Abstract
Contamination with enniatins A, A1, B and B1 was investigated in 1240 samples of small grain cereals (470 wheat, 260 durum wheat, 282 spring barley, 172 triticale and 56 winter barley) from the French harvests of 2012 to 2014. Associations with Fusarium avenaceum, F. tricinctum and F. poae were assessed, with the identification of Fusarium species by real-time PCR and mycotoxin quantification by LC–MS/MS. Enniatins were common in the fields sampled. Enniatin concentrations varied between years but were consistently highest on spring barley (mean values of 199 to 1316 μg/kg) and triticale (mean values from 131 to 1218 μg/kg), and lower on wheat (mean values from 47 to 142 μg/kg) and durum wheat (mean values from 55 to 596 μg/kg). The concentrations of the various enniatins were strongly correlated with each other (Pearson’s correlation coefficient of 0.61 to 0.98). Enniatin B was the most frequent (68% of the total enniatin content), followed by enniatin B1 (22%), enniatin A1 (7%) and enniatin A (3%). Fusarium species were quantified by calculating arithmetic mean total DNA levels. F. tricinctum was the most abundant (0.177 pg/ng total DNA), followed by F. avenaceum (0.141 pg/ng total DNA) and F. poae (0.091 pg/ng total DNA). Total DNA levels for each species, and the predominant species varied between years and crops. Small grain cereal species (p value < 0.001), harvest year (p value = < 0.001) and the presence of F. avenaceum (p value < 0.001), F. tricinctum (p value < 0.001) or F. poae (p value = 0.017) affected enniatin content. F. tricinctum was the leading enniatin producer on durum wheat (29% to 45%) and spring barley (23 to 37%). F. avenaceum produced large amounts of enniatins on durum wheat (13% to 17%) and wheat (1% to 18%) and was the leading producer on triticale (30% to 55%). F. poae made a minor contribution on all crops, never accounting for more than 2% of total enniatin content. Enniatins are, thus, highly prevalent in French small grain cereals and are mostly produced by F. avenaceum and F. tricinctum.
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Data availability
The raw datasets generated and analysed in this study are very large and are not publicly available: they are the property of ARVALIS-Institut du végétal. All data generated or analysed during this study are included in this published article in the form of descriptive tables.
References
Bottalico A (1998) Fusarium diseases of cereals: species complex and related mycotoxin profiles in Europe. Eur J Plant Pathol 80:85–103
Bottalico A, Perrone G (2002) Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur J Plant Pathol 108:611–624. https://doi.org/10.1023/A:1020635214971
Boutigny AL, Gautier A, Basler R, Dauthieux F, Leite S, Valade R, Aguayo J, Ioos R, Laval V (2019) Metabarcoding targeting the EF1 alpha region to assess Fusarium diversity on cereals. PLoS One 14(1):e0207988. https://doi.org/10.1371/journal.pone.0207988
Bryla M, Waskiewicz A, Podolska G, Szymczyk K, Jedrezjczak R, Damaziak K, Sulek A (2016) Occurrence of 26 mycotoxins in the grain of cereals cultivated in Poland. Toxins 8(6):160. https://doi.org/10.3390/toxins8060160
Burmeister HR, Plattner RD (1987) Enniatin production by Fusarium tricinctum and its effect on germinating wheat seeds. Phytopathology 77:1483–1487. https://doi.org/10.1094/Phyto-77-1483
COFRAC (French Committee for Accreditation) (2017) Technical guide to accreditation: mycotoxins and phycotoxins in foodstuffs intended for humans or animals. Available at: https://www.cofrac.fr/documentation/LAB-GTA-21. Accessed Jan 2019
Decleer M, Landschoot S, De Saeger S, Rajkovic A, Audenaert K (2018) Impact of fungicides and weather on cyclodepsipeptide-producing Fusarium spp. and beauvericin and enniatin levels in wheat grains. J Sci Food Agric 99:253–262. https://doi.org/10.1002/jsfa.9167
Elbelt S, Siou D, Gelisse S, Cruaud C, Lannou C, Lebrun MH, Laval V (2018) Optimized real-time qPCR assays for detecting and quantifying the Fusarium and Microdochium species responsible for wheat head blight, as defined by MIQE guidelines. BioRix:272534. https://doi.org/10.1101/272534
European Food Safety Authority (2014) Scientific opinion on the risks to human and animal health related to the presence of beauvericin and enniatins in food and feed. EFSA J 2014(12):3802, 174 pp. https://doi.org/10.2903/j.efsa.2014.3802
Fox J, Weisberg S (2011) An R companion to applied regression, second edition. Thousand oaks CA: Sage. Available at: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion. Accessed July 2018
Gäumann E, Roth S, Ettlinger L, Plattnerp A, Nager U (1947) Enniatin, ein neues, gegen Mykobakterien wirksames Antibiotikum. Experientia 3:202–203. https://doi.org/10.1007/BF02163993
Gorczyca A, Oleksy A, Gala-Czekaj D, Urbaniak M, Laskowska M, Waśkiewicz A, Stępień Ł (2018) Fusarium head blight incidence and mycotoxin accumulation in three durum wheat cultivars in relation to sowing date and density. Sci Nat 105:2. https://doi.org/10.1007/s00114-017-1528-7
Gourdain E, Piraux F, Barrier-Guillot B (2011) A model combining agronomic and weather factors to predict occurrence of deoxynivalenol in durum wheat kernels. World Mycotoxin J 4(2):129–139. https://doi.org/10.3920/WMJ2009.1190
Ioos R, Belhadj A, Menez M (2002) Occurrence and distribution of Microdochium nivale and Fusarium species isolated from barley, durum and soft wheat grains in France from 2000 to 2002. Mycopathologia 158:351–362
Ioos R, Belhadj A, Menez M, Faure A (2005) The effects of fungicides on Fusarium spp. and Microdochium nivale and their associated trichothecene mycotoxins in French naturally-infected cereal grains. Crop Prot 24:894–902
Jestoi M, Rokka M, Yli-Mattila T, Parikka P, Rizzo A, Peltonen K (2004) Presence and concentrations of the Fusarium-related mycotoxins beauvericin, enniatins and moniliformin in Finnish grain samples. Food Addit Contam 21(8):794–802. https://doi.org/10.1080/02652030410001713906
Juan C, Mañes J, Raiola A, Ritieni A (2013) Evaluation of beauvericin and enniatins in Italian cereal products and multicereal food by liquid chromatography coupled to triple quadrupole mass spectrometry. Food Chem 140:755–762. https://doi.org/10.1016/j.foodchem.2012.08.02
Lenth RV (2018) Package lsmeans. Available at: https://cran.r-project.org/web/packages/lsmeans/lsmeans.pdf. Accessed July 2018
Logrieco A, Rizzo A, Ferracane R, Ritieni A (2002) Occurrence of beauvericin and enniatins in wheat affected by Fusarium avenaceum head blight. Appl Environ Microbiol 68:82–85. https://doi.org/10.1128/AEM.68.1.82-85.2002
Météo France (2018) Bilan climatiques. http://www.meteofrance.fr/climat-passe-et-futur/bilans-climatiques Accessed 27 November 2018
Nazari L, Pattori E, Manstretta V, Terzi V, Morcia C, Somma S, Moretti A, Ritieni A, Rossi V (2018) Effect of temperature on growth, wheat head infection, and nivalenol production by Fusarium poae. Food Microbiol 76:83–90 https://www.sciencedirect.com/science/article/pii/S0740002017310110?via%3Dihub
Nielsen LK, Cookb DJ, Edward SG, Ray RV (2014) The prevalence and impact of Fusarium head blight pathogens and mycotoxins on malting barley quality in UK. Int J Food Microbiol 179:38–49. https://doi.org/10.1016/j.ijfoodmicro.2014.03.023
Opoku N, Back MA, Edwards SG (2018) Susceptibility of cereal species to Fusarium langsethiae under identical field conditions. Eur J Plant Pathol 150:869–879. https://doi.org/10.1007/s10658-017-1329-z
R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rossi V, Ravanetti A, Pattori E, Giosuè S (2001) Influence of temperature and humidity on the infection of wheat spikes by some fungi causing Fusarium head blight. J Plant Pathol 83(3):189–198
Santini A, Meca G, Uhlig S, Ritieni A (2012) Fusaproliferin, beauvericin and enniatins: occurrence in food review. World Mycotoxin J 5:71–81. https://doi.org/10.3920/WMJ2011.1331
Smith MC, Madec S, Coton E, Hymery N (2016) Natural co-occurrence of mycotoxins in foods and feeds and their in vitro combined toxicological effects. Toxins 8:94. https://doi.org/10.3390/toxins8040094
Stanciu O, Juan C, Miere D, Loghin F, Mañes J (2017) Occurrence and co-occurrence of Fusarium mycotoxins in wheat grains and wheat flour from Romania. Food Control 73:147–155. https://doi.org/10.1016/j.foodcont.2016.07.042
Svingen T, Hansen NL, Taxvig C, Vinggaard AM, Jensen U, Rasmussen PH, (2017) Enniatin B and beauvericin are common in Danish cereals and show high hepatotoxicity on a high-content imaging platform. Environmental Toxicology 32(5):1658–1664
Sy-Cordero AA, Pearce CJ, Oberlies NH (2012) Revisiting the enniatins: a review of their isolation, biosynthesis, structure determination and biological activities. J Antibiot 65:541–549. https://doi.org/10.1038/ja.2012.71
Tittlemier SA, Roscoe M, Trelka R, Gaba D, Chan JM, Patrick SK, Sulyok M, Krska R, McKendry T, Gräfenhan T (2013) Fusarium damage in small cereal grains from western Canada. Occurrence of Fusarium toxins and their source organisms in durum wheat harvested in 2010. J Agric Food Chem 61:5438–5448. https://doi.org/10.1021/jf400652e
Tuffet C, Berthoud A (2015) Fusariose des épis du blé: opération Cartofusa. Phytoma 686:22–25
Uhlig S, Ivanova L (2004) Determination of beauvericin and four other enniatins in grain by liquid chromatography–mass spectrometry. J Chromatogr A 1050:173–178. https://doi.org/10.1016/j.chroma.2004.08.031
Uhlig S, Torp M, Heier BT (2006) Beauvericin and enniatins A, A1, B and B1 in Norwegian grain: a survey. Food Chem 94:193–201. https://doi.org/10.1016/j.foodchem.2004.11.004
Vogelgsang S, Sulyok M, Hecker A, Jenny E, Krsja R, Schuhmacher R, Forrer HR (2008) Toxigenicity and pathogenicity of Fusarium poae and Fusarium avenaceum on wheat. Eur J Plant Pathol 122:265–276. https://doi.org/10.1016/j.foodchem.2004.11.004
Wright K (2018) Package ‘corrgram’ Available at: https://cran.rproject.org/web/packages/corrgram/corrgram.pdf. Accessed July 2018
Acknowledgments
We thank FranceAgriMer and all the farmers involved for their commitment to this study.
We also thank the ARVALIS-Institut du végétal technical team in Villerable for cleaning and preparing all the samples analysed.
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We thank FranceAgriMer for the financial support.
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Orlando, B., Grignon, G., Vitry, C. et al. Fusarium species and enniatin mycotoxins in wheat, durum wheat, triticale and barley harvested in France. Mycotoxin Res 35, 369–380 (2019). https://doi.org/10.1007/s12550-019-00363-x
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DOI: https://doi.org/10.1007/s12550-019-00363-x