brigitte Poppenberger. The acyltransferase PMAT1 malonylates brassinolide glucoside. Journal of Biological Chemistry 2021, 296, 100424 .

AMA Style

Sufu Gan, Wilfried Rozhon, Elisabeth Varga, Jyotirmoy Halder, Franz Berthiller, Brigitte Poppenberger. The acyltransferase PMAT1 malonylates brassinolide glucoside. Journal of Biological Chemistry. 2021; 296 ():100424.

Chicago/Turabian Style

Sufu Gan; Wilfried Rozhon; Elisabeth Varga; Jyotirmoy Halder; Franz Berthiller; Brigitte Poppenberger. 2021. "The acyltransferase PMAT1 malonylates brassinolide glucoside." Journal of Biological Chemistry 296, no. : 100424.

Genotoxicity and carcinogenicity
Published: 04 July 2020 in Archives of Toxicology
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Molds of the genus Alternaria produce several mycotoxins, some of which may pose a threat for health due to their genotoxicity. Due to the lack of adequate toxicological and occurrence data, they are currently not regulated. Interactions between mycotoxins, gut microbiota and food constituents might occur after food ingestion, modifying the bioavailability and, therefore, overall toxicity of mycotoxins. The present work aimed to investigate the impact of in vitro short-term fecal incubation on the in vitro DNA-damaging effects exerted by 5 µg/mL of an Alternaria alternata extract, containing, among others, 15 nM alternariol, 12 nM alternariol monomethyl ether, 241 nM altertoxin II and 301 nM stemphyltoxin III, all of which are known as genotoxic. The involvement of microorganisms, undigested food constituents and soluble substances of human fecal samples in modifying the composition and the genotoxicity of the extract was investigated through the application of LC–MS/MS analysis and comet assays in HT-29 cells. Results showed that the potential of the mycotoxins to induce DNA strand breaks was almost completely quenched, even before anaerobic incubation, by contact with the different fractions of the fecal samples, while the potency to induce formamidopyrimidine DNA glycosylase (FPG)-sensitive sites was only slightly reduced. These effects were in line with a reduction of mycotoxin concentrations found in samples analyzed by LC–MS/MS. Although a direct correlation between the metabolic activity of the gut microbiota and modifications in mycotoxin contents was not clearly observed, adsorptive phenomena to bacterial cells and to undigested food constituents might explain the observed modifications.

ACS Style

Francesco Crudo; Georg Aichinger; Jovana Mihajlovic; Luca Dellafiora; Elisabeth Varga; Hannes Puntscher; Benedikt Warth; Chiara Dall'Asta; David Berry; Doris Marko. Gut microbiota and undigested food constituents modify toxin composition and suppress the genotoxicity of a naturally occurring mixture of Alternaria toxins in vitro. Archives of Toxicology 2020, 94, 3541 -3552.

AMA Style

Francesco Crudo, Georg Aichinger, Jovana Mihajlovic, Luca Dellafiora, Elisabeth Varga, Hannes Puntscher, Benedikt Warth, Chiara Dall'Asta, David Berry, Doris Marko. Gut microbiota and undigested food constituents modify toxin composition and suppress the genotoxicity of a naturally occurring mixture of Alternaria toxins in vitro. Archives of Toxicology. 2020; 94 (10):3541-3552.

Chicago/Turabian Style

Francesco Crudo; Georg Aichinger; Jovana Mihajlovic; Luca Dellafiora; Elisabeth Varga; Hannes Puntscher; Benedikt Warth; Chiara Dall'Asta; David Berry; Doris Marko. 2020. "Gut microbiota and undigested food constituents modify toxin composition and suppress the genotoxicity of a naturally occurring mixture of Alternaria toxins in vitro." Archives of Toxicology 94, no. 10: 3541-3552.

Journal article
Published: 01 July 2020 in Plant Physiology
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Previous research complemented with results on BIA1 enzymatic activities shows that the enzyme regulates brassinosteroid homeostasis via mono- and diacetylation of castasterone.

ACS Style

Sufu Gan; Wilfried Rozhon; Elisabeth Varga; Simon Josef Unterholzner; Franz Berthiller; Brigitte Poppenberger. The BAHD Acyltransferase BIA1 Uses Acetyl-CoA for Catabolic Inactivation of Brassinosteroids. Plant Physiology 2020, 184, 23 -26.

AMA Style

Sufu Gan, Wilfried Rozhon, Elisabeth Varga, Simon Josef Unterholzner, Franz Berthiller, Brigitte Poppenberger. The BAHD Acyltransferase BIA1 Uses Acetyl-CoA for Catabolic Inactivation of Brassinosteroids. Plant Physiology. 2020; 184 (1):23-26.

Chicago/Turabian Style

Sufu Gan; Wilfried Rozhon; Elisabeth Varga; Simon Josef Unterholzner; Franz Berthiller; Brigitte Poppenberger. 2020. "The BAHD Acyltransferase BIA1 Uses Acetyl-CoA for Catabolic Inactivation of Brassinosteroids." Plant Physiology 184, no. 1: 23-26.

In vitro systems
Published: 17 February 2020 in Archives of Toxicology
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Deoxynivalenol (DON), one of the most abundant mycotoxins in cereal products, was recently detected with other mycotoxins and the emetic bacterial toxin cereulide (CER) in maize porridge. Within a cereal-based diet, co-exposure to these toxins is likely, hence raising the question of combinatory toxicological effects. While the toxicological evaluation of DON has quite progressed, consequences of chronic, low-dose CER exposure are still insufficiently explored. Information about the combinatory toxicological effects of these toxins is lacking. In the present study, we investigated how CER (0.1–100 ng/mL) and DON (0.01–10 µg/mL) alone and in a constant ratio of 1:100 (CER:DON) affect the cytotoxicity and immune response of differentiated human intestinal Caco-2 cells. While DON alone reduced cell viability only in the highest concentration (10 µg/mL), CER caused severe cytotoxicity upon prolonged incubation (starting from 10 ng/mL after 24 h and 48 h, 2.5 ng/mL and higher after 72 h). After 72 h, synergistic effects were observed at 2.5 ng/mL CER and 0.25 µg/mL DON. Different endpoints of inflammation were investigated in interleukin-1β-stimulated Caco-2 cells. Notably, DON-induced interleukin-8 transcription and secretion were diminished by the presence of 10 and 25 ng/mL CER after short-term (5 h) incubation, indicating immunosuppressive properties. We hypothesise that habitual consumption of cereal-based foods co-contaminated with CER and DON may cause synergistic cytotoxic effects and an altered immune response in the human intestine. Therefore, further research concerning effects of co-occurring bacterial toxins and mycotoxins on the impairment of intestinal barrier integrity, intestinal inflammation and the promotion of malnutrition is needed.

ACS Style

Julia Beisl; Gudrun Pahlke; Helen Abeln; Monika Ehling-Schulz; Giorgia Del Favero; Elisabeth Varga; Benedikt Warth; Michael Sulyok; Wilfred Abia; Chibundu N. Ezekiel; Doris Marko. Combinatory effects of cereulide and deoxynivalenol on in vitro cell viability and inflammation of human Caco-2 cells. Archives of Toxicology 2020, 94, 833 -844.

AMA Style

Julia Beisl, Gudrun Pahlke, Helen Abeln, Monika Ehling-Schulz, Giorgia Del Favero, Elisabeth Varga, Benedikt Warth, Michael Sulyok, Wilfred Abia, Chibundu N. Ezekiel, Doris Marko. Combinatory effects of cereulide and deoxynivalenol on in vitro cell viability and inflammation of human Caco-2 cells. Archives of Toxicology. 2020; 94 (3):833-844.

Chicago/Turabian Style

Julia Beisl; Gudrun Pahlke; Helen Abeln; Monika Ehling-Schulz; Giorgia Del Favero; Elisabeth Varga; Benedikt Warth; Michael Sulyok; Wilfred Abia; Chibundu N. Ezekiel; Doris Marko. 2020. "Combinatory effects of cereulide and deoxynivalenol on in vitro cell viability and inflammation of human Caco-2 cells." Archives of Toxicology 94, no. 3: 833-844.

Review
Published: 03 November 2019 in Toxins
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Mycotoxins are low-molecular weight compounds produced by diverse genera of molds that may contaminate food and feed threatening the health of humans and animals. Recent findings underline the importance of studying the combined occurrence of multiple mycotoxins and the relevance of assessing the toxicity their simultaneous exposure may cause in living organisms. In this context, for the first time, this work has critically reviewed the most relevant data concerning the occurrence and toxicity of mycotoxins produced by Alternaria spp., which are among the most important emerging risks to be assessed in food safety, alone or in combination with other mycotoxins and bioactive food constituents. According to the literature covered, multiple Alternaria mycotoxins may often occur simultaneously in contaminated food, along with several other mycotoxins and food bioactives inherently present in the studied matrices. Although the toxicity of combinations naturally found in food has been rarely assessed experimentally, the data collected so far, clearly point out that chemical mixtures may differ in their toxicity compared to the effect of toxins tested individually. The data presented here may provide a solid foothold to better support the risk assessment of Alternaria mycotoxins highlighting the actual role of chemical mixtures on influencing their toxicity.

ACS Style

Francesco Crudo; Elisabeth Varga; Georg Aichinger; Gianni Galaverna; Doris Marko; Chiara Dall'Asta; Luca Dellafiora. Co-Occurrence and Combinatory Effects of Alternaria Mycotoxins and other Xenobiotics of Food Origin: Current Scenario and Future Perspectives. Toxins 2019, 11, 640 .

AMA Style

Francesco Crudo, Elisabeth Varga, Georg Aichinger, Gianni Galaverna, Doris Marko, Chiara Dall'Asta, Luca Dellafiora. Co-Occurrence and Combinatory Effects of Alternaria Mycotoxins and other Xenobiotics of Food Origin: Current Scenario and Future Perspectives. Toxins. 2019; 11 (11):640.

Chicago/Turabian Style

Francesco Crudo; Elisabeth Varga; Georg Aichinger; Gianni Galaverna; Doris Marko; Chiara Dall'Asta; Luca Dellafiora. 2019. "Co-Occurrence and Combinatory Effects of Alternaria Mycotoxins and other Xenobiotics of Food Origin: Current Scenario and Future Perspectives." Toxins 11, no. 11: 640.

Original research article
Published: 18 October 2019 in Frontiers in Pharmacology
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The mycotoxin zearalenone (ZEN) is produced by many plant pathogenic Fusarium species. It is well known for its estrogenic activity in humans and animals, but whether ZEN has a role in plant–pathogen interaction and which process it is targeting in planta was so far unclear. We found that treatment of Arabidopsis thaliana seedlings with ZEN induced transcription of the AtHSP90.1 gene. This heat shock protein (HSP) plays an important role in plant–pathogen interaction, assisting in stability and functionality of various disease resistance gene products. Inhibition of HSP90 ATPase activity impairs functionality. Because HSP90 inhibitors are known to induce HSP90 gene expression and due to the structural similarity with the known HSP90 inhibitor radicicol (RAD), we tested whether ZEN and its phase I metabolites α- and ß-zearalenol are also HSP90 ATPase inhibitors. Indeed, AtHSP90.1 and wheat TaHSP90-2 were inhibited by ZEN and ß-zearalenol, while α-zearalenol was almost inactive. Plants can efficiently glycosylate ZEN and α/ß-zearalenol. We therefore tested whether glucosylation has an effect on the inhibitory activity of these metabolites. Expression of the A. thaliana glucosyltransferase UGT73C6 conferred RAD resistance to a sensitive yeast strain. Glucosylation of RAD, ZEN, and α/ß-zearalenol abolished the in vitro inhibitory activity with recombinant HSP90 purified from Escherichia coli. In conclusion, the mycotoxin ZEN has a very prominent target in plants, HSP90, but it can be inactivated by glycosylation. This may explain why there is little evidence for a virulence function of ZEN in host plants.

ACS Style

Juan Antonio Torres Acosta; Herbert Michlmayr; Mehrdad Shams; Wolfgang Schweiger; Gerlinde Wiesenberger; Rudolf Mitterbauer; Ulrike Werner; David Merz; Marie-Theres Hauser; Christian Hametner; Elisabeth Varga; Rudolf Krska; Franz Berthiller; Gerhard Adam. Zearalenone and ß-Zearalenol But Not Their Glucosides Inhibit Heat Shock Protein 90 ATPase Activity. Frontiers in Pharmacology 2019, 10, 1 .

AMA Style

Juan Antonio Torres Acosta, Herbert Michlmayr, Mehrdad Shams, Wolfgang Schweiger, Gerlinde Wiesenberger, Rudolf Mitterbauer, Ulrike Werner, David Merz, Marie-Theres Hauser, Christian Hametner, Elisabeth Varga, Rudolf Krska, Franz Berthiller, Gerhard Adam. Zearalenone and ß-Zearalenol But Not Their Glucosides Inhibit Heat Shock Protein 90 ATPase Activity. Frontiers in Pharmacology. 2019; 10 ():1.

Chicago/Turabian Style

Juan Antonio Torres Acosta; Herbert Michlmayr; Mehrdad Shams; Wolfgang Schweiger; Gerlinde Wiesenberger; Rudolf Mitterbauer; Ulrike Werner; David Merz; Marie-Theres Hauser; Christian Hametner; Elisabeth Varga; Rudolf Krska; Franz Berthiller; Gerhard Adam. 2019. "Zearalenone and ß-Zearalenol But Not Their Glucosides Inhibit Heat Shock Protein 90 ATPase Activity." Frontiers in Pharmacology 10, no. : 1.

Journal article
Published: 04 May 2019 in Toxins
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Harmful algal blooms of Prymnesium parvum have recurrently been associated with the killing of fish. The causative ichthyotoxic agents of this haptophyte are believed to be prymnesins, a group of supersized ladder-frame polyether compounds currently divided into three types. Here, the development of a quantitative method to assess the molar sum of prymnesins in water samples and in algal biomass is reported. The method is based on the derivatization of the primary amine group and subsequent fluorescence detection using external calibrants. The presence of prymnesins in the underivatized sample should be confirmed by liquid chromatography mass spectrometry. The method is currently only partly applicable to water samples due to the low amounts that are present. The growth and cellular toxin content of two B-type producing strains were monitored in batch cultures eventually limited by an elevated pH. The cellular toxin contents varied by a factor of ~2.5 throughout the growth cycle, with the highest amounts found in the exponential growth phase and the lowest in the stationary growth/death phases. The strain K-0081 contained ~5 times more toxin than K-0374. Further investigations showed that the majority of prymnesins were associated with the biomass (89% ± 7%). This study provides the basis for further investigations into the toxicity and production of prymnesins.

ACS Style

Daniel Killerup Svenssen; Sofie Bjørnholt Binzer; Nikola Medić; Per Juel Hansen; Thomas Ostenfeld Larsen; Elisabeth Varga. Development of an Indirect Quantitation Method to Assess Ichthyotoxic B-Type Prymnesins from Prymnesium parvum. Toxins 2019, 11, 251 .

AMA Style

Daniel Killerup Svenssen, Sofie Bjørnholt Binzer, Nikola Medić, Per Juel Hansen, Thomas Ostenfeld Larsen, Elisabeth Varga. Development of an Indirect Quantitation Method to Assess Ichthyotoxic B-Type Prymnesins from Prymnesium parvum. Toxins. 2019; 11 (5):251.

Chicago/Turabian Style

Daniel Killerup Svenssen; Sofie Bjørnholt Binzer; Nikola Medić; Per Juel Hansen; Thomas Ostenfeld Larsen; Elisabeth Varga. 2019. "Development of an Indirect Quantitation Method to Assess Ichthyotoxic B-Type Prymnesins from Prymnesium parvum." Toxins 11, no. 5: 251.

Journal article
Published: 11 February 2019 in World Mycotoxin Journal
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Immunoassay based techniques are an important and fast option for the detection and quantification of mycotoxins. They are frequently used as on-site screening tools in grain elevators, storage and production facilities. However, accurate quantification may be hampered by the co-recognition of structurally related metabolites by the used antibodies. Therefore, it is crucial to assess their cross-reactivity to avoid misinterpretation of the results. Several immunoassays for the determination of deoxynivalenol (DON) are commercially available. Recently, novel trichothecene mycotoxins with structures similar to DON, the NX-toxins (NX-2, NX-3 and NX-4), were discovered, which can potentially co-occur with DON in cereals. So far, no data about the cross-reactivity of those toxins with DON-antibodies are available. The aim of this study was to assess the cross-reactivities of NX-toxins and some other DON-related metabolites with DON-antibodies in buffer solutions. Six commercially available enzyme-linked immunosorbent assays (ELISAs) and two previously developed DON-antibodies (Mab#1 and Mab#22) were tested. Cross-reactivity with NX-metabolites was not observed for any of the ELISA-kits nor Mab#22, whereas Mab#1 reacted moderately against NX-3 and NX-4 (cross-reactivity based on a molar basis of 14 and 30%, respectively). Modifications at position C-3 (3-acetyl-DON and DON-3-glucoside) led to moderate or high cross-reactivity with Mab#22 and the commercial ELISA-kits, whereas these compounds were not recognised by Mab#1. Similar to NX-metabolites, 15-acetyl-DON interacted only weakly with Mab#22 and the commercial ELISA-kits, but strongly with Mab#1. The results demonstrate the importance of proper antibody characterisation. If NX-metabolites prove to be widely distributed and reach significant levels, the development of specific antibodies targeting these novel metabolites might become necessary.

ACS Style

N.T. Nguyen; E. Varga; C. Maragos; S. Baumgartner; G. Adam; F. Berthiller. Cross-reactivity of commercial and non-commercial deoxynivalenol-antibodies to emerging trichothecenes and common deoxynivalenol-derivatives. World Mycotoxin Journal 2019, 12, 45 -53.

AMA Style

N.T. Nguyen, E. Varga, C. Maragos, S. Baumgartner, G. Adam, F. Berthiller. Cross-reactivity of commercial and non-commercial deoxynivalenol-antibodies to emerging trichothecenes and common deoxynivalenol-derivatives. World Mycotoxin Journal. 2019; 12 (1):45-53.

Chicago/Turabian Style

N.T. Nguyen; E. Varga; C. Maragos; S. Baumgartner; G. Adam; F. Berthiller. 2019. "Cross-reactivity of commercial and non-commercial deoxynivalenol-antibodies to emerging trichothecenes and common deoxynivalenol-derivatives." World Mycotoxin Journal 12, no. 1: 45-53.

Journal article
Published: 28 November 2018 in Harmful Algae
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Harmful blooms formed by planktonic microalgae (HABs) in both freshwater and coastal waters regularly lead to severe mortalities of fish and invertebrates causing substantial economic losses of marine products worldwide. The mixotrophic haptophyte Prymnesium parvum is one of the most important microalgae associated with fish kills. Here 26 strains of P. parvum with a wide geographical distribution were screened for the production of prymnesins, the suspected causative allelochemical toxins. All investigated strains produced prymnesins, indicating that the toxins play an important role for the organism. The prymnesins can be classified into three types based on the length of the carbon backbone of the compound and each algal strain produced only one of these types. Biogeographical mapping of the prymnesin distribution indicated a global distribution of each type. In addition, phylogenetic analyses based on internal transcribed spacer (ITS) sequences revealed monophyletic origin of all prymnesin types and clades could therefore be defined based on the toxic compound. It might be that evolution of new species within the P. parvum species complex is driven by changes in toxin type or that they are a result of it. Such a correlation between chemotype and phylotype has never been documented before for a harmful microalga. Chemotaxonomy and ITS-type classification may thus be used to further delimit the P. parvum species complex.

ACS Style

Sofie Bjørnholt Binzer; Daniel Killerup Svenssen; Niels Daugbjerg; Catharina Alves-De-Souza; Ernani Pinto; Per Juel Hansen; Thomas Ostenfeld Larsen; Elisabeth Varga. A-, B- and C-type prymnesins are clade specific compounds and chemotaxonomic markers in Prymnesium parvum. Harmful Algae 2018, 81, 10 -17.

AMA Style

Sofie Bjørnholt Binzer, Daniel Killerup Svenssen, Niels Daugbjerg, Catharina Alves-De-Souza, Ernani Pinto, Per Juel Hansen, Thomas Ostenfeld Larsen, Elisabeth Varga. A-, B- and C-type prymnesins are clade specific compounds and chemotaxonomic markers in Prymnesium parvum. Harmful Algae. 2018; 81 ():10-17.

Chicago/Turabian Style

Sofie Bjørnholt Binzer; Daniel Killerup Svenssen; Niels Daugbjerg; Catharina Alves-De-Souza; Ernani Pinto; Per Juel Hansen; Thomas Ostenfeld Larsen; Elisabeth Varga. 2018. "A-, B- and C-type prymnesins are clade specific compounds and chemotaxonomic markers in Prymnesium parvum." Harmful Algae 81, no. : 10-17.

Journal article
Published: 06 March 2018 in Toxins
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Trichothecene toxins are confirmed or suspected virulence factors of various plant-pathogenic Fusarium species. Plants can detoxify these to a variable extent by glucosylation, a reaction catalyzed by UDP-glucosyltransferases (UGTs). Due to the unavailability of analytical standards for many trichothecene-glucoconjugates, information on such compounds is limited. Here, the previously identified deoxynivalenol-conjugating UGTs HvUGT13248 (barley), OsUGT79 (rice) and Bradi5g03300 (Brachypodium), were expressed in E. coli, affinity purified, and characterized towards their abilities to glucosylate the most relevant type A and B trichothecenes. HvUGT13248, which prefers nivalenol over deoxynivalenol, is also able to conjugate C-4 acetylated trichothecenes (e.g., T-2 toxin) to some degree while OsUGT79 and Bradi5g03300 are completely inactive with C-4 acetylated derivatives. The type A trichothecenes HT-2 toxin and T-2 triol are the kinetically preferred substrates in the case of HvUGT13248 and Bradi5g03300. We glucosylated several trichothecenes with OsUGT79 (HT-2 toxin, T-2 triol) and HvUGT13248 (T-2 toxin, neosolaniol, 4,15-diacetoxyscirpenol, fusarenon X) in the preparative scale. NMR analysis of the purified glucosides showed that exclusively β-D-glucosides were formed regio-selectively at position C-3-OH of the trichothecenes. These synthesized standards can be used to investigate the occurrence and toxicological properties of these modified mycotoxins.

ACS Style

Herbert Michlmayr; Elisabeth Varga; Alexandra Malachova; Philipp Fruhmann; Marta Piatkowska; Christian Hametner; Jana Šofrová; Günther Jaunecker; Georg Häubl; Marc Lemmens; Franz Berthiller; Gerhard Adam. UDP-Glucosyltransferases from Rice, Brachypodium, and Barley: Substrate Specificities and Synthesis of Type A and B Trichothecene-3-O-β-d-glucosides. Toxins 2018, 10, 111 .

AMA Style

Herbert Michlmayr, Elisabeth Varga, Alexandra Malachova, Philipp Fruhmann, Marta Piatkowska, Christian Hametner, Jana Šofrová, Günther Jaunecker, Georg Häubl, Marc Lemmens, Franz Berthiller, Gerhard Adam. UDP-Glucosyltransferases from Rice, Brachypodium, and Barley: Substrate Specificities and Synthesis of Type A and B Trichothecene-3-O-β-d-glucosides. Toxins. 2018; 10 (3):111.

Chicago/Turabian Style

Herbert Michlmayr; Elisabeth Varga; Alexandra Malachova; Philipp Fruhmann; Marta Piatkowska; Christian Hametner; Jana Šofrová; Günther Jaunecker; Georg Häubl; Marc Lemmens; Franz Berthiller; Gerhard Adam. 2018. "UDP-Glucosyltransferases from Rice, Brachypodium, and Barley: Substrate Specificities and Synthesis of Type A and B Trichothecene-3-O-β-d-glucosides." Toxins 10, no. 3: 111.

Journal article
Published: 23 December 2017 in Toxicology Letters
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A new type A trichothecene mycotoxin, NX-2, was previously reported to be produced by North American isolates of the cereal pathogen Fusarium graminearum. Here we describe the isolation and structural characterization of a rearrangement product, called NX2-M1, and related compounds with different acetylation patterns (NX3-M1 and NX4-M1). In the NX-M1 derivatives, the epoxide ring is opened, and a covalent bridge between C-10 and C-12 of the trichothecene backbone is formed. In vitro translation assays showed that NX3-M1 is less toxic for eukaryotic ribosomes than NX-3. NX3-M1 also has a greatly reduced cytotoxic potential on two tested human colon cell lines. Formation of NX3-M1 can therefore be regarded as a detoxification reaction. The related F. graminearum mycotoxin deoxynivalenol (DON), which is frequently occurring worldwide, is very stable during food processing. Testing NX-3 at different pH-values and temperature conditions, as well as under conditions that simulate the storage of infected grains and bread-making process, revealed a strongly reduced stability of NX-3 and concurrent formation of NX3-M1. Although the NX-3 formed in planta is as toxic as DON, the extensive formation of the non-toxic rearrangement product should be taken into account for risk assessment of this emerging food contaminant.

ACS Style

Elisabeth Varga; Gerlinde Wiesenberger; Lydia Woelflingseder; Krisztian Twaruschek; Christian Hametner; Marta Vaclaviková; Alexandra Malachová; Doris Marko; Franz Berthiller; Gerhard Adam. Less-toxic rearrangement products of NX-toxins are formed during storage and food processing. Toxicology Letters 2017, 284, 205 -212.

AMA Style

Elisabeth Varga, Gerlinde Wiesenberger, Lydia Woelflingseder, Krisztian Twaruschek, Christian Hametner, Marta Vaclaviková, Alexandra Malachová, Doris Marko, Franz Berthiller, Gerhard Adam. Less-toxic rearrangement products of NX-toxins are formed during storage and food processing. Toxicology Letters. 2017; 284 ():205-212.

Chicago/Turabian Style

Elisabeth Varga; Gerlinde Wiesenberger; Lydia Woelflingseder; Krisztian Twaruschek; Christian Hametner; Marta Vaclaviková; Alexandra Malachová; Doris Marko; Franz Berthiller; Gerhard Adam. 2017. "Less-toxic rearrangement products of NX-toxins are formed during storage and food processing." Toxicology Letters 284, no. : 205-212.

Journal article
Published: 09 February 2017 in Toxins
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Zearalenone (ZEN) is an estrogenic mycotoxin occurring in Fusarium-infected cereals. Glucosylation is an important plant defense mechanism and generally reduces the acute toxicity of mycotoxins to humans and animals. Toxicological information about ZEN-glucosides is limited due to the unavailability of larger amounts required for animal studies. HvUGT14077, a recently-validated ZEN-conjugating barley UDP-glucosyltransferase was expressed in Escherichia coli, affinity purified, and characterized. HvUGT14077 possesses high affinity (Km = 3 µM) and catalytic efficiency (kcat/Km = 190 s−1·mM−1) with ZEN. It also efficiently glucosylates the phase-I ZEN-metabolites α-zearalenol and β-zearalenol, with kcat/Km of 40 and 74 s−1·mM−1, respectively. HvUGT14077 catalyzes O-glucosylation at C-14 and C-16 with preference of 14-glucoside synthesis. Furthermore, relatively slow consecutive formation of 14,16-di-glucosides was observed; their structures were tentatively identified by mass spectrometry and for ZEN-14,16-di-glucoside confirmed by nuclear magnetic resonance spectroscopy. Recombinant HvUGT14077 allowed efficient preparative synthesis of ZEN-glucosides, yielding about 90% ZEN-14-glucoside and 10% ZEN-16-glucoside. The yield of ZEN-16-glucoside could be increased to 85% by co-incubation with a β-glucosidase highly selective for ZEN-14-glucoside. Depletion of the co-substrate UDP-glucose was counteracted by a sucrose synthase based regeneration system. This strategy could also be of interest to increase the yield of minor glucosides synthesized by other glucosyltransferases.

ACS Style

Herbert Michlmayr; Elisabeth Varga; Francesca Lupi; Alexandra Malachová; Christian Hametner; Franz Berthiller; Gerhard Adam. Synthesis of Mono- and Di-Glucosides of Zearalenone and α-/β-Zearalenol by Recombinant Barley Glucosyltransferase HvUGT14077. Toxins 2017, 9, 58 .

AMA Style

Herbert Michlmayr, Elisabeth Varga, Francesca Lupi, Alexandra Malachová, Christian Hametner, Franz Berthiller, Gerhard Adam. Synthesis of Mono- and Di-Glucosides of Zearalenone and α-/β-Zearalenol by Recombinant Barley Glucosyltransferase HvUGT14077. Toxins. 2017; 9 (2):58.

Chicago/Turabian Style

Herbert Michlmayr; Elisabeth Varga; Francesca Lupi; Alexandra Malachová; Christian Hametner; Franz Berthiller; Gerhard Adam. 2017. "Synthesis of Mono- and Di-Glucosides of Zearalenone and α-/β-Zearalenol by Recombinant Barley Glucosyltransferase HvUGT14077." Toxins 9, no. 2: 58.

Journal article
Published: 08 February 2017 in Toxins
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The Fusarium mycotoxin zearalenone (ZEN) can be conjugated with polar molecules, like sugars or sulfates, by plants and fungi. To date, the fate of these modified forms of ZEN has not yet been elucidated in animals. In order to investigate whether ZEN conjugates contribute to the total ZEN exposure of an individual, ZEN (10 µg/kg b.w.) and equimolar amounts of two of its plant metabolites (ZEN-14-O-β-glucoside, ZEN-16-O-β-glucoside) and of one fungal metabolite (ZEN-14-sulfate) were orally administered to four pigs as a single bolus using a repeated measures design. The concentrations of ZEN, its modified forms and its mammalian metabolites ZEN-14-glucuronide, α-zearalenol (α-ZEL) and α-ZEL-14-glucuronide in excreta were analyzed by high-performance liquid chromatography tandem mass spectrometry (HPLC-MS/MS) based methods. The biological recovery of ZEN in urine was 26% ± 10%, the total biological recovery in excreta was 40% ± 8%. Intact ZEN-14-sulfate, ZEN-14-O-β-glucoside and ZEN-16-O-β-glucoside were neither detected in urine nor in feces. After ZEN-14-sulfate application, 19% ± 5% of the administered dose was recovered in urine. In feces, no ZEN metabolites were detected. The total biological recoveries of ZEN-14-O-β-glucoside and ZEN-16-O-β-glucoside in the form of their metabolites in urine were 19% ± 11% and 13% ± 7%, respectively. The total biological recoveries in urine and feces amounted to 48% ± 7% and 34 ± 3%. An explanation for the low biological recoveries could be extensive metabolization by intestinal bacteria to yet unknown metabolites. In summary, ZEN-14-sulfate, ZEN-14-O-β-glucoside, and ZEN-16-O-β-glucoside were completely hydrolyzed in the gastrointestinal tract of swine, thus contributing to the overall toxicity of ZEN.

ACS Style

Sabina B. Binder; Heidi E. Schwartz-Zimmermann; Elisabeth Varga; Gerlinde Bichl; Herbert Michlmayr; Gerhard Adam; Franz Berthiller. Metabolism of Zearalenone and Its Major Modified Forms in Pigs. Toxins 2017, 9, 56 .

AMA Style

Sabina B. Binder, Heidi E. Schwartz-Zimmermann, Elisabeth Varga, Gerlinde Bichl, Herbert Michlmayr, Gerhard Adam, Franz Berthiller. Metabolism of Zearalenone and Its Major Modified Forms in Pigs. Toxins. 2017; 9 (2):56.

Chicago/Turabian Style

Sabina B. Binder; Heidi E. Schwartz-Zimmermann; Elisabeth Varga; Gerlinde Bichl; Herbert Michlmayr; Gerhard Adam; Franz Berthiller. 2017. "Metabolism of Zearalenone and Its Major Modified Forms in Pigs." Toxins 9, no. 2: 56.

Journal article
Published: 14 October 2016 in Toxins
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Trichothecenes are a class of structurally diverse mycotoxins with more than 200 naturally occurring compounds. Previously, a new compound, pentahydroxyscirpene (PHS), was reported as a byproduct of a nivalenol producing Fusarium strain, IFA189. PHS contains a hydroxy group at C-8 instead of the keto group of type B trichothecenes. In this work, we demonstrate that IFA189 belongs to the species Fusarium kyushuense using molecular tools. Production of PHS in vitro was also observed for several isolates of other Fusarium species producing nivalenol. Furthermore, we report the formation of 4-acetyl-PHS by F. kyushuense on inoculated rice. Wheat ears of the variety Remus were infected with IFA189 and the in planta production of PHS was confirmed. Natural occurrence of PHS was verified in barley samples from the Czech Republic using a liquid chromatographic-tandem mass spectrometric method validated for this purpose. Toxicity of PHS to wheat ribosomes was evaluated with a coupled in vitro transcription and translation assay, which showed that PHS inhibits protein biosynthesis slightly less than nivalenol and deoxynivalenol.

ACS Style

Elisabeth Varga; Gerlinde Wiesenberger; Philipp Fruhmann; Alexandra Malachová; Thomas Svoboda; Marc Lemmens; Gerhard Adam; Franz Berthiller. Pentahydroxyscirpene—Producing Strains, Formation In Planta, and Natural Occurrence. Toxins 2016, 8, 295 .

AMA Style

Elisabeth Varga, Gerlinde Wiesenberger, Philipp Fruhmann, Alexandra Malachová, Thomas Svoboda, Marc Lemmens, Gerhard Adam, Franz Berthiller. Pentahydroxyscirpene—Producing Strains, Formation In Planta, and Natural Occurrence. Toxins. 2016; 8 (10):295.

Chicago/Turabian Style

Elisabeth Varga; Gerlinde Wiesenberger; Philipp Fruhmann; Alexandra Malachová; Thomas Svoboda; Marc Lemmens; Gerhard Adam; Franz Berthiller. 2016. "Pentahydroxyscirpene—Producing Strains, Formation In Planta, and Natural Occurrence." Toxins 8, no. 10: 295.

Journal article
Published: 21 June 2016 in Food and Chemical Toxicology
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The gastrointestinal tract is the first target after ingestion of the mycotoxin deoxynivalenol (DON) via feed and food. Deoxynivalenol is known to affect the proliferation and viability of animal and human intestinal epithelial cells. In addition to DON, feed and food is often co-contaminated with modified forms of DON, such as 3-acetyldeoxynivalenol (3ADON), 15-acetyl-deoxynivalenol (15ADON) and deoxynivalenol-3-β-D-glucoside (DON3G). The goal of this study was to determine the in vitro intrinsic cytotoxicity of these modified forms towards differentiated and proliferative porcine intestinal epithelial cells by means of flow cytometry. Cell death was assessed by dual staining with Annexin-V-fluorescein isothiocyanate (FITC) and propidium iodide (PI), which allows the discrimination of viable (FITC−/PI−), apoptotic (FITC+/PI−) and necrotic cells (FITC+/PI+). Based on the data from the presented pilot in vitro study, it is concluded that cytotoxicity for proliferative cells can be ranked as follows: DON3G ≪ 3ADON < DON ≈ 15ADON.

ACS Style

Nathan Broekaert; Mathias Devreese; Kristel Demeyere; Franz Berthiller; Herbert Michlmayr; Elisabeth Varga; Gerhard Adam; Evelyne Meyer; Siska Croubels. Comparative in vitro cytotoxicity of modified deoxynivalenol on porcine intestinal epithelial cells. Food and Chemical Toxicology 2016, 95, 103 -109.

AMA Style

Nathan Broekaert, Mathias Devreese, Kristel Demeyere, Franz Berthiller, Herbert Michlmayr, Elisabeth Varga, Gerhard Adam, Evelyne Meyer, Siska Croubels. Comparative in vitro cytotoxicity of modified deoxynivalenol on porcine intestinal epithelial cells. Food and Chemical Toxicology. 2016; 95 ():103-109.

Chicago/Turabian Style

Nathan Broekaert; Mathias Devreese; Kristel Demeyere; Franz Berthiller; Herbert Michlmayr; Elisabeth Varga; Gerhard Adam; Evelyne Meyer; Siska Croubels. 2016. "Comparative in vitro cytotoxicity of modified deoxynivalenol on porcine intestinal epithelial cells." Food and Chemical Toxicology 95, no. : 103-109.

Journal article
Published: 25 December 2015 in Toxins
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Increasing frequencies of 3-acetyl-deoxynivalenol (3-ADON)-producing strains of Fusarium graminearum (3-ADON chemotype) have been reported in North America and Asia. 3-ADON is nearly nontoxic at the level of the ribosomal target and has to be deacetylated to cause inhibition of protein biosynthesis. Plant cells can efficiently remove the acetyl groups of 3-ADON, but the underlying genes are yet unknown. We therefore performed a study of the family of candidate carboxylesterases (CXE) genes of the monocot model plant Brachypodium distachyon. We report the identification and characterization of the first plant enzymes responsible for deacetylation of trichothecene toxins. The product of the BdCXE29 gene efficiently deacetylates T-2 toxin to HT-2 toxin, NX-2 to NX-3, both 3-ADON and 15-acetyl-deoxynivalenol (15-ADON) into deoxynivalenol and, to a lesser degree, also fusarenon X into nivalenol. The BdCXE52 esterase showed lower activity than BdCXE29 when expressed in yeast and accepts 3-ADON, NX-2, 15-ADON and, to a limited extent, fusarenon X as substrates. Expression of these Brachypodium genes in yeast increases the toxicity of 3-ADON, suggesting that highly similar genes existing in crop plants may act as susceptibility factors in Fusarium head blight disease.

ACS Style

Clemens Schmeitzl; Elisabeth Varga; Benedikt Warth; Karl G. Kugler; Alexandra Malachová; Herbert Michlmayr; Gerlinde Wiesenberger; Klaus F. X. Mayer; Hans-Werner Mewes; Rudolf Krska; Rainer Schuhmacher; Franz Berthiller; Gerhard Adam. Identification and Characterization of Carboxylesterases from Brachypodium distachyon Deacetylating Trichothecene Mycotoxins. Toxins 2015, 8, 6 .

AMA Style

Clemens Schmeitzl, Elisabeth Varga, Benedikt Warth, Karl G. Kugler, Alexandra Malachová, Herbert Michlmayr, Gerlinde Wiesenberger, Klaus F. X. Mayer, Hans-Werner Mewes, Rudolf Krska, Rainer Schuhmacher, Franz Berthiller, Gerhard Adam. Identification and Characterization of Carboxylesterases from Brachypodium distachyon Deacetylating Trichothecene Mycotoxins. Toxins. 2015; 8 (1):6.

Chicago/Turabian Style

Clemens Schmeitzl; Elisabeth Varga; Benedikt Warth; Karl G. Kugler; Alexandra Malachová; Herbert Michlmayr; Gerlinde Wiesenberger; Klaus F. X. Mayer; Hans-Werner Mewes; Rudolf Krska; Rainer Schuhmacher; Franz Berthiller; Gerhard Adam. 2015. "Identification and Characterization of Carboxylesterases from Brachypodium distachyon Deacetylating Trichothecene Mycotoxins." Toxins 8, no. 1: 6.

Research paper
Published: 03 September 2015 in Analytical and Bioanalytical Chemistry
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An extensive study of the metabolism of the type A trichothecene mycotoxins HT-2 toxin and T-2 toxin in barley using liquid chromatography coupled to high-resolution mass spectrometry (LC-HRMS) is reported. A recently developed untargeted approach based on stable isotopic labelling, LC-Orbitrap-MS analysis with fast polarity switching and data processing by MetExtract software was combined with targeted LC-Q-TOF-MS(/MS) analysis for metabolite structure elucidation and quantification. In total, 9 HT-2 toxin and 13 T-2 toxin metabolites plus tentative isomers were detected, which were successfully annotated by calculation of elemental formulas and further LC-HRMS/MS measurements as well as partly identified with authentic standards. As a result, glucosylated forms of the toxins, malonylglucosides, and acetyl and feruloyl conjugates were elucidated. Additionally, time courses of metabolite formation and mass balances were established. For absolute quantification of those compounds for which standards were available, the method was validated by determining apparent recovery, signal suppression, or enhancement and extraction recovery. Most importantly, T-2 toxin was rapidly metabolised to HT-2 toxin and for both parent toxins HT-2 toxin-3-O-β-glucoside was identified (confirmed by authentic standard) as the main metabolite, which reached its maximum already 1 day after toxin treatment. Isotope-assisted untargeted screening of HT-2 toxin and T-2 toxin metabolites in barley

ACS Style

Jacqueline Meng-Reiterer; Elisabeth Varga; Alexis V. Nathanail; Christoph Bueschl; Justyna Rechthaler; Susan McCormick; Herbert Michlmayr; Alexandra Malachová; Philipp Fruhmann; Gerhard Adam; Franz Berthiller; Marc Lemmens; Rainer Schuhmacher. Tracing the metabolism of HT-2 toxin and T-2 toxin in barley by isotope-assisted untargeted screening and quantitative LC-HRMS analysis. Analytical and Bioanalytical Chemistry 2015, 407, 8019 -8033.

AMA Style

Jacqueline Meng-Reiterer, Elisabeth Varga, Alexis V. Nathanail, Christoph Bueschl, Justyna Rechthaler, Susan McCormick, Herbert Michlmayr, Alexandra Malachová, Philipp Fruhmann, Gerhard Adam, Franz Berthiller, Marc Lemmens, Rainer Schuhmacher. Tracing the metabolism of HT-2 toxin and T-2 toxin in barley by isotope-assisted untargeted screening and quantitative LC-HRMS analysis. Analytical and Bioanalytical Chemistry. 2015; 407 (26):8019-8033.

Chicago/Turabian Style

Jacqueline Meng-Reiterer; Elisabeth Varga; Alexis V. Nathanail; Christoph Bueschl; Justyna Rechthaler; Susan McCormick; Herbert Michlmayr; Alexandra Malachová; Philipp Fruhmann; Gerhard Adam; Franz Berthiller; Marc Lemmens; Rainer Schuhmacher. 2015. "Tracing the metabolism of HT-2 toxin and T-2 toxin in barley by isotope-assisted untargeted screening and quantitative LC-HRMS analysis." Analytical and Bioanalytical Chemistry 407, no. 26: 8019-8033.

Journal article
Published: 01 September 2015 in Cereal Research Communications
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ACS Style

V. Shala-Mayrhofer; R. Marjakaj; Elisabeth Varga; F. Berthiller; A. Musolli; M. Lemmens. Occurrence of Fusarium head blight and mycotoxins as well as morphological identification ofFusariumspecies in winter wheat in Kosovo. Cereal Research Communications 2015, 43, 438 -448.

AMA Style

V. Shala-Mayrhofer, R. Marjakaj, Elisabeth Varga, F. Berthiller, A. Musolli, M. Lemmens. Occurrence of Fusarium head blight and mycotoxins as well as morphological identification ofFusariumspecies in winter wheat in Kosovo. Cereal Research Communications. 2015; 43 (3):438-448.

Chicago/Turabian Style

V. Shala-Mayrhofer; R. Marjakaj; Elisabeth Varga; F. Berthiller; A. Musolli; M. Lemmens. 2015. "Occurrence of Fusarium head blight and mycotoxins as well as morphological identification ofFusariumspecies in winter wheat in Kosovo." Cereal Research Communications 43, no. 3: 438-448.