¹Department of Plant Pathology, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, OH 44691
²USDA-ARS-CSWQRU, Soft Wheat Quality Laboratory, Wooster, OH 44691
³Department of Plant Sciences, North Dakota State University, Fargo, ND 58108

Published Online:5 Mar 2023https://doi.org/10.1094/PHYTO-06-22-0199-R

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Abstract

Fusarium head blight (FHB) of wheat, caused by the fungus Fusarium graminearum, is associated with grain contamination with mycotoxins such as deoxynivalenol (DON). Although FHB is often positively correlated with DON, this relationship can break down under certain conditions. One possible explanation for this could be the conversion of DON to DON-3-glucoside (D3G), which is typically missed by common DON testing methods. The objective of this study was to quantify the effects of temperature, relative humidity (RH), and preharvest rainfall on DON, D3G, and the D3D/DON relationship. D3G levels were higher in grain from spikes exposed to 100% RH than to 70, 80, or 90% RH at 20 and 25°C across all tested levels of mean FHB index (percentage of diseased spikelets per spike). Mean D3G contamination was higher at 20°C than at 25 or 30°C. There were significantly positive linear relationships between DON and D3G. Rainfall treatments resulted in significantly higher mean D3G than the rain-free check and induced preharvest sprouting, as indicated by low falling numbers (FNs). There were significant positive relationships between the rate of increase in D3G per unit increase in DON (a measure of conversion) and sprouting. As FN decreased, the rate of D3G conversion increased, and this rate of conversion per unit decrease in FN was greater at relatively low than at high mean DON levels. These results provide strong evidence that moisture after FHB visual symptom development was associated with DON-to-D3G conversion and constitute valuable new information for understanding this complex disease-mycotoxin system.

Literature Cited

AACC International. 2001. Determination of falling number. Method 56–81.03 in: Approved Methods of Analysis, 11th ed. AACCI, St. Paul, MN. Google Scholar
Andersen, K. F., Madden, L. V., and Paul, P. A. 2015. Fusarium head blight development and deoxynivalenol accumulation in wheat as influenced by post-anthesis moisture patterns. Phytopathology 105:210-219. https://doi.org/10.1094/PHYTO-04-14-0104-R Link, ISI, Google Scholar
Audenaert, K., De Boevre, M., Vanheule, A., Callewaert, J., Bekaert, B., Höfte, M., De Saeger, S., and Haesaert, G. 2013. Mycotoxin glucosylation in commercial wheat varieties: Impact on resistance to Fusarium graminearum under laboratory and field conditions. Food Control 34:756-762. https://doi.org/10.1016/j.foodcont.2013.06.019 Crossref, ISI, Google Scholar
Bai, G.-H., Desjardins, A. E., and Plattner, R. D. 2002. Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91-98. https://doi.org/10.1023/A:1014419323550 Crossref, Medline, ISI, Google Scholar
Berthiller, F., Crews, C., Dall'Asta, C., Saeger, S. D., Haesaert, G., Karlovsky, P., Oswald, I. P., Seefelder, W., Speijers, G., and Stroka, J. 2013. Masked mycotoxins: A review. Mol. Nutr. Food Res. 57:165-186. https://doi.org/10.1002/mnfr.201100764 Crossref, Medline, ISI, Google Scholar
Berthiller, F., Krska, R., Domig, K. J., Kneifel, W., Juge, N., Schuhmacher, R., and Adam, G. 2011. Hydrolytic fate of deoxynivalenol-3-glucoside during digestion. Toxicol. Lett. 206:264-267. https://doi.org/10.1016/j.toxlet.2011.08.006 Crossref, Medline, ISI, Google Scholar
Cowger, C., and Arrellano, C. 2010. Plump kernels with high deoxynivalenol linked to late Gibberella zeae infection and marginal disease conditions in winter wheat. Phytopathology 100:719-728. https://doi.org/10.1094/PHYTO-100-7-0719 Link, ISI, Google Scholar
Cowger, C., Patton-Özkurt, J., Brown-Guedira, G., and Perugini, L. 2009. Post-anthesis moisture increased Fusarium head blight and deoxynivalenol levels in North Carolina winter wheat. Phytopathology 99:320-327. https://doi.org/10.1094/PHYTO-99-4-0320 Link, ISI, Google Scholar
Culler, M. D., Miller-Garvin, J. E., and Dill-Macky, R. 2007. Effect of extended irrigation and host resistance on deoxynivalenol accumulation in Fusarium-infected wheat. Plant Dis. 91:1464-1472. https://doi.org/10.1094/PDIS-91-11-1464 Link, ISI, Google Scholar
Dall'Erta, A., Cirlini, M., Dall'Asta, M., Del Rio, D., Galaverna, G., and Dall'Asta, C. 2013. Masked mycotoxins are efficiently hydrolyzed by human colonic microbiota releasing their aglycones. Chem. Res. Toxicol. 26:305-312. https://doi.org/10.1021/tx300438c Crossref, Medline, ISI, Google Scholar
D'Angelo, D. L., Bradley, C. A., Ames, K. A., Willyerd, K. T., Madden, L. V., and Paul, P. A. 2014. Efficacy of fungicide applications during and after anthesis against Fusarium head blight and deoxynivalenol in soft red winter wheat. Plant Dis. 98:1387-1397. https://doi.org/10.1094/PDIS-01-14-0091-RE Link, ISI, Google Scholar
Del Ponte, E. M., Fernandes, J. M. C., and Bergstrom, G. C. 2007. Influence of growth stage on Fusarium head blight and deoxynivalenol production in wheat. J. Phytopathol. 155:577-581. https://doi.org/10.1111/j.1439-0434.2007.01281.x Crossref, ISI, Google Scholar
Derera, N. F. 1989. The effects of preharvest rain. Pages 1-14 in: Preharvest Field Sprouting in Cereals. N. F. Derera, ed. CRC Press, Boca Raton, FL. Google Scholar
Desjardins, A. E., Proctor, R. H., Bai, G., McCormick, S. P., Shaner, G., Buechley, G., and Hohn, T. M. 1996. Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Mol. Plant-Microbe Interact. 9:775-781. https://doi.org/10.1094/MPMI-9-0775 Crossref, ISI, Google Scholar
DeWolf, E., and Paul, P. A. 2014. Predicting mycotoxin contamination in wheat. Page 248 in: Mycotoxin Reduction in Grain Chains. J. F. Leslie and A. F. Logrieco, eds. Wiley Blackwell, Hoboken, NJ. Google Scholar
Edwards, R. A., Ross, A. S., Mares, D. J., Ellison, F. W., and Tomlinson, J. D. 1989. Enzymes from rain-damaged and laboratory-germinated wheat I. Effects on product quality. J. Cereal Sci. 10:157-167. https://doi.org/10.1016/S0733-5210(89)80044-X Crossref, ISI, Google Scholar
EFSA Panel on Contaminants in the Food Chain (EFSA CONTAM Panel), Knutsen, H. K., Alexander, J., Barregård, L., Bignami, M., Brüschweiler, B., Ceccatelli, S., Cottrill, B., Dinovi, M., and Grasl-Kraupp, B. 2017. Risks to human and animal health related to the presence of deoxynivalenol and its acetylated and modified forms in food and feed. EFSA J. 15:4718. ISI, Google Scholar
EFSA Panel on Contaminants in the Food Chain (EFSA CONTAM Panel). 2014. Scientific Opinion on the risks for human and animal health related to the presence of modified forms of certain mycotoxins in food and feed. EFSA J. 12:3916. Google Scholar
Foroud, N. A., and Eudes, F. 2009. Trichothecenes in cereal grains. Int. J. Mol. Sci. 10:147-173. https://doi.org/10.3390/ijms10010147 Crossref, Medline, ISI, Google Scholar
Frandsen, T. P., Lok, F., Mirgorodskaya, E., Roepstorff, P., and Svensson, B. 2000. Purification, enzymatic characterization, and nucleotide sequence of a high-isoelectric-point α-glucosidase from barley malt. Plant Physiol. 123:275-286. https://doi.org/10.1104/pp.123.1.275 Crossref, Medline, ISI, Google Scholar
Galaverna, G., DallAsta, C., Mangia, M., Dossena, A., and Marchelli, R. 2009. Masked mycotoxins: An emerging issue for food safety. Czech J. Food Sci. 27:S89. https://doi.org/10.17221/1064-CJFS Crossref, ISI, Google Scholar
Gardiner, D. M., Kazan, K., and Manners, J. M. 2009. Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet. Biol. 46:604-613. https://doi.org/10.1016/j.fgb.2009.04.004 Crossref, Medline, ISI, Google Scholar
Gautam, P., and Dill-Macky, R. 2012. Free water can leach mycotoxins from Fusarium-infected wheat heads. J. Phytopathol. 160:484-490. https://doi.org/10.1111/j.1439-0434.2012.01928.x Crossref, ISI, Google Scholar
González-Arias, C. A., Marín, S., Sanchis, V., and Ramos, A. 2013. Mycotoxin bioaccessibility/absorption assessment using in vitro digestion models: A review. World Mycotoxin J. 6:167-184. https://doi.org/10.3920/WMJ2012.1521 Crossref, ISI, Google Scholar
Hagberg, S. 1961. Note on a simplified rapid method for determining alpha-amylase activity. Cereal Chem. 38:202-203. ISI, Google Scholar
Hughes, K., Griffey, C., Parrish, D., Barbeau, W., Souza, E., and Thomason, W. 2010. Preharvest sprouting tolerance in current soft red winter wheat cultivars. Crop Sci. 50:1449-1457. https://doi.org/10.2135/cropsci2009.09.0497 Crossref, ISI, Google Scholar
Ilgen, P., Hadeler, B., Maier, F. J., and Schäfer, W. 2009. Developing kernel and rachis node induce the trichothecene pathway of Fusarium graminearum during wheat head infection. Mol. Plant-Microbe Interact. 22:899-908. https://doi.org/10.1094/MPMI-22-8-0899 Link, ISI, Google Scholar
Jin, Z., Zhou, B., Gillespie, J., Gross, T., Barr, J., Simsek, S., Brueggeman, R., and Schwarz, P. 2018. Production of deoxynivalenol (DON) and DON-3-glucoside during the malting of Fusarium infected hard red spring wheat. Food Control 85:6-10. https://doi.org/10.1016/j.foodcont.2017.09.002 Crossref, ISI, Google Scholar
Kang, Z., and Buchenauer, H. 1999. Immunocytochemical localization of Fusarium toxins in infected wheat spikes by Fusarium culmorum. Physiol. Mol. Plant Pathol. 55:275-288. https://doi.org/10.1006/pmpp.1999.0233 Crossref, ISI, Google Scholar
Karlovsky, P. 2011. Biological detoxification of the mycotoxin deoxynivalenol and its use in genetically engineered crops and feed additives. Appl. Microbiol. Biotechnol. 91:491-504. https://doi.org/10.1007/s00253-011-3401-5 Crossref, Medline, ISI, Google Scholar
Kluger, B., Bueschl, C., Lemmens, M., Michlmayr, H., Malachova, A., Koutnik, A., Maloku, I., Berthiller, F., Adam, G., and Krska, R. 2015. Biotransformation of the mycotoxin deoxynivalenol in Fusarium resistant and susceptible near isogenic wheat lines. PLoS One 10:e0119656. https://doi.org/10.1371/journal.pone.0119656 Crossref, Medline, ISI, Google Scholar
Köppen, R., Koch, M., Siegel, D., Merkel, S., Maul, R., and Nehls, I. 2010. Determination of mycotoxins in foods: Current state of analytical methods and limitations. Appl. Microbiol. Biotechnol. 86:1595-1612. https://doi.org/10.1007/s00253-010-2535-1 Crossref, Medline, ISI, Google Scholar
Kostelanska, M., Dzuman, Z., Malachova, A., Capouchova, I., Prokinova, E., Skerikova, A., and Hajslova, J. 2011. Effects of milling and baking technologies on levels of deoxynivalenol and its masked form deoxynivalenol-3-glucoside. J. Agric. Food Chem. 59:9303-9312. https://doi.org/10.1021/jf202428f Crossref, Medline, ISI, Google Scholar
Kostelanska, M., Hajslova, J., Zachariasova, M., Malachova, A., Kalachova, K., Poustka, J., Fiala, J., Scott, P. M., Berthiller, F., and Krska, R. 2009. Occurrence of deoxynivalenol and its major conjugate, deoxynivalenol-3-glucoside, in beer and some brewing intermediates. J. Agric. Food Chem. 57:3187-3194. https://doi.org/10.1021/jf803749u Crossref, Medline, ISI, Google Scholar
Kovalsky, P., Kos, G., Nährer, K., Schwab, C., Jenkins, T., Schatzmayr, G., Sulyok, M., and Krska, R. 2016. Co-occurrence of regulated, masked and emerging mycotoxins and secondary metabolites in finished feed and maize—An extensive survey. Toxins (Basel) 8:363. https://doi.org/10.3390/toxins8120363 Crossref, Medline, ISI, Google Scholar
Kutner, M. H., Nachtsheim, C. J., and Neter, J. 2004. Applied Linear Regression Models. 4th ed. McGraw-Hill/Irwin, New York, NY. Google Scholar
Lancova, K., Hajslova, J., Poustka, J., Krplova, A., Zachariasova, M., Dostálek, P., and Sachambula, L. 2008. Transfer of Fusarium mycotoxins and ‘masked’ deoxynivalenol (deoxynivalenol-3-glucoside) from field barley through malt to beer. Food Addit. Contam. 25:732-744. https://doi.org/10.1080/02652030701779625 Crossref, ISI, Google Scholar
Lemmens, M., Scholz, U., Berthiller, F., Dall'Asta, C., Koutnik, A., Schuhmacher, R., Adam, G., Buerstmayr, H., Mesterházy, Á., and Krska, R. 2005. The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for Fusarium head blight resistance in wheat. Mol. Plant-Microbe Interact. 18:1318-1324. https://doi.org/10.1094/MPMI-18-1318 Link, ISI, Google Scholar
Lemmens, M., Steiner, B., Sulyok, M., Nicholson, P., Mesterhazy, A., and Buerstmayr, H. 2016. Masked mycotoxins: Does breeding for enhanced Fusarium head blight resistance result in more deoxynivalenol-3-glucoside in new wheat varieties? World Mycotoxin J. 9:741-754. https://doi.org/10.3920/WMJ2015.2029 Crossref, ISI, Google Scholar
Lindsey, L. E., Lentz, E., Michel, A., Tilmon, K., Culman, S., and Paul, P. 2017. Small grain production. Pages 69-81 in: Ohio Agronomy Guide, 15th ed. D. Barker, S. Culman, A. Dorrance, J. Fulton, R. Haden, E. Lentz, A. Lindsey, L. Lindsey, M. Loux, E. McCoy, A. Michel, J. Noel, P. Paul, M. Sulc, P. Thomison, K. Tilmon, and J. Witter, eds. The Ohio State University, Columbus, OH. Google Scholar
Madden, L., and Paul, P. 2011. Meta-analysis for evidence synthesis in plant pathology: An overview. Phytopathology 101:16-30. https://doi.org/10.1094/PHYTO-03-10-0069 Link, ISI, Google Scholar
Madden, L. V., and Paul, P. A. 2020. Is disease intensity a good surrogate for yield loss or toxin contamination? A case study with Fusarium head blight of wheat. Phytopathology 110:1632-1646. https://doi.org/10.1094/PHYTO-11-19-0427-R Link, ISI, Google Scholar
Maier, F. J., Miedaner, T., Hadeler, B., Felk, A., Salomon, S., Lemmens, M., Kassner, H., and Schäfer, W. 2006. Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Mol. Plant Pathol. 7:449-461. https://doi.org/10.1111/j.1364-3703.2006.00351.x Crossref, Medline, ISI, Google Scholar
Major, B., Kettlewell, P., and Scott, R. 2001. Mechanisms leading to excess alpha-amylase activity in wheat (Triticum aestivum L.) grain in the UK. J. Cereal Sci. 33:313-329. Crossref, ISI, Google Scholar
Mares, D., Mrva, K., and Panozzo, J. 1994. Characterization of the high α-amylase levels in grain of the wheat cultivar BD 159. Aust. J. Agric. Res. 45:1003-1011. https://doi.org/10.1071/AR9941002 Crossref, Google Scholar
Mares, D. J., and Mrva, K. 2014. Wheat grain preharvest sprouting and late maturity alpha-amylase. Planta 240:1167-1178. https://doi.org/10.1007/s00425-014-2172-5 Crossref, Medline, ISI, Google Scholar
Maul, R., Müller, C., Rieß, S., Koch, M., Methner, F.-J., and Irene, N. 2012. Germination induces the glucosylation of the Fusarium mycotoxin deoxynivalenol in various grains. Food Chem. 131:274-279. https://doi.org/10.1016/j.foodchem.2011.08.077 Crossref, ISI, Google Scholar
McMullen, M., Bergstrom, G., De Wolf, E., Dill-Macky, R., Hershman, D., Shaner, G., and Van Sanford, D. 2012. A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Dis. 96:1712-1728. https://doi.org/10.1094/PDIS-03-12-0291-FE Link, ISI, Google Scholar
McMullen, M., Jones, R., and Gallenberg, D. 1997. Scab of wheat and barley: A re-emerging disease of devastating impact. Plant Dis. 81:1340-1348. https://doi.org/10.1094/PDIS.1997.81.12.1340 Link, ISI, Google Scholar
Moot, D. J., and Every, D. 1990. A comparison of bread baking, falling number, α-amylase assay and visual method for the assessment of pre-harvest sprouting in wheat. J. Cereal Sci. 11:225-234. https://doi.org/10.1016/S0733-5210(09)80166-5 Crossref, ISI, Google Scholar
Moraes, W. B. 2021. Sampling for Fusarium Head Blight (FHB) Index Estimation and Quantifying the Effects of Environmental Conditions on FHB Development, Mycotoxin Contamination of Grain, and their Management in Wheat. The Ohio State University, United States of America. Google Scholar
Moraes, W. B., Madden, L. V., and Paul, P. A. 2022a. Characterizing heterogeneity and determining sample sizes for accurately estimating wheat Fusarium head blight index in research plots. Phytopathology 112:315-334. https://doi.org/10.1094/PHYTO-04-21-0157-R Link, ISI, Google Scholar
Moraes, W. B., Madden, L. V., and Paul, P. A. 2022b. Efficacy of genetic resistance and fungicide application against Fusarium head blight and mycotoxins in wheat under persistent pre- and postanthesis moisture. Plant Dis. 106:2839-2855. https://doi.org/10.1094/PDIS-02-22-0263-RE Link, ISI, Google Scholar
Ovando-Martínez, M., Ozsisli, B., Anderson, J., Whitney, K., Ohm, J.-B., and Simsek, S. 2013. Analysis of deoxynivalenol and deoxynivalenol-3-glucoside in hard red spring wheat inoculated with Fusarium graminearum. Toxins (Basel) 5:2522-2532. https://doi.org/10.3390/toxins5122522 Crossref, Medline, ISI, Google Scholar
Paul, P. A., El-Allaf, S. M., Lipps, P. E., and Madden, L. V. 2005a. Relationships between incidence and severity of Fusarium head blight on winter wheat in Ohio. Phytopathology 95:1049-1060. https://doi.org/10.1094/PHYTO-95-1049 Link, ISI, Google Scholar
Paul, P. A., Lipps, P. E., and Madden, L. V. 2005b. Relationship between visual estimates of Fusarium head blight intensity and deoxynivalenol accumulation in harvested wheat grain: A meta-analysis. Phytopathology 95:1225-1236. https://doi.org/10.1094/PHYTO-95-1225 Link, ISI, Google Scholar
Paul, P. A., Lipps, P. E., and Madden, L. V. 2006. Meta-analysis of regression coefficients for the relationship between Fusarium head blight and deoxynivalenol content of wheat. Phytopathology 96:951-961. https://doi.org/10.1094/PHYTO-96-0951 Link, ISI, Google Scholar
Pestka, J. J. 2010. Deoxynivalenol: Mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 84:663-679. https://doi.org/10.1007/s00204-010-0579-8 Crossref, Medline, ISI, Google Scholar
Poppenberger, B., Berthiller, F., Lucyshyn, D., Sieberer, T., Schuhmacher, R., Krska, R., Kuchler, K., Glössl, J., Luschnig, C., and Adam, G. 2003. Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J. Biol. Chem. 278:47905-47914. https://doi.org/10.1074/jbc.M307552200 Crossref, Medline, ISI, Google Scholar
Proctor, R. H., Hohn, T. M., and McCormick, S. P. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant-Microbe Interact. 8:593-601. https://doi.org/10.1094/MPMI-8-0593 Crossref, Medline, ISI, Google Scholar
Rocha, O., Ansari, K., and Doohan, F. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: A review. Food Addit. Contam. 22:369-378. https://doi.org/10.1080/02652030500058403 Crossref, Medline, ISI, Google Scholar
Rockland, L. B. 1960. Saturated salt solutions for static control of relative humidity between 5° and 40°C. Anal. Chem. 32:1375-1376. https://doi.org/10.1021/ac60166a055 Crossref, ISI, Google Scholar
Salgado, J. D., Lindsey, L. E., and Paul, P. A. 2017. Effects of row spacing and nitrogen rate on wheat grain yield and profitability as influenced by diseases. Plant Dis. 101:1998-2011. https://doi.org/10.1094/PDIS-03-17-0414-RE Link, ISI, Google Scholar
Salgado, J. D., Wallhead, M., Madden, L. V., and Paul, P. A. 2011. Grain harvesting strategies to minimize grain quality losses due to Fusarium head blight in wheat. Plant Dis. 95:1448-1457. https://doi.org/10.1094/PDIS-04-11-0309 Link, ISI, Google Scholar
Schwarz, P. B. 2017. Fusarium head blight and deoxynivalenol in malting and brewing: Successes and future challenges. Trop. Plant Pathol. 42:153-164. https://doi.org/10.1007/s40858-017-0146-4 Crossref, ISI, Google Scholar
Schweiger, W., Boddu, J., Shin, S., Poppenberger, B., Berthiller, F., Lemmens, M., Muehlbauer, G. J., and Adam, G. 2010. Validation of a candidate deoxynivalenol-inactivating UDP-glucosyltransferase from barley by heterologous expression in yeast. Mol. Plant-Microbe Interact. 23:977-986. https://doi.org/10.1094/MPMI-23-7-0977 Link, ISI, Google Scholar
Sewald, N., von Gleissenthall, J. L., Schuster, M., Müller, G., and Aplin, R. T. 1992. Structure elucidation of a plant metabolite of 4-desoxynivalenol. Tetrahedron Asymmetry 3:953-960. https://doi.org/10.1016/S0957-4166(00)82193-X Crossref, Google Scholar
Shaner, G. 2003. Epidemiology of Fusarium head blight of small grain cereals in North America. Pages 84-119 in: Fusarium Head Blight of Wheat and Barley. K. J. Leonard and W. R. Bushnell, eds. American Phytopathological Society, St. Paul, MN. Google Scholar
Shin, S., Torres-Acosta, J. A., Heinen, S. J., McCormick, S., Lemmens, M., Paris, M. P. K., Berthiller, F., Adam, G., and Muehlbauer, G. J. 2012. Transgenic Arabidopsis thaliana expressing a barley UDP-glucosyltransferase exhibit resistance to the mycotoxin deoxynivalenol. J. Exp. Bot. 63:4731-4740. https://doi.org/10.1093/jxb/ers141 Crossref, Medline, ISI, Google Scholar
Siou, D., Gélisse, S., Laval, V., Repinçay, C., Canalès, R., Suffert, F., and Lannou, C. 2014. Effect of wheat spike infection timing on Fusarium head blight development and mycotoxin accumulation. Plant Pathol. 63:390-399. https://doi.org/10.1111/ppa.12106 Crossref, ISI, Google Scholar
Sneller, C., Guttieri, M., Paul, P., Costa, J., and Jackwood, R. 2012. Variation for resistance to kernel infection and toxin accumulation in winter wheat infected with Fusarium graminearum. Phytopathology 102:306-314. https://doi.org/10.1094/PHYTO-05-11-0143 Link, ISI, Google Scholar
Stroup, W. W. 2013. Generalized Linear Mixed Models: Modern Concepts, Methods and Applications. CRC Press, Boca Raton, FL. Google Scholar
Stroup, W. W., Milliken, G. A., Claassen, E. A., and Wolfinger, R. D. 2018. SAS for Mixed Models: Introduction and Basic Applications. SAS Institute Inc., Cary, NC. Google Scholar
Tucker, J. R., Badea, A., Blagden, R., Pleskach, K., Tittlemier, S. A., and Fernando, W. 2019. Deoxynivalenol-3-glucoside content is highly associated with deoxynivalenol levels in two-row barley genotypes of importance to Canadian barley breeding programs. Toxins (Basel) 11:319. https://doi.org/10.3390/toxins11060319 Crossref, Medline, ISI, Google Scholar
Vidal, A., Bendicho, J., Sanchis, V., Ramos, A. J., and Marín, S. 2016. Stability and kinetics of leaching of deoxynivalenol, deoxynivalenol-3-glucoside and ochratoxin A during boiling of wheat spaghettis. Food Res. Int. 85:182-190. https://doi.org/10.1016/j.foodres.2016.04.037 Crossref, Medline, ISI, Google Scholar
Winston, P. W., and Bates, D. H. 1960. Saturated solutions for the control of humidity in biological research. Ecology 41:232-237. https://doi.org/10.2307/1931961 Crossref, ISI, Google Scholar
Wu, F., Groopman, J. D., and Pestka, J. J. 2014. Public health impacts of foodborne mycotoxins. Annu. Rev. Food Sci. Technol. 5:351-372. https://doi.org/10.1146/annurev-food-030713-092431 Crossref, Medline, ISI, Google Scholar

Vol. 113, No. 2
February 2023

ISSN:0031-949X
e-ISSN:1943-7684

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Cassava mosaic-diseased cassava plant in Africa showing severe mosaic and leaf deformation symptoms caused by co-infection with a group of cassava mosaic viruses of the genus Begomovirus in the family Geminiviridae (Tatineni and Hein). Photo credit: O. Alabi

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Article History

Issue Date: 13 Mar 2023
Published: 5 Mar 2023
First Look: 21 Sep 2022
Accepted: 20 Sep 2022

Pages: 206-224

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Funding

U.S. Department of Agriculture–Agricultural Research Service
Grant/Award Number: 59-0206-4-018

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The author(s) declare no conflict of interest.

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