Vol. 63 No. 2 (2024)
Articles

Fusarium species and assessments of mycotoxin (deoxynivalenol), in wheat seeds from different regions of Türkiye

Kubra SARACOGLU
Department of Agricultural and Food Sciences (DISTAL), University of Bologna, 40126, Bologna, Italy
Greice Amaral CARNEIRO
Department of Agricultural and Food Sciences (DISTAL), University of Bologna, 40126, Bologna, Italy
Eleonora CAPPELLETTI
Department of Agricultural and Food Sciences (DISTAL), University of Bologna, 40126, Bologna, Italy
Fatma Sara DOLAR
Ankara University, Faculty of Agriculture, Department of Plant Protection, 06120 Ankara
Antonio PRODI
Department of Agricultural and Food Sciences (DISTAL), University of Bologna, 40126, Bologna, Italy

Published 2024-09-16

Keywords

  • Species complex,
  • DON,
  • wheat kernels,
  • molecular characterisation,
  • phylogenetic analyses

How to Cite

[1]
K. SARACOGLU, G. A. CARNEIRO, E. CAPPELLETTI, F. S. DOLAR, and A. PRODI, “Fusarium species and assessments of mycotoxin (deoxynivalenol), in wheat seeds from different regions of Türkiye”, Phytopathol. Mediterr., vol. 63, no. 2, pp. 233–253, Sep. 2024.

Abstract

Wheat cultivation is important in Turkish agriculture, which ranks 10th among international wheat producers, and is an important wheat exporter, particularly to Europe. Fusarium-related threats, such as Fusarium Head Blight (FHB) and Fusarium Crown and Root Rots (FCR, FRR), and related mycotoxin seed contamination, jeopardize product quality. This study analysed 65 wheat seed samples for presence of Fusarium species, from cultivars of Triticum aestivum (bread wheat) and T. durum (durum wheat) collected from seven regions of Türkiye. PCR with specific primers, and phylogenetic analyses of TEF1-α segments, discriminated Fusarium species. Levels of the mycotoxin deoxynivalenol (DON) in flour samples were also evaluated. Out of 195 Fusarium isolates, the prominent species included F. graminearum (32% of isolates), F. proliferatum (16%), F. avenaceum (11%), F. clavum (11%), and F. verticillioides (7%). Less frequently isolated species were F. oxysporum (6%), F. acuminatum (3%), F. ramigenum (3%), F. culmorum (3%), F. poae (2%), F. sambucinum (2%), F. tricinctum (2%), Fusarium sp. FTSC12 (2%), F. andiyazi (1%), and F. equiseti, F. incarnatum, and F. fasciculatum (each 0.5%). Five of the 65 samples tested positive for DON, with two exceeding the European Commission threshold for mycotoxin contamination; one bread wheat from the Black Sea region, known for its annual rainfall, and a durum wheat sample from southeastern Anatolia, which had the highest detected DON level of 1730 μg kg-1. Among these samples F. graminearum was the predominant species. As F. andiyazi and F. ramigenum are not normally associated with wheat plants, a pathogenicity test was conducted with two isolates of each of these species, revealing no pathogenicity on the durum wheat cultivar ‘San Carlo’. These results provide a basis for managing fungal threats and mycotoxin contamination, safeguarding the quality of wheat grain as an essential agricultural product.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

  1. Abdallah-Nekache N., Laraba I., Ducos C., Barreau C., Bouznad Z., Boureghda H., 2019. Occurrence of Fusarium head blight and Fusarium crown rot in Algerian wheat: identification of associated species and assessment of aggressiveness. European Journal of Plant Pathology 154(3): 499–512. https://doi.org/10.1007/s10658-019-01673-7. DOI: https://doi.org/10.1007/s10658-019-01673-7
  2. Alkadri D., Nipoti P., Döll K., Karlovsky P., Prodi A., Pisi A., 2013. Study of fungal colonization of wheat kernels in Syria with a focus on Fusarium species. International Journal of Molecular Sciences 14(3): 5938–5951. https://doi:10.3390/ijms14035938. DOI: https://doi.org/10.3390/ijms14035938
  3. Amato B., Pfohl, K., Tonti S., Nipoti P., Dastjerdi R., … Prodi A., 2015. Fusarium proliferatum and fumonisin B1 co-occur with Fusarium species causing Fusarium head blight in durum wheat in Italy. Journal of Applied Botany and Food Quality 88: 228–233. https://doi.org/10.5073/JABFQ.2015.088.033.
  4. Arıcı Ş. E., Arap Ü., Yatağan F. B., 2013. Isparta ve Burdur İlleri Buğday Ekim Alanlarındaki Kök ve Kök Boğazı Fungal Hastalık Etmenlerinin Belirlenmesi (in Turkish). Journal of Natural and Applied Science 17(2): 26–30.
  5. Beccari G., Senatore M. T., Tini F., Sulyok M., Covarelli L., 2018. Fungal community, Fusarium head blight complex and secondary metabolites associated with malting barley grains harvested in Umbria, central Italy. International Journal of Food Microbiology 273: 33–42. https://doi.org/10.1016/j.ijfoodmicro.2018.03.005. DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.03.005
  6. Bentley A., Tunali B., Nicol J., Burgess L., Summerell B., 2006., A survey of Fusarium species associated with wheat and grass stem bases in northern Turkey. Sydowia 58(2): 163–177.
  7. Boratyn G. M., Camacho C., Cooper P. S., Coulouris G., Fong A., … Zaretskaya I., 2013. BLAST: a more efficient report with usability improvements. Nucleic Acids Research 41: 29–33. https://doi.org/10.1093/nar/gkt282. DOI: https://doi.org/10.1093/nar/gkt282
  8. Busman M., Desjardins A. E., Proctor R. H., 2012. Analysis of fumonisin contamination and the presence of Fusarium in wheat with kernel black point disease in the United States. Food Additives and Contaminants 29(7): 1092–1100. https://doi.org/10.1080/19440049.2012.671787. DOI: https://doi.org/10.1080/19440049.2012.671787
  9. BÜGEM, 2021. Bitkisel Üretim Genel Müdürlüğü Available at: https://www.tarimorman.gov.tr/BUGEM/TTSM/Sayfalar/Detay.aspx?SayfaId=158 Acession Date: 01.05.2023.
  10. Chernomor O., Von Haeseler A., Minh B. Q., 2016. Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65(6): 997–1008. https://doi.org/10.1093/sysbio/syw037. DOI: https://doi.org/10.1093/sysbio/syw037
  11. Cowger C., Ward T. J., Nilsson K., Arellano C., McCormick S. P., Busman M., 2020. Regional and field-specific differences in Fusarium species and mycotoxins associated with blighted North Carolina wheat. International Journal of Food Microbiology 323. https://doi.org/10.1016/j.ijfoodmicro.2020.108594. DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108594
  12. Dal Prà M., Tonti S., Pancaldi D., Nipoti P., Alberti I., 2010. First report of Fusarium andiyazi associated with rice bakanae in Italy. Plant Disease 94(8): 1070. https://doi.org/10.1094/PDIS-94-8-1070A. DOI: https://doi.org/10.1094/PDIS-94-8-1070A
  13. Dehghanpour-Farashah S., Taheri P., Falahati-Rastegar M., 2019. Virulence factors of Fusarium spp., causing wheat crown and root rot in Iran. Phytopathologia Mediterranea 58(1): 115–125. https://doi.org/10.13128/Phytopathol_Mediterr-23860.
  14. Demirdogen A., Guldal H. T., Sanli H., 2023. Monoculture, crop rotation policy, and fire. Ecological Economics 203. https://doi.org/10.1016/j.ecolecon.2022.107611. DOI: https://doi.org/10.1016/j.ecolecon.2022.107611
  15. Desjardins A. E., Busman M., Proctor R. H., Stessman R., 2007. Wheat kernel black point and fumonisin contamination by Fusarium proliferatum. Food Additives and Contaminants 24(10): 1131–1137. https://doi.org/10.1080/02652030701513834. DOI: https://doi.org/10.1080/02652030701513834
  16. Drakopoulos D., Kägi A., Gimeno A., Six J., Jenny E., … Vogelgsang S., 2020. Prevention of Fusarium head blight infection and mycotoxins in wheat with cut-and-carry biofumigation and botanicals. Field Crops Research 246. https://doi.org/10.1016/j.fcr.2019.107681. DOI: https://doi.org/10.1016/j.fcr.2019.107681
  17. Eğerci Y., 2019. Balikesir ve Çanakkale Illerinde çeltik kök çürüklüğüne Neden Olan Fusarium Türlerinin Saptanmasi, Yayginlik Oranlarinin Belirlenmesi ve Mücadelesine Yönelik Araştirmalar. PhD Thesis, Ege University, Türkiye, 160 pp.
  18. El-Gremi S. M., Draz I. S., Youssef W. A. E., 2017. Biological control of pathogens associated with kernel black point disease of wheat. Crop Protection 91: 13–19. https://doi.org/10.1016/j.cropro.2016.08.034. DOI: https://doi.org/10.1016/j.cropro.2016.08.034
  19. Er Ö., Akgül D. S., 2021. Osmaniye ili buğday ekim alanlarında sap çürüklüğü hastalığıyla ilişkili Fusarium türleri. Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi 26(2): 292–305. https://doi.org/10.37908/mkutbd.884544. DOI: https://doi.org/10.37908/mkutbd.884544
  20. Eskola M. Kos G., Elliot C.T., Hajšlová J., Mayar S., Krska R., 2020. Worldwide contamination of food-crops with mycotoxins: validity of the widely cited ‘FAO estimate’ of 25%. Critical Reviews in Food Science Nutrition 60(16): 2773–2789. doi: 10.1080/10408398.2019.1658570. DOI: https://doi.org/10.1080/10408398.2019.1658570
  21. FAOSTAT, 2021. Food and Agriculture Organization of the United Nations (FAO). FAOSTAT Database. Available at https://www.fao.org/faostat/en/#home Accessed March 1, 2023.
  22. Golinsky, P., Kostecki, M., Lasocka, I., Wisniewska, H., Chelkowsky, J., Kaczmarek, Z., 1996. Moniliformin accumulation and other effects of Fusarium avenaceum (Fr.) Sacc. on kernels of winter wheat cultivars. Journal of Phytopathology 144(9–10): 459–499. https://doi.org/10.1111/j.1439-0434.1996.tb00331.x. DOI: https://doi.org/10.1111/j.1439-0434.1996.tb00331.x
  23. Gräfenhan T., Patrick S. K., Roscoe M., Trelka R., Gaba D., … Tittlemier S. A., 2013. Fusarium damage in cereal grains from Western Canada. 1. Phylogenetic analysis of moniliformin-producing Fusarium species and their natural occurrence in mycotoxin-contaminated wheat, oats, and rye. Journal of Agricultural and Food Chemistry 61(23): 5425–5437. https://doi.org/10.1021/jf400651p. DOI: https://doi.org/10.1021/jf400651p
  24. Gruber-Dorninger C., Jenkins T., Schatzmayr G., 2019. Global mycotoxin occurrence in feed: a ten-year survey. Toxins 11(7): 375. https://doi.org/10.3390/toxins11070375. DOI: https://doi.org/10.3390/toxins11070375
  25. Guo H., Ji J., Wang J.S., Sun X., 2020. Deoxynivalenol: Masked forms, fate during food processing, and potential biological remedies. Comprehensive Reviews in Food Science and Food Safety 19(2): 895–926. https://doi.org/10.1111/1541-4337.12545. DOI: https://doi.org/10.1111/1541-4337.12545
  26. Haidukowski M., Somma S., Ghionna V., Cimmarusti M. T., Masiello M., … Moretti A., 2022. Deoxynivalenol and T-2 toxin as major concerns in durum wheat from Italy. Toxins 14(9): 627. https://doi.org/10.3390/toxins14090627. DOI: https://doi.org/10.3390/toxins14090627
  27. Haile J.K., N’Diaye A., Walkowiak S., Nilsen K.T., Clarke J.M., … Pozniak C.J., 2019. Fusarium head blight in durum wheat: recent status, breeding directions, and future research prospects. Journal Phytopathology 109(10): 1664–1675. https://doi.org/10.1094/PHYTO-03-19-0095-RVW. DOI: https://doi.org/10.1094/PHYTO-03-19-0095-RVW
  28. Hassani F., Zare L., Khaledi N., 2019. Evaluation of germination and vigor indices associated with Fusarium-infected seeds in pre-basic seeds wheat fields. Journal of Plant Protection Research 59(1): 69–85. https://doi.org/10.24425/jppr.2019.126037. DOI: https://doi.org/10.24425/jppr.2019.126037
  29. Ioos R., Belhadj A., Menez M., 2004. 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. https://doi.org/10.1007/s11046-004-2228-3. DOI: https://doi.org/10.1007/s11046-004-2228-3
  30. Isebaert S., de Saeger S., Devreese R., Verhoeven R., Maene P., … Haesaert G., 2009. Mycotoxin-producing Fusarium species occurring in winter wheat in Belgium (Flanders) during 2022–2005. Journal Phytopathology 157(2): 108–116. https://doi.org/10.1111/j.1439-0434.2008.01443.x. DOI: https://doi.org/10.1111/j.1439-0434.2008.01443.x
  31. Jedidi I., Jurado M., Cruz A., Trabelsi M. M., Said S., González-Jaén M. T., 2021. Phylogenetic analysis and growth profiles of Fusarium incarnatum-equiseti species complex strains isolated from Tunisian cereals. International Journal of Food Microbiology 353. https://doi.org/10.1016/j.ijfoodmicro.2021.109297. DOI: https://doi.org/10.1016/j.ijfoodmicro.2021.109297
  32. Ji F., He D., Olaniran A.O., Mokoena M.P., Xu J. Shi J., 2019. Occurrence, toxicity, production and detection of Fusarium mycotoxin: a review. Food Production, Processing and Nutrition 1(6). https://doi.org/10.1186/s43014-019-0007-2. DOI: https://doi.org/10.1186/s43014-019-0007-2
  33. Katoh K., Standley D. M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780. https://doi.org/10.1093/molbev/mst010. DOI: https://doi.org/10.1093/molbev/mst010
  34. Khaledi N., Zare L., Hashemi Fesharaki S., 2023. Effect of Fusarium head blight disease on the quality indicators of germination of wheat (Triticum aestivum L.). Journal of Applied Research in Plant Protection 12 (3): 303–321. https://doi.org/10.22034/ARPP.2023.16370.
  35. Kosiak B., Torp M., Skjerve E., Thrane, U., 2003. The prevalence and distribution of Fusarium species in Norwegian cereals: A survey. Acta Agriculturae Scandinavica Section B: Soil and Plant Science 53 (4): 168–176. https://doi.org/10.1080/09064710310018118. DOI: https://doi.org/10.1080/09064710310018118
  36. Leslie J.F., Summerell B.A., 2006. The Fusarium Laboratory Manual. Blackwell Publishing, Hoboken, 1-2. https://doi.org/10.1002/9780470278376 DOI: https://doi.org/10.1002/9780470278376
  37. Leyva-Mir S. G., Garc Ia-Le E., Camacho-Tapia M., Villase~ Nor-Mir H. E., Leyva-Madrigal K. Y., … Tovar-Pedraza J. M., 2022. Occurrence of the Fusarium incarnatum-equiseti species complex causing Fusarium head blight of wheat in Mexico. Plant Disease 106(10): 2755. https://doi.org/10.1094/PDIS-11-21-2467-PDN. DOI: https://doi.org/10.1094/PDIS-11-21-2467-PDN
  38. Marín P., Moretti A., Ritieni A., Jurado M., Vázquez C., González-Jaén M.T., 2012. Phylogenetic analyses and toxigenic profiles of Fusarium equiseti and Fusarium acuminatum isolated from cereals from Southern Europe. Food Microbiology 31(2): 229–37. https://doi.org/10.1016/j.fm.2012.03.014. DOI: https://doi.org/10.1016/j.fm.2012.03.014
  39. McKinney H.H, 1923. Influence of soil temperature and moisture on infection of wheat seedling by Helminthosporium sativum. Journal of Agricultural Research 26: 195–217.
  40. Mishra S., Dewangan J., Divakar A., Rath S.K., 2019. Global occurrence of deoxynivalenol in food commodities and exposure risk assessment in humans in the last decade: a survey. Critical Reviews in Food Science and Nutrition 60(8): 1346–1374. doi: 10.1080/10408398.2019.1571479. DOI: https://doi.org/10.1080/10408398.2019.1571479
  41. Moretti A., Ferracane L., Somma S., Ricci V., Mulè G., … Logrieco A. F., 2010. Identification, mycotoxin risk and pathogenicity of Fusarium species associated with fig endosepsis in Apulia, Italy. Food Additives & Contaminants: Part A: Chemistry, Analysis, Control, Exposure & Risk Assessment. Foreword 27(5): 718–728. https://doi.org/10.1080/19440040903573040. DOI: https://doi.org/10.1080/19440040903573040
  42. Morgounov A., Keser M., Kan M., Küçükçongar M., Özdemir F., … Qualset C.O., 2016. Wheat landraces currently grown in Turkey: distribution, diversity, and use. Crop Science 56(6):1–13. https://doi.org/10.2135/cropsci2016.03.0192. DOI: https://doi.org/10.2135/cropsci2016.03.0192
  43. Mousavi Khaneghah A., Farhadib A., Nematollahic A., Vasseghiand Y., Fakhrie Y., 2020. A systematic review and meta-analysis to investigate the concentration and prevalence of trichothecenes in the cereal-based food. Trends in Food Science & Technology 102:193–202. https://doi.org/10.1016/j.tifs.2020.05.026. DOI: https://doi.org/10.1016/j.tifs.2020.05.026
  44. Mulè G., Susca A., Stea G., Moretti A., 2004. A species-specific PCR assay based on the calmodulin partial gene for identification of Fusarium verticillioides, F. proliferatum and F. subglutinans. European Journal of Plant Pathology 110: 495–502. doi: 10.1023/B:EJPP.0000032389.84048.71. DOI: https://doi.org/10.1007/978-1-4020-2285-2_4
  45. Nazari L., Pattori E., Manstretta V., Terzi V., Morcia C., … Rossi V., 2018. Effect of temperature on growth, wheat head infection, and nivalenol production by Fusarium poae. Food Microbiology 76: 83–90. https://doi.org/10.1016/j.fm.2018.04.015. DOI: https://doi.org/10.1016/j.fm.2018.04.015
  46. Niehaus E.M., Von Bargen K.W., Espino J.J., Pfannmuller A., Humpf H.U., Tudzynski B., 2014. Characterization of the fusaric acid gene cluster in Fusarium fujikuroi. Applied Microbiology Biotechnology 98(4): 1749–1762. doi: 10.1007/s00253-013-5453-1. DOI: https://doi.org/10.1007/s00253-013-5453-1
  47. Nicholson P., Simpson D.R., Weston G, Rezanoor H.N., Lees A.K., … Joyce D., 1998. Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiological and Molecular Plant Pathology 53: 17–37. DOI: https://doi.org/10.1006/pmpp.1998.0170
  48. Nielsen L.K., Jensen J.D. Nielsen G.C., Jensen J.E., Spliid N.H., … Jorgensen L.N., 2011. Fusarium head blight of cereals in Denmark: species complex and related mycotoxins. Phytopathology 101(8): 960–969. https://doi.org/10.1094/PHYTO-07-10-0188. DOI: https://doi.org/10.1094/PHYTO-07-10-0188
  49. O’Donnell, K., Cigelnik, E., Nirenberg, H.I., 1998. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90(3): 465–493. https://doi.org/10.1080/00275514.1998.12026933O’Donnell K, Sutton DA, Rinaldi MG., 2009. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-equiseti and F. chlamydosporum species complexes within the United States. Journal of Clinical Microbiology 47(12): 3851– 3861. https://doi.org/ 10.1128/JCM.01616-09. DOI: https://doi.org/10.1128/JCM.01616-09
  50. O’Donnell K., McCormick S. P., Busman M., Proctor R. H., Ward T. J., … Geiser D. M., Alberts J. F., Rheeder J. P., 2018. Toxigenic Fusarium species: identity and mycotoxicology revisited. Mycologia 110(6): 1058– 1080. https://doi.org/10.1080/00275514.2018.1519773. DOI: https://doi.org/10.1080/00275514.2018.1519773
  51. Pecoraro F., Giannini M., Beccari G., Covarelli L., Filippini G., … Prodi A., 2018. Comparative studies about fungal colonization and deoxynivalenol translocation in barley plants inoculated at the base with Fusarium graminearum, Fusarium culmorum and Fusarium pseudograminearum. Agricultural and Food Science 27(1): 74–83. https://dx.doi.org/10.23986/afsci.67704. DOI: https://doi.org/10.23986/afsci.67704
  52. Parry D. W, Bayles R. A, Priestley R. H., 1985. Resistance of winter wheat varieties to ear blight caused by Fusarium avenaceum and F. culmorum. Tests of Agrochemicals and Cultivars 6: 164–165.
  53. Parry D. W., Nicholson, P., 1996. Development of a PCR assay to detect Fusarium poae in wheat. Plant Pathology 45(2): 383–391. https://doi.org/10.1046/j.1365-3059.1996.d01-133.x. DOI: https://doi.org/10.1046/j.1365-3059.1996.d01-133.x
  54. Pereyra S., Dill-Macky, R., 2021. Fusarium species recovered from wheat and barley grains in Uruguay, pathogenicity and deoxynivalenol content. Agrociencia Uruguay 14 (2): 33–44. https://doi.org/10.31285/AGRO.14.625. DOI: https://doi.org/10.31285/AGRO.14.625
  55. Prodi A., Purahong W., Tonti S., Salomoni D., Nipoti P., … Pisi A., 2011. Difference in chemotype composition of Fusarium graminearum populations isolated from durum wheat in adjacent areas separated by the Apennines in Northern-Central Italy. Plant Pathology Journal 27(4): 354–359. http://dx.doi.org/10.5423/PPJ.2011.27.4.354. DOI: https://doi.org/10.5423/PPJ.2011.27.4.354
  56. Ronquist F., Teslenko M., Van der Mark P., Ayres D. L., Darling A., … Huelsenbeck J. P., 2012. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029. DOI: https://doi.org/10.1093/sysbio/sys029
  57. Rigorth K. S., Finckh M. R., Šišić A., 2021. First report of Fusarium venenatum causing foot and root rot of wheat (Triticum aestivum) in Germany. Plant Disease 105(6): 1855. https://doi.org/10.1094/PDIS-10-20-2202-PDN. DOI: https://doi.org/10.1094/PDIS-10-20-2202-PDN
  58. Savary S., Willocquet L., Pethybridge S.J., Esker P., McRoberts N., Nelson A., 2019. The global burden of pathogens and pests on major food crops. Nature Ecologia & Evolution 3(3): 430–439 https://doi.org/10.1038/s41559-018-0793-y. DOI: https://doi.org/10.1038/s41559-018-0793-y
  59. Scherm B., Balmas V., Spanu F., 2013. Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molecular Plant Pathology 14: 323–41. https://doi.org/10.1111/mpp.12011. DOI: https://doi.org/10.1111/mpp.12011
  60. Senatore M. T., Ward T. J., Cappelletti E., Beccari G., McCormick S. P., … Laraba I., O’Donnell K., Prodi A., 2021. Species diversity and mycotoxin production by members of the Fusarium tricinctum species complex associated with Fusarium head blight of wheat and barley in Italy. International Journal of Food Microbiology 358. https://doi.org/10.1016/j.ijfoodmicro.2021.109298. DOI: https://doi.org/10.1016/j.ijfoodmicro.2021.109298
  61. Senatore M.T., Prodi A., Tini F., Balmas V., Infantino A., … Beccari G., 2023. 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. Journal of The Science of Food and Agriculture 103(9): 4251–4719. https://doi.org/ 10.1002/jsfa.12526. DOI: https://doi.org/10.1002/jsfa.12526
  62. Shah L., Ali A., Yahya M., Zhu Y., Wang S., … Ma C., 2018. Integrated control of Fusarium head blight and deoxynivalenol mycotoxin in wheat. Plant Pathology 67(3): 532–548. https://doi.org/10.1111/ppa.12785. DOI: https://doi.org/10.1111/ppa.12785
  63. Shikur Gebremariam, E. S., 2015. Determination of Fusarium Species Associated with Crown Rot of Wheat in Turkey and Assessment of Resistance Status of Some Wheat Genotypes to Fusarium culmorum. PhD Thesis, Ankara University Graduate School of Natural and Applied Sciences, 132 pp.
  64. Shikur Gebremariam, E., Sharma-Poudyal, D., Paulitz, T. C., Erginbas-Orakci, G., Karakaya, A., Dababat, A. A., 2018. Identity and pathogenicity of Fusarium species associated with crown rot on wheat (Triticum spp.) in Turkey. European Journal of Plant Pathology 150(2): 387–399. https://doi.org/10.1007/s10658-017-1285-7. DOI: https://doi.org/10.1007/s10658-017-1285-7
  65. Smiley R. W., Gourlie J. A., Easley S. A., Patterson L. M., 2005. Pathogenicity of fungi associated with the wheat crown rot complex in Oregon and Washington. Plant Disease 89(9): 949–957. https://doi.org/ 10.1094/PD-89-0949. DOI: https://doi.org/10.1094/PD-89-0949
  66. Stanković S., Lević J., Ivanović D., Krnjaja V., Stanković G., Tanćić S., 2012. Fumonisin B1 and its co-occurrence with other fusariotoxins in naturally-contaminated wheat grain. Food Control 23: 384–388. https://doi.org/10.1016/j.foodcont.2011.08.003. DOI: https://doi.org/10.1016/j.foodcont.2011.08.003
  67. Summerell B.A., 2019. Resolving Fusarium: current status of the genus. Annual Review of Phytopathology 57: 323–339. https://doi.org/10.1146/annurev-phyto-082718-100204. DOI: https://doi.org/10.1146/annurev-phyto-082718-100204
  68. Tamura K., Stecher G., Kumar, S., 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution 38(7): 3022–3027. https://doi.org/ 10.1093/molbev/msab120. DOI: https://doi.org/10.1093/molbev/msab120
  69. Tian Y., Zhang D., Cai P., Lin H., Ying H., Hu Q., Wu A., 2022. Elimination of Fusarium mycotoxin deoxynivalenol (DON) via microbial and enzymatic strategies: Current status and future perspectives. Trends in Food Science & Technology 124: 96–107. https://doi.org/10.1016/j.tifs.2022.04.002. DOI: https://doi.org/10.1016/j.tifs.2022.04.002
  70. Torbati M., Arzanlou M., Sandoval-Denis M., Crous P.W., 2019. Multigene phylogeny reveals new fungicolous species in the Fusarium tricinctum species complex and novel hosts in the genus Fusarium from Iran. Mycological Progress 18: 119–133. https://doi.org/10.1007/s11557-018-1422-5. DOI: https://doi.org/10.1007/s11557-018-1422-5
  71. Torres-Cruz T. J., Whitaker B., Proctor R. H., Laraba I., Kim H.-S., … Geiser D. M., 2022. FUSARIUM-ID v.3.0: An updated downloadable resource for Fusarium species identification. Plant Disease 106(6):1610–1616. https://doi.org/10.1094/PDIS-09-21-2105-SR. DOI: https://doi.org/10.1094/PDIS-09-21-2105-SR
  72. Tunalı B., Nicol J., Erol F. Y., Altiparmak G., 2006. Pathogenicity of Turkish crown and head scab isolates on stem bases on winter wheat under greenhouse conditions. Plant Pathology Journal 5(2): 143–149. doi: 10.3923/ppj.2006.143.149. DOI: https://doi.org/10.3923/ppj.2006.143.149
  73. Tunalı B., Nicol J. M., Hodson D., Uçkun Z., Büyük O., … Bağci S. A., 2008. Root and crown rot fungi associated with spring, facultative, and winter wheat in Turkey. Plant Disease 92(9): 1299–1306. https://doi.org/10.1094/PDIS-92-9-1299. DOI: https://doi.org/10.1094/PDIS-92-9-1299
  74. TÜİK, 2021. Türkiye İstatistik Kurumu (in Turkish) Available at: https://data.tuik.gov.tr/Kategori/GetKategori?p=Tarim-111. Accessed March 1, 2023.
  75. Turco S., Grottoli A., Drais MI., De Spirito C., Faino L., … Mazzaglia A., 2021. Draft genome sequence of a new Fusarium isolate belonging to Fusarium tricinctum species complex collected from hazelnut in central Italy. Frontiers in Plant Science (12). https: //doi.org/10.3389/fpls.2021.788584. DOI: https://doi.org/10.3389/fpls.2021.788584
  76. Ünal F., Dolar F. S., Tekiner N., Yeğin N. Z., 2017. Molecular identification, virulens and genetic diversity of Fusarium species on wheat. Eurasian Journal of Agricultural research 1(2): 13–22.
  77. Ünüsan N., 2019. Systematic review of mycotoxins in food and feeds in Turkey. Food Control 97: 1–14. https://doi.org/10.1016/j.foodcont.2018.10.015. DOI: https://doi.org/10.1016/j.foodcont.2018.10.015
  78. Waalwijk C., Kastelein P., De Vries I., Kerényi Z., Van Der Lee T., … Kema G., 2003. Major changes in Fusarium spp. in wheat in the Netherlands. European Journal of Plant Pathology 109: 743–754. https://doi.org/10.1023/A:1026086510156. DOI: https://doi.org/10.1023/A:1026086510156
  79. Wang M. M., Chen Q., Diao Y. Z., Duan W. J., Cai L., 2019. Fusarium incarnatum-equiseti complex from China. Persoonia 43: 70–89. https://doi.org/10.3767/persoonia.2019.43.03. DOI: https://doi.org/10.3767/persoonia.2019.43.03
  80. Wright D. G., Thomas G. J., Loughman R., Fuso-Nyarko J., Bullock S., 2010. Detection of Fusarium graminearum in wheat grains in Western Australia. Australasian Plant Disease Notes 5: 82–84. https://doi.org/10.1071/DN10029. DOI: https://doi.org/10.1071/DN10029
  81. Xia J. W., Sandoval- Denis M., Crous P. W., Zhang X. G., Lombard L., 2019. Numbers to names - restyling the Fusarium incarnatum-equiseti species complex. Persoonia 43: 186–221. https://doi.org/ 10.3767/persoonia.2019.43.05. DOI: https://doi.org/10.3767/persoonia.2019.43.05
  82. Xu X., Nicholson P., 2009. Community ecology of fungal pathogens causing wheat head blight. Annual Review of Phytopathology 47: 83–103. https://doi.org/ 10.1146/annurev-phyto-080508-081737. DOI: https://doi.org/10.1146/annurev-phyto-080508-081737
  83. Zhou H., He X., Wang S., Ma Q., Sun B., … Li H., 2019. Diversity of the Fusarium pathogens associated with crown rot in the Huanghuai wheat-growing region of China. Applied Microbiology 21(8): 2740–2754. https://doi.org/10.1111/1462-2920.14602. DOI: https://doi.org/10.1111/1462-2920.14602