The effect of biological control on mycotoxin concentrations and the mycobiome in durum wheat grain and stems

Posted on
the-effect-of-biological-control-on-mycotoxin-concentrations-and-the-mycobiome-in-durum-wheat-grain-and-stems
The effect of biological control on mycotoxin concentrations and the mycobiome in durum wheat grain and stems

References

  1. Beccari, G. et al. Causal agents of Fusarium head blight of durum wheat (Triticum durum Desf,) in central Italy and their in vitro biosynthesis of secondary metabolites. Food Microbiol. 70, 17–27. https://doi.org/10.1016/j.fm.2017.08.016 (2018).

    Google Scholar 

  2. Grosse-Heilmann, M., Cristiano, E., Deidda, R. & Viola, F. Durum wheat productivity today and tomorrow: A review of influencing factors and climate change effects. Resour. Environ. Sustain. 100170 https://doi.org/10.1016/j.resenv.2024.100170 (2024).

  3. Gorczyca, A. et al. 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 (2018).

    Google Scholar 

  4. Viviani, A. et al. Priority actions for Fusarium head blight resistance in durum wheat: Insights from the wheat initiative. Plant. Genome. 18, e20539. https://doi.org/10.1002/tpg2.20539 (2025).

    Google Scholar 

  5. Chiotta, M. L. et al. Fusarium graminearum species complex occurrence on soybean and F. graminearum sensu stricto inoculum maintenance on residues in soybean-wheat rotation under field conditions. J. Appl. Microbiol. 130, 208–216. https://doi.org/10.1111/jam.14765 (2021).

    Google Scholar 

  6. Senatore, M. T. et al. Different diagnostic approaches for the characterization of the fungal community and Fusarium species complex composition of Italian durum wheat grain and correlation with secondary metabolite accumulation. J. Sci. Food. Agric. 103, 4503–4521. https://doi.org/10.1002/jsfa.12526 (2023).

    Google Scholar 

  7. Ji, F. et al. Occurrence, toxicity, production and detection of Fusarium mycotoxin: a review. Food Prod. Process. Nutr. 1 (6). https://doi.org/10.1186/s43014-019-0007-2 (2019).

  8. McCormick, S. P., Alexander, N. J. & Proctor, R. H. Trichothecene triangle: Toxins, genes, and plant disease. In (Ed. Gang, D.) Phytochemicals, plant growth, and the environment. Recent advances in phytochemistry (Vol. 42, pp. 1–17). Springer. (2013). https://doi.org/10.1007/978-1-4614-4066-6_1

  9. Hill, R., Buggs, R. J., Vu, D. T. & Gaya, E. Lifestyle transitions in fusarioid fungi are frequent and lack clear genomic signatures. Mol. Biol. Evol. 39, msac085. https://doi.org/10.1093/molbev/msac085 (2022).

    Google Scholar 

  10. Alisaac, E. & Mahlein, A. K. Fusarium head blight on wheat: Biology, modern detection and diagnosis and integrated disease management. Toxins 15, 192. https://doi.org/10.3390/toxins15030192 (2023).

    Google Scholar 

  11. Haile, J. K. et al. Fusarium head blight in durum wheat: Recent status, breeding directions, and future research prospects. Phytopathology 109, 1664–1675. https://doi.org/10.1094/PHYTO-03-19-0095-RVW (2019).

    Google Scholar 

  12. Scarpino, V. & Blandino, M. Effects of durum wheat cultivars with different degrees of FHB susceptibility grown under different meteorological conditions on the contamination of regulated, modified and emerging mycotoxins. Microorganisms 9, 408. https://doi.org/10.3390/microorganisms9020408 (2021).

    Google Scholar 

  13. Sweany, R. R. et al. Why do plant-pathogenic fungi produce mycotoxins? Potential roles toxins in the plant ecosystem. Phytopathology 112, 2044–2051. https://doi.org/10.1094/PHYTO-02-22-0053-SYM (2022).

    Google Scholar 

  14. Covarelli, L. et al. Fusarium species, chemotype characterisation and trichothecene contamination of durum and soft wheat in an area of central Italy. J. Sci. Food. Agric. 95, 540–551. https://doi.org/10.1002/jsfa.6772 (2015).

    Google Scholar 

  15. Crippin, T., Renaud, J. B., Sumarah, M. W. & Miller, J. D. Comparing genotype and chemotype of Fusarium graminearum from cereals in Ontario, Canada. PLoS ONE 14, e0216735. (2019). https://doi.org/10.1371/journal.pone.0216735

  16. Foroud, N. A. et al. Trichothecenes in cereal grains – An update. Toxins 11, 634. https://doi.org/10.3390/toxins11110634 (2019).

    Google Scholar 

  17. Kelly, A. C. & Ward, T. J. Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen. PLoS ONE. 13, e0194616. https://doi.org/10.1371/journal.pone.0194616 (2018).

    Google Scholar 

  18. Commission Regulation (EU). 2024/1022 of 8 April 2024 amending Regulation (EU) 2023/915 as regards maximum levels of deoxynivalenol in food. https://eur-lex.europa.eu/eli/reg/2024/1022/oj/eng

  19. Commission Recommendation (EU). 2013/165 of 27 March 2013 on the presence of T-2 and HT-2 toxin in cereals and cereal products. https://www.stradalex.eu/en/se_src_publ_leg_eur_jo/document/ojeu_2013.091.01.0012.01

  20. Wachowska, U. & Rychcik, B. Plants control the structure of mycorrhizal and pathogenic fungal communities in soil in a 50-year maize monoculture experiment. Plant. Soil. 484, 133–153. https://doi.org/10.1007/s11104-022-05779-6 (2023).

    Google Scholar 

  21. Zaied, C., Zouaoui, N., Bacha, H. & Abid, S. Natural occurrence of zearalenone in Tunisian wheat grains. Food Control. 25, 773–777. https://doi.org/10.1016/j.foodcont.2011.12.012 (2012).

    Google Scholar 

  22. Falkauskas, R. et al. Zearalenone and Its Metabolites in Blood Serum, Urine, and Milk of Dairy Cows. Animals 12, 1651. (2022). https://doi.org/10.3390/ani12131651

  23. Gruber-Dorninger, C., Novak, B., Nagl, V. & Berthiller, F. Emerging mycotoxins: beyond traditionally determined food contaminants. J. Agric. Food Chem. 65, 7052–7070. https://doi.org/10.1021/acs.jafc.6b03413 (2017).

    Google Scholar 

  24. Cipollone, M. J., Moya, P., Martínez, I., Saparrat, M. & Sisterna, M. Grain discoloration in different genotypes of durum wheat (Triticum durum L.) in Argentina: associated mycobiota and peroxidase activity. J. Plant. Prot. Res. 60, 14–20. https://doi.org/10.24425/jppr.2020.132200 (2020).

    Google Scholar 

  25. Masiello, M. et al. Molecular identification and mycotoxin production by Alternaria species occurring on durum wheat, showing black point symptoms. Toxins 12, 275. https://doi.org/10.3390/toxins12040275 (2020).

    Google Scholar 

  26. Daichi, M. B. et al. Assessing Alternaria species and related mycotoxin contamination in wheat in Algeria: A food safety risk. Toxins (Basel). 17309. https://doi.org/10.3390/toxins17060309 (2025).

  27. Jarolim, K. et al. Activation of the Nrf2-ARE pathway by the Alternaria alternata mycotoxins altertoxin I and II. Arch. Toxicol. 91, 203–216. https://doi.org/10.1007/s00204-016-1726-7 (2017).

    Google Scholar 

  28. Brugger, E. M. et al. Mutagenicity of the mycotoxin alternariol in cultured mammalian cells. Toxicol. Lett. 164, 221–230. https://doi.org/10.1016/j.toxlet.2006.01.001 (2006).

    Google Scholar 

  29. Ostry, V. Alternaria mycotoxins: an overview of chemical characterization, producers, toxicity, analysis and occurrence in foodstuffs. World Mycotoxin J. 1, 175–188. https://doi.org/10.3920/WMJ2008.x013 (2008).

    Google Scholar 

  30. Schmutz, C., Cenk, E. & Marko, D. The Alternaria mycotoxin alternariol triggers the immune response of il-1β‐stimulated, differentiated caco‐2 cells. Mol. Nutr. Food Res. 63, 1900341. https://doi.org/10.1002/mnfr.201900341 (2019).

    Google Scholar 

  31. Fleck, S. C., Burkhardt, B., Pfeiffer, E. & Metzler, M. Alternaria toxins: Altertoxin II is a much stronger mutagen and DNA strand breaking mycotoxin than alternariol and its methyl ether in cultured mammalian cells. Toxicol. Lett. 214, 27–32. https://doi.org/10.1016/j.toxlet.2012.08.003 (2012).

    Google Scholar 

  32. Abbas, H. K. & Riley, R. T. The presence and phytotoxicity of fumonisins and AAL-toxin in Alternaria alternata. Toxicon 34, 133–136. https://doi.org/10.1016/0041-0101(95)00124-7 (1996).

    Google Scholar 

  33. Haidukowski, M. et al. Deoxynivalenol and T-2 toxin as major concerns in durum wheat from Italy. Toxins 14, 627. https://doi.org/10.3390/toxins14090627 (2022).

    Google Scholar 

  34. Solanki, M. K. et al. Analysis of stored wheat grain-associated microbiota reveals biocontrol activity among microorganisms against mycotoxigenic fungi. J. Fungi. 7, 781. https://doi.org/10.3390/jof7090781 (2021).

    Google Scholar 

  35. Wachowska, U., Głowacka, K., Mikołajczyk, W. & Kucharska, K. Biofilm of Aureobasidium pullulans var. pullulans on winter wheat kernels and its effect on other microorganisms. Microbiology 85, 523–530. https://doi.org/10.1134/S0026261716050192 (2016).

    Google Scholar 

  36. Abdel-Kareem, M. M., Zohri, A. N. A. & Nasr, S. A. E. E. Novel marine yeast strains as plant growth-promoting agents improve defense in wheat (Triticum aestivum) against Fusarium oxysporum. J. Plant Dis. Prot. 128, 973–988. https://doi.org/10.1007/s41348-021-00461-y (2021).

    Google Scholar 

  37. Wachowska, U., Stuper-Szablewska, K. & Perkowski, J. Yeasts isolated from wheat grain can suppress Fusarium head blight and decrease trichothecene concentrations in bread wheat and durum wheat grain. Pol. J. Environ. Stud. 29, 4345–4360. https://doi.org/10.15244/pjoes/118427 (2020).

    Google Scholar 

  38. Chi, Z., Wang, X. X., Ma, Z. C., Buzdar, M. A. & Chi, Z. M. The unique role of siderophore in marine-derived Aureobasidium pullulans HN6. 2. Biometals 25, 219–230. (2012). https://doi.org/10.1007/s10534-011-9499-1

  39. Böswald, C., Engelhardt, G., Vogel, H. & Wallnöfer, P. R. Metabolism of the Fusarium mycotoxins zearalenone and deoxynivalenol by yeast strains of technological relevance. Nat. Toxins. 3, 138–144. https://doi.org/10.1002/nt.2620030304 (1995).

    Google Scholar 

  40. Illueca, F. et al. Antifungal activity of biocontrol agents in vitro and potential application to reduce mycotoxins (aflatoxin B1 and ochratoxin A). Toxins 13, 752. https://doi.org/10.3390/toxins13110752 (2021).

    Google Scholar 

  41. Papp, L. A., Horváth, E., Peles, F., Pócsi, I. & Miklós, I. Insight into yeast–mycotoxin relations. Agriculture 11, 1291. https://doi.org/10.3390/agriculture11121291 (2021).

    Google Scholar 

  42. Vanhoutte, I., Audenaert, K. & De Gelder, L. Biodegradation of mycotoxins: Tales from known and unexplored worlds. Front. Microbiol. 7, 561. https://doi.org/10.3389/fmicb.2016.00561 (2016).

    Google Scholar 

  43. Giedrojć, W. & Wachowska, U. Mycobiome and pathogenic Fusarium fungi in the rhizosphere of durum wheat after seed dressing with Debaryomyces hansenii. Agriculture 15, 639. https://doi.org/10.3390/agriculture15060639 (2025).

    Google Scholar 

  44. Meier, U. Phenological Growth Stages. In Phenology: An Integrative Environmental Science. (Ed. Schwartz, M.D.) Tasks for Vegetation Science. Springer: Dordrecht, The Netherlands, p. 39. (2003).

  45. Gams, W. in Cephalosporium-Artige Schimmelpilze (Hyphomycetes). (eds Fischer, G.) (Taylor & Francis, Ltd., 1971).

  46. Leslie, J. F. & Summerell, B. A. The Fusarium Laboratory Manual (Blackwell Publishing Professional, 2006).

  47. Statistica (Data Analysis. Software System) version 13 (TIBCO Software Inc, 2017).

  48. Rojas, E. C. et al. Selection of fungal endophytes with biocontrol potential against Fusarium head blight in wheat. Biol. Control. 144, 104222. https://doi.org/10.1016/j.biocontrol.2020.104222 (2020).

    Google Scholar 

  49. Bamforth, J. et al. A survey of Fusarium species and ADON genotype on Canadian wheat grain. Front. Fungal Biology. 3, 1062444. https://doi.org/10.3389/ffunb.2022.1062444 (2022).

    Google Scholar 

  50. Varga, E. et al. New tricks of an old enemy: isolates of Fusarium graminearum produce a type A trichothecene mycotoxin. Environ. Microbiol. 17, 2588–2600. https://doi.org/10.1111/1462-2920.12718 (2015).

    Google Scholar 

  51. Wachowska, U. et al. Secondary metabolites of pathogenic fungi in Triticum durum grain protected with Debaryomyces hansenii in two different locations in Poland. Agronomy 13, 721. https://doi.org/10.3390/agronomy13030721 (2023).

    Google Scholar 

  52. Bertuzzi, T. et al. Co-occurrence of moniliformin and regulated Fusarium toxins in maize and wheat grown in Italy. Molecules 25, 2440. https://doi.org/10.3390/molecules25102440 (2020).

    Google Scholar 

  53. Perellò, A., Moreno, M. & Sisterna, M. Alternaria infectoria species-group associated with black point of wheat in Argentina. Plant. Pathol. 57, 379. https://doi.org/10.1111/j.1365-3059.2007.01713.x (2008).

    Google Scholar 

  54. Somma, S., Amatulli., M. T., Masiello, M., Moretti, A. & Logrieco, A. F. Alternaria species associated to wheat black point identified through a multilocus sequence approach. Int. J. Food Microbiol. 293, 34–43. https://doi.org/10.1016/j.ijfoodmicro.2019.01.001 (2019).

    Google Scholar 

  55. Pero, R. W., Posner, H., Blois, M., Harvan, D. & Spalding, J. W. Toxicity of metabolites produced by the Alternaria. Environ. Health Perspect. 4, 87–94. https://doi.org/10.1289/ehp.730487 (1973).

    Google Scholar 

  56. Aamot, H. U. et al. Microdochium majus and other fungal pathogens associated with reduced gluten quality in wheat grain. Int. J. Food Microbiol. 331, 108712. https://doi.org/10.1016/j.ijfoodmicro.2020.108712 (2020).

    Google Scholar 

  57. Xu, X. M. et al. Relationship between the fungal complex causing Fusarium head blight of wheat and environmental conditions. Phytopathology 98, 69–78. https://doi.org/10.1094/PHYTO-98-1-0069 (2008).

    Google Scholar 

  58. Balendres, M. A. et al. Epicoccum. In: (eds Amaresan, N. & Kumar, K.) Compendium of Phytopathogenic Microbes in Agro-Ecology. Springer, Cham. https://doi.org/10.1007/978-3-031-81770-0_13 (2025).

    Google Scholar 

  59. Jensen, B. D., Knorr, K. & Nicolaisen, M. In vitro competition between Fusarium graminearum and Epicoccum nigrum on media and wheat grains. Eur. J. Plant Pathol. 146, 657–670. https://doi.org/10.1007/s10658-016-0950-6 (2016).

    Google Scholar 

  60. Nzabanita, C., Zhang, L., Wang, Y., Wang, S. & Guo, L. The wheat endophyte Epicoccum layuense J4-3 inhibits Fusarium graminearum and enhances plant growth. J. Fungi. 10, 10. https://doi.org/10.3390/jof10010010 (2023).

    Google Scholar 

  61. Alfonzo, A., Sicard, D., Di Miceli, G., Guezenec, S. & Settanni, L. Ecology of yeasts associated with kernels of several durum wheat genotypes and their role in co-culture with Saccharomyces cerevisiae during dough leavening. Food Microbiol. 94, 103666. https://doi.org/10.1016/j.fm.2020.103666 (2021).

    Google Scholar 

  62. Shude, S. P. N., Mbili, N. C. & Yobo, K. S. Epiphytic yeasts as potential antagonists against Fusarium head blight of wheat (Triticum aestivum L.) caused by Fusarium graminearum sensu stricto. J. Saudi Soc. Agricultural Sci. 21, 404–411. https://doi.org/10.1016/j.jssas.2021.11.001 (2022).

    Google Scholar 

  63. Wachowska, U. et al. The application of antagonistic yeasts and bacteria: An assessment of in vivo and under field conditions pattern of Fusarium mycotoxins in winter wheat grain. Food Control. 138, 109039. https://doi.org/10.1016/j.foodcont.2022.109039 (2022).

    Google Scholar 

  64. Palazzini, J. et al. Biocontrol of Fusarium graminearum sensu stricto, reduction of deoxynivalenol accumulation and phytohormone induction by two selected antagonists. Toxins 10, 88. https://doi.org/10.3390/toxins10020088 (2018).

    Google Scholar 

  65. Sherif, M., Kirsch, N., Splivallo, R., Pfohl, K. & Karlovsky, P. The role of mycotoxins in interactions between Fusarium graminearum and F. verticillioides growing in saprophytic cultures and co-infecting maize plants. Toxins 15, 575. https://doi.org/10.3390/toxins15090575 (2023).

    Google Scholar 

  66. Cooney, J. M., Lauren, D. R. & di Menna, M. E. Impact of competitive fungi on trichothecene production by Fusarium graminearum. J. Agric. Food Chem. 49, 522–526. https://doi.org/10.1021/jf0006372 (2001).

    Google Scholar 

  67. Boeira, L. S., Bryce, J. H., Stewart, G. G. & Flannigan, B. The effect of combinations of Fusarium mycotoxins (deoxynivalenol, zearalenone and fumonisin B1) on growth of brewing yeasts. J. Appl. Microbiol. 88, 388–403. https://doi.org/10.1046/j.1365-2672.2000.00972.x (2000).

    Google Scholar 

  68. Whitehead, M. P. & Flannigan, B. The Fusarium mycotoxin deoxynivalenol and yeast growth and fermentation. J. Inst. Brew. 95, 411–413. https://doi.org/10.1002/j.2050-0416.1989.tb04646.x (1989).

    Google Scholar 

  69. Wall-Martínez, H. A. et al. The fate of Fusarium mycotoxins (deoxynivalenol and zearalenone) through wort fermenting by Saccharomyces yeasts (S. cerevisiae and S. pastorianus). Food Res. Int. 126, 108587. https://doi.org/10.1016/j.foodres.2019.108587 (2019).

    Google Scholar 

  70. Tillmann, M., von Tiedemann, A. & Winter, M. Crop rotation effects on incidence and diversity of Fusarium species colonizing stem bases and grains of winter wheat. J. Plant Dis. Prot. 124, 121–130 (2017).

    Google Scholar 

  71. Vujanovic, V., Mavragani, D. & Hamel, Ch.  Fungal communities associated with durum wheat production system: A characterization by growth stage plant organ and preceding crop, Crop Prot 37, 26-34. https://doi.org/10.1016/j.cropro.2012.02.006 (2012).

    Google Scholar 

  72. Seybold, H. et al. A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition. Nat. Commun. 11, 1910. https://doi.org/10.1038/s41467-020-15633-x (2020).

  73. Adamik, L. et al. Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses. Sci. Rep. 15, 11773. https://doi.org/10.1038/s41598-025-96159-4 (2025).

  74. Marburger, D.A. et al. Crop rotation and management effect on Fusarium spp. populations. Crop Sci. 55, 365-376. https://doi.org/10.2135/cropsci2014.03.0199 (2015)

  75. Karlsson, I., Persson, P. & Friberg, H. Fusarium head blight from a microbiome perspective. Front. Microbiol. 12, 628373. https://doi.org/10.3389/fmicb.2021.628373 (2021)

  76. Grudzinska-Sterno, M., Yuen, J., Stenlid, J. & Djurle, A. Fungal communities in organically grown winter wheat affected by plant organ and development stage. Eur. J. Plant Pathol. 146, 1–17. https://doi.org/10.1007/s10658-016-0927-5 (2016).

Download references

Related Posts