Nitrogen Fertilization Influence on Fusarium and Deoxynivalenol Contamination of Wheat

Abstract

Fusarium head blight (FHB) is the most devastating disease of small cereal grains worldwide caused by several Fusarium species. F. graminearum sensu stricto is the most frequently identified FHB pathogen within the F. graminearum species complex (FGSC). This pathogen produces the mycotoxin deoxynivalenol, which reduces grain quality and poses a threat to human and animal health. In this study, the effect of nitrogen (N) fertilizer rates (0, 50, and 100 kg N ha–1) on the incidence of Fusarium spp., levels of deoxynivalenol (DON), agronomic traits (plant height – PH, spike length – SL, and thousand-grain weight – TGW) and grain yield (GY) in two winter wheat cultivars (Nogal and NS Ilina) over two growing seasons (2016–2017 and 2017–2018) was investigated. Among Fusarium species, FGSC strains were the most frequently isolated in both years. The incidence of FGSC strains (20.22%), DON levels (323.59 µg kg–1), PH (83.21 cm), TGW (38.68 g), and GY (8.88 t ha–1) were higher in 2017 than in 2018 (9.66%, 97.72 µg kg–1, 71.05 cm, 34.35 g, and 5.11 t ha–1, respectively). Cultivar NS Ilina had significantly higher FGSC incidence (20.11%), DON levels (302 µg kg–1 ), PH (85.57 cm), and SL (9.11 cm) than cultivar Nogal (9.77%, 104.71 µg kg–1 , 68.68 cm, and 7.65 cm, respectively). The N rate significantly increased PH, but did not affect the other investigated parameters. Although both wheat cultivars tested were susceptible to Fusarium pathogens and DON, Nogal displayed less susceptibility than NS Ilina. Therefore, adopting integrated disease management that focuses on FHB resistant or less susceptible wheat cultivars can reduce the risk of pathogen presence and DON.

Keywords

• deoxynivalenol
• Fusarium spp.
• nitrogen fertilization
• agronomic traits
• winter wheat

Supporting Institution

The Ministry of Science, Technological Development and Innovation of the Republic of Serbia

Project Number

No. 451-03-136/2025-03/200022, No. 451-03-137/2025-03/200116, No. 451-03-137/2025-03/200383 and No. 451-03-136/2024-03/200040

References

1. Abera, T., Firomsa, T., & Husen, A. (2024). Determining optimal nitrogen level and soil test-based phosphorus calibration study for bread wheat (Triticum aestivum L.) in Dugda District, East Shewa Zone, Oromia, Ethiopia. Cross Current International Journal of Agricultural and Veterinary Sciences, 6(4), 85–92. https://doi.org/10.36344/ccijavs.2024.v06i04.001
2. Akgul, D. S., & Erkilic, A. (2016). Effect of wheat cultivars, fertilizers, and fungicides on Fusarium foot rot disease of wheat. Turkish Journal of Agriculture and Forestry, 40, 101–108. https://doi.org/10.3906/tar-1410-31
3. Alaamer, S. A., Shtewy, N., & Alsharifi, S. K. A. (2024). Wheat response to nitrogen fertilizers in productivity. SABRAO Journal of Breeding and Genetics, 56(6), 2532–2543. https://doi.org/10.54910/sabrao2024.56.6.35
4. Al-Hashimi, A., Aina, O., Daniel, A. I., Du Plessis, M., Keyster, M., & Klein, A. (2025). Critical review on characterization, management, and challenges of fusarium head blight disease in wheat. Physiological and Molecular Plant Pathology, 136, 102557. https://doi.org/10.1016/j.pmpp.2024.102557
5. Andersen, K. F., Madden, L. V., & 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
6. Beccari, G., Hao, G., & Liu, H. (2022). Editorial: Fusarium pathogenesis: Infection mechanisms and disease progression in host plants. Frontiers in Plant Science, 13, 1020404. https://doi.org/10.3389/fpls.2022.1020404
7. Berraies, S., Ruan, I., Knok, R., DePauv, R., Bokore, F., Cuthbert, R., Blackvell, B., Henrikuez, M.A., Konkin, D., Iu, B., Pozniak, C., & Meier, B. (2024). Genetic mapping of deoxynivalenol and fusarium damaged kernel resistance in an adapted durum wheat population. BMC Plant Biology, 24, 183. https://doi.org/10.1186/s12870-023-04708-8
8. Bilska, K., Jurczak, S., Kulik, T., Ropelewska, E., Olszewski, J., Żelechowski, M., & Zapotoczny, P. (2018). Species composition and trichothecene genotype profiling of Fusarium field isolates recovered from wheat in Poland. Toxins, 10(8), 325. https://doi.org/10.3390/toxins10080325

9. Chrpová, J., Grausgruber, H., Weyermann, V., Buerstmayr, M., Palicová, J., Kozová, J., Trávníčková, M., Nguyen, Q. T., Moreno Amores, J. E., Buerstmayr, H., & Janovská, D. (2021). Resistance of winter spelt wheat [Triticum aestivum subsp. spelta (L.) Thell.] to Fusarium head blight. Frontiers in Plant Science, 12, 661484. https://doi.org/10.3389/fpls.2021.661484
10. Covarelli, L., Beccari, G., Prodi, A., Generotti, S., Etruschi, F., Juan, C., Ferrer, E., & Mañes, J. (2015). Fusarium species, chemotype characterisation and trichothecene contamination of durum and soft wheat in an area of central Italy. Journal of the Science and Food and Agriculture, 95, 540–551. https://doi.org/10.1002/jsfa.6772
11. Cowger, C., Patton-Özkurt, J., Brown-Guedira, G., & 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
12. Cuthbert, R. D., DePauw, R. M., Knox, R. E., Singh, A. K., McCaig, T. N., McCallum, B., & Fetch, T. (2017). AAC Brandon hard red spring wheat. Canadian Journal of Plant Science, 97, 393–401. https://doi.org/10.1139/cjps-2016- 0150
13. DePauw, R. M., Knox, R. E., McCaig, T. N., Clarke, F. R., & Clarke, J. M. (2011). Carberry hard red spring wheat. Canadian Journal of Plant Science, 91, 529–534. https://doi.org/10.4141/cjps10187
14. Dordas, C. (2008). Role of nutrients in controlling plant diseases in sustainable agriculture: A review. Agronomy for Sustainable Development, 28(1), 33–46. https://doi.org/10.1051/agro:2007051
15. Dweba, C. C., Figlan, S., Shimelis, H. A., Motaung, T. E., Sydenham, S., Mwadzingeni, L., & Tsilo, T.J. (2017). Fusarium head blight of wheat: Pathogenesis and control strategies. Crop Protection, 91, 114–122. https://doi.org/10.1016/j.cropro.2016.10.002
16. FAO. (2025). Food and Agriculture Organisation of the United Nations. FAOSTAT. http://www.fao.org/faostat/en/#data (April 7, 2025).
17. Foroud, N. A., Baines, D., Gagkaeva, T. Y., Thakor, N., Badea, A., Steiner, B., Bürstmayr, M., & Bürstmayr, H. (2019). Trichothecenes in cereal grains – an update. Toxins, 11(11), 634. https://doi.org/10.3390/toxins11110634
18. El Chami, E., El Chami, J., Tarnawa, Á., Kassai, K.M., Kende, Z., & Jolánkai, K. (2022). Influence of growing season, nitrogen fertilisation and wheat variety on Fusarium infection and mycotoxin production in wheat kernel. Acta Alimentaria, 51, 282–289. https://doi.org/10.1556/066.2022.00036
19. Hammond, G. P., & McCann, N. (2022). Bioethanol processing from wheat straw: investment appraisal of a full-scale UK biofuel refinery. Biofuels, 14(3), 267–277. https://doi.org/10.1080/17597269.2022.2132722
20. Heier, T., Jain, S. K., Kogel, K. H., & Pons-Kühnemann, J. (2005). Influence of N-fertilization and fungicide strategies on Fusarium head blight severity and mycotoxin content in winter wheat. Journal of Phytopathology, 153, 551–557. https://doi.org/10.1111/j.1439-0434.2005.01021.x
21. Jajić, I., Jurić, V., Glamočić, D., & Abramović, B. (2008). Occurrence of deoxynivalenol in maize and wheat in Serbia. International Journal of Molecular Science, 9(11), 2114-2126. http://doi.org/10.3390/ijms9112114
22. Jevtić, R., Župunski, V., Lalošević, M., & Tančić Živanov S. (2019). Colonization of winter wheat grain with Fusarium and Alternaria species and influence on pest control management. Journal of General Plant Pathology, 85, 273–281. https://doi.org/10.1007/s10327-019-00844-y
23. Jevtić, R., Skenderović, N., Župunski, V., Lalošević, M., Orbović, B., & Maširević, S. (2022). The relationship between Fusarium head blight traits, thousand-kernel weight, and yield in winter wheat. Scientia Agricola, 79(3), e20200046. http://doi.org/10.1590/1678-992X-2020-0046
24. Jiménez-Rosado, M., Zarate-Ramírez, L. S., Romero, A., Bengoechea, C., Partal, P., & Guerrero, A. (2019). Bioplastics based on wheat gluten processed by extrusion. Journal of Cleaner Production, 239, 117994. https://doi.org/10.1016/j.jclepro.2019.117994
25. Khalid, A., Hameed, A., & Tahir, M. F. (2023). Wheat quality: A review on chemical composition, nutritional attributes, grain anatomy, types, classification, and function of seed storage proteins in bread making quality. Frontiers in Nutrition, 10, 1053196. https://doi.org/10.3389/fnut.2023.1053196
26. Kim, K. H., & Kim, J. Y. (2021). Understanding wheat starch metabolism in properties, environmental stress condition, and molecular approaches for value-added utilization. Plants, 10(11) 2282. https://doi.org/10.3390/plants10112282
27. Krnjaja, V., Mandić, V., Lević, J., Stanković, S., Petrović, T., Vasić, T., & Obradović, A. (2015). Influence of Nfertilization on Fusarium head blight and mycotoxin levels in winter wheat. Crop Protection, 67, 251–256. https://doi.org/10.1016/j.cropro.2014.11.001
28. Krnjaja, V., Stanković, S., Obradović, A., Petrović, T., Mandić, V., Bijelić, & Z., Božić, M. (2018). Trichothecene genotypes of Fusarium graminearum populations isolated from winter wheat crops in Serbia. Toxins, 10(11), 460. https://doi.org/103390/toxins10110460
29. Krnjaja, V. S., Stanković, S. Ž., Obradović, A. M., Nikolić, M. V., Savić, I. J., Mandić, V. T., & Bijelić, Z. D. (2022). Contamination of durum wheat lines kernels with Fusarium species and deoxynivalenol. Matica Srpska Journal of Natural Science, 143, 27–38. https://doi.org/10.2298/ZMSPN2243027K
30. Landschoot, S., Audenaert, K., Waegeman, W., De Baets, B., & Haesaert, G. (2013). Influence of maize–wheat rotation systems on Fusarium head blight infection and deoxynivalenol content in wheat under low versus high disease pressure. Crop Protection, 52, 14–21. https://doi.org/10.1016/j.cropro.2013.04.013
31. Lemmens, M., Haim, K., Lew, H., & Ruckenbauer, P. (2004). The effect of nitrogen fertilization on Fusarium head blight development and deoxynivalenol contamination in wheat. Journal of Phytopathology, 152, 1–8. https://doi.org/10.1046/j.1439-0434.2003.00791.x
32. Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual. Blackwell Publishing Professional, Ames, Iowa, USA.
33. Leslie, J. F., Moretti, A., Mesterházy, Á., Ameye, M., Audenaert, K., Singh, P. K., Richard-Forget, F., Chulze, S. N., Del Ponte, E. M., Chala, A., et al. (2021). Key global actions for mycotoxin management in wheat and other small grains. Toxins, 13, 725. https://doi.org/10.3390/toxins13100725
34. Litke, L., Gaile, Z., & Ruža, A. (2018). Effect of nitrogen fertilization on winter wheat yield and yield quality. Agronomy Research, 16(2), 500–509. https://doi.org/10.15159/AR.18.064
35. Luo, C., Guo, Z., Xiao, J., Dong, K., & Dong, Y. (2021). Effects of applied ratio of nitrogen on the light environment in the canopy and growth, development and yield of wheat when intercropped. Frontiers in Plant Science, 12, 719850. https://doi.org/10.3389/fpls.2021.719850
36. Ma, B. L., Yan, W., Dwyer, L. M., Fregeau-Reid, J., Voldeng, H. D., Dion, Y., & Nass, H. (2004). Graphic analysis of genotype, environment, nitrogen fertilizer, and their interactions on spring wheat yield. Agronomy Journal, 96(1), 169– 180. https://doi.org/10.2134/agronj2004.1690
37. McMullen, M., Bergstrom, G., De Wolf, E., Dill-Macky, R., Hershman, D., Shaner, G., & van Sanford, D. (2012). A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Disease, 96, 1712–1728. https://doi.org/10.1094/PDIS-03-12-0291-FE
38. Mesterházy, A. (1995). Types and components of resistance to Fusarium head blight of wheat. Plant Breeding, 114, 377– 386. https://doi.org/10.1111/j.1439-0523.1995.tb00816.x
39. Miedaner, T, Gwiazdowska, D., & Waśkiewicz, A. (2017). Editorial: management of Fusarium species and their mycotoxins in cereal food and feed. Frontiers in Microbiology, 8, 1543. https://doi.org/10.3389/fmicb.2017.01543
40. Miedaner, T., Lenhardt, M., Grehl, J., Gruner, P., & Koch, S. (2022). Dwarfing gene Rht24 does not affect Fusarium head blight resistance in a large European winter wheat diversity panel. Euphytica, 218(6), 73. https://doi.org/10.1007/s10681-022-03028-6
41. Miedaner, T., Flamm, C., & Oberforster, M. (2024). The importance of Fusarium head blight resistance in the cereal breeding industry: Case studies from Germany and Austria. Plant Breeding, 143, 44–58. https://doi.org/10.1111/pbr.13098
42. Mitura, K., Cacak-Pietrzak, G., Feledyn-Szewczyk, B., Szablewski, T., & Studnicki, M. (2023). Yield and grain quality of common wheat (Triticum aestivum L.) depending on the different farming systems (organic vs. integrated vs. conventional). Plants, 12(5), 1022. https://doi.org/10.3390/plants12051022
43. Nguyen, T. B. H., Henri-Sanvoisin, A., Coton, M., Le Floch, G., & Picot, A. (2024). Shifts in Fusarium communities and mycotoxins in maize residues, soils, and wheat grains throughout the wheat cycle: implications for Fusarium head blight epidemiology. Microorganisms, 12(9), 1783. https://doi.org/10.3390/microorganisms12091783
44. Obradović, A., Stepanović, J., Bulajić, A., Hrustić, J., Stanković, G., Krnjaja, V., & Stanković, S. (2025). Characterization of Fusarium graminearum and Fusarium vorosii originated from small cereals grain in Serbia. Scientia Agricola, 82, e20230149. https://doi.org/10.1590/1678-992X-2023-0149
45. Okorski, A., Milewska, A., Pszczółkowska, A., Karpiesiuk, K., Kozera,W., Dąbrowska, J. A., & Radwińska, J. (2022). Prevalence of Fusarium fungi and deoxynivalenol levels in winter wheat grain in different climatic regions of Poland. Toxins, 14, 102. https://doi.org/10.3390/toxins14020102
46. Oldenburg, E., Bramm, A., & Valenta, H. (2007). Influence of nitrogen fertilization on deoxynivalenol contamination of winter wheat – Experimental field trials and evaluation of analytical methods. Mycotoxin Research, 23(1), 7–12. https://doi.org/10.1007/BF02946018
47. Palazzini, J. M., Ramirez, M. L., Torres, A. M., & Chulze, S. N. (2007). Potential biocontrol agents for Fusarium head blight and deoxynivalenol production in wheat. Crop Protection, 26(11), 1702–1710. https://doi.org/10.1016/j.cropro.2007.03.004.
48. Palazzini, J., Fumero, V., Yerkovich, N., Barros, G., Cuniberti, M., & Chulze, S. (2015). Correlation between Fusarium graminearum and deoxynivalenol during the 2012/13 wheat Fusarium head blight outbreak in Argentina. Cereal Research Communications, 43(3), 341–348. https://doi.org/10.1556/0806.43.2015.017
49. Pestka, J. J. (2010). Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Archives of Toxicology, 84(9), 663-679. https://doi.org/10.1007/s00204-010-0579-8
50. Podolska, G., Bryła, M., Sułek, A., Waśkiewicz, A., Szymczyk, K., & Jędrzejczak, R. (2017). Influence of the cultivar and nitrogen fertilisation level on the mycotoxin contamination in winter wheat. Quality Assurance and Safety of Crops and Foods, 9, 451–461. https://doi.org/10.3920/QAS2016.1064
51. Salgado, J., Lindsei, L., & Paul, P. (2017). Effects of row spacing and nitrogen rate on wheat grain yield and profitability as influenced by disease. Plant Disease, 101, 1998–2001. https://doi.org/10.1094/PDIS-03-17-0414-RE
52. Shah, L., Ali, A., Yahya, M., Zhu, Y., Wang, S., Si, H., Rahman, H., & Ma, C. (2018). Integrated control of fusarium head blight and deoxynivalenol mycotoxin in wheat. Plant Pathology, 67, 532–548. https://doi.org/10.1111/ppa.12785
53. Tabak, M., Lepiarczyk, A., Filipek-Mazur, B., & Lisowska, A. (2020). Efficiency of nitrogen fertilization of winter wheat depending on sulfur fertilization. Agronomy, 10(9), 1304. https://doi.org/10.3390/agronomy10091304
54. Tekauz, A., McCallum, B., & Gilbert, J. (2000). Review: Fusarium head blight of barley in western Canada. Canadian Journal of Plant Pathology, 22(1), 9-16. https://doi.org/10.1080/07060660009501156
55. Tian, Y., Tan, Y., Liu, N., Liao, Y., Sun, C., Wang, S., & Wu, A. (2016). Functional agents to biologically control deoxynivalenol contamination in cereal grains. Frontiers in Microbiology, 7, 395. https://doi.org/10.3389/fmicb.2016.00395
56. Ullah, I., Ali, N., Durrani, S., Shabaz, M. A., Hafeez, A., Ameer, H., Ishfaq, M., Fayyaz, M. R., Rehman, A., & Waheed, A. (2018). Effect of different nitrogen levels on growth, yield and yield contributing attributes of wheat. International Journal of Scientific & Engineering Research, 9(9), 595. https://doi.org/10.14299/ijser.2018.09.01
57. Van der Burgt, G. J. H. M., Timmermans, B. G. H., Scholberg, J. M. S., & Osman, A. M. (2011). Fusarium head blight and deoxynivalenol contamination in wheat as affected by nitrogen fertilization. NJAS: Wageningen Journal of Life Sciences, 58(3–4), 123–129. https://doi.org/10.1016/j.njas.2011.09.005
58. Van Grinsven, H. J. M., Ebanyat, P., Glendining, M., Gu, B., Hijebeeks, R., Lam S. K., Lassaletta L., Mueller, N. D., Pacheo, F. S., Quemada, M., Bruulsema, T. W., Jacobsen, B. H., & ten Berge, H. F. M. (2022). Establishing long-term nitrogen response of global cereals to assess sustainable fertilizer rates. Nature Food, 3, 122– 132.https://doi.org/10.1038/s43016-021-00447-x
59. Wegulo, S. N., Bockus, W. W., Hernandez Nopsa, J., De Wolf, E. D., Eskridge, K. M., Peiris, K. H. S., & Dowell, F. E. (2011). Effects of integrating cultivar resistance and fungicide application on Fusarium head blight and deoxynivalenol in winter wheat. Plant Disease, 95, 554–560. https://doi.org/10.1094/PDIS-07-10-0495
60. Wegulo, S. N. (2012). Factors influencing deoxynivalenol accumulation in small grain cereals. Toxins, 4, 1157–1180. https://doi.org/10.3390/toxins4111157
61. Yoshida, M., T. Nakajima, & Tonooka, T. (2008). Effect of nitrogen application at anthesis on Fusarium head blight and mycotoxin accumulation in breadmaking wheat in the western part of Japan. Journal of General Plant Pathology, 74, 355–363. https://doi.org/10.1007/s10327-008-0109-1
62. Younis, M., Hussain, S., Albadrani, G. M., Alwutayd, K., Wang, J., Jabeen, S., Ali, S., Yavas, I., & Hussain, S. (2023). Evaluation of wheat with different coated controlled-release urea and application times in semi-arid conditions. Turkish Journal of Field Crops, 28(2), 147–155. https://doi.org/10.17557/tjfc.1291613
63. Zheng, J. C., Zhang, H., Yu, J., Zhan, Q. W., Li, W. Y., Xu, F., Wang, G. J., Liu, T., & Li, J. C. (2021). Late sowing and nitrogen application to optimize canopy structure and grain yield of bread wheat in a fluctuating climate. Turkish Journal of Field Crops, 26(2), 170–179. https://doi.org/10.17557/tjfc.1036633
64. Župunski, V., Jevtić, R, Lalošević, M., Jocković, B., Župunski, LJ., & Skenderović, N. (2021). Effect of cultivation practices on diversity in susceptibility reactions of winter genotypes to Fusarium head blight. European Journal of Agronomy, 125, 126250. https://doi.org/10.1016/j.eja.2021.126250.