Aggressiveness and trichothecene production of Fusarium graminearum isolates from cereals in Serbia

  • Ana Obradović Maize Research Institute Zemun Polje, Slobodana Bajića 1, 11185 Belgrade
  • Jelena Vukadinović Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade
  • Milica Nikolić Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade
  • Aleksandra Bulajić University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade
  • Goran Stanković Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade
  • Nenad Delić Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade
  • Slavica Stanković Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade
Keywords: cereals, Fusarium graminearum, mycotoxins, chemotypes, trichotecene, pathogenicity

Abstract


The aim of this study was to assess variations in aggressiveness and trichothecene production of F. graminearum isolates originating from maize, wheat and barley in Serbia. Analyzing F. graminearum isolates (98) obtained from various agroecological conditions of Serbia over the period from 1993 to 2010, using the HPLC method, the following two chemotypes were observed: 3-acetyl-deoxinivalenol (3ADON) and 15-acetyl-deoxinivalenol (15ADON). A great diversity in the production of deoxinivalenol (DON) derivatives was observed. A majority of F. graminearum isolates, regardless of their origin (maize, wheat or barley) belonged to the 15ADON chemotype. The 3ADON chemotype was also detected, but in a significantly smaller number (13/98) samples, compared to the 15ADON chemotype (85/98). None of the tested isolates belonged to the NIV chemotype. The examined isolates showed different pathogenicity on barley leaf, wheat class and maize ears. The average pathogenicity of the tested isolates was the highest on barley leaf. It was observed that isolates originating from wheat had the highest average daily increase in mycelium growth rate (27.37 mm). Statistical analysis of the obtained results for mycotoxins synthesis showed that there was a highly significant statistical correlation between the production potentials of total DON, 3ADON and 15ADON in F. graminearum isolates belonging to various chemotypes. However, there was no statistically significant correlation between the aggressiveness of isolates and the production of total DON in isolates belonging to 3ADON and 15ADON chemotypes.

Author Biographies

Jelena Vukadinović, Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade

Research Assistant

Milica Nikolić, Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade

Research Associate

Aleksandra Bulajić, University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade

Full professor

Goran Stanković, Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade

Research Associate

Nenad Delić, Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade

Principal Research Fellow

Slavica Stanković, Maize Research Institute Zemun Polje, Sloodana Bajića 1, 11185 Belgrade

Principal Research Fellow

References

Aamot, H.U., Ward, T.J., Brodal, G., Vralstad, T., Larsen, G.B., Klemsdal, S.S. ... Hofgaard, I.S. (2015). Genetic and phenotypic diversity within the Fusarium graminearum species complex in Norway. European Journal of Plant Pathology, 142, 501-519.

Abramson, D., Clear, R.M., Gaba, D., Smith, D.M., Patrick, S.K., & Saydak, D. (2001). Trichothecene and moniliformin production by Fusarium species from western Canadian wheat. Journal of Food Protection, 64, 1220-1225.

Atanassov, Z., Nakamura, C., Mori, N., Kaneda, C., Kato, H., Jin, Y-Z. ... Murai, K. (1994). Mycotoxin production and pathogenicity of Fusarium species and wheat resistance to Fusarium head blight. Canadian Journal of Botany, 72, 161-167.

Backhouse, D. (2014). Global distribution of Fusarium graminearum, F. asiaticum and F. boothii from wheat in relation to climate. European Journal of Plant Pathology, 139, 161-173.

Blandino, M., Haidukowski, M., Pascale, M., Plizzari, L., Scudellari, D., & Reyneri, A. (2012). Integrated strategies for the control of Fusarium head blight and deoxynivalenol contamination in winter wheat. Field Crops Research, 133, 139-149.

Boutigny, A.L., Ward, T.J., Ballois, N., Iancu, G., & Ioos, R. (2014). Diversity of the Fusarium graminearum species complex on French cereals. European Journal of Plant Pathology, 138, 133-148.

Bozac, P., Popescu, S., Botau, D., Boldura, O.M., & Pirvulescu, P. (2016). Molecular characterization for some new Fusarium isolates collected from the West Part of Romania. Romanian Biotechnological Letters, 21(3), 11560-11568.

Burgess, L.W., Summerell, B.A., Bullock, S., Gott, K.P., & Backhouse, D. (1994). Laboratory manual for Fusarium research (3rd ed.). Sydney, Australia: University of Sydney & Royal Botanic Gardens.

Carter, J.P., Rezanoor, H.N., Holden, D., Desjardins, A.E., Plattner, R.D., & Nicholson, P. (2002). Variation in pathogenicity associated with the genetic diversity of Fusarium graminearum. European Journal of Plant Pathology, 108, 573-583.

Fredlund, E., Gidlund, A., Sulyok, M., Borjesson, T., Krska, R., Olsen, M., & Lidlblad, M. (2013). Deoxynivalenol and other selected Fusarium toxins in Swedish oats–occurrence and correlation to specific Fusarium species. International Journal of Food Microbiology, 167, 276-283.

Gale, L.R., Harrison, S.A., Ward, T.J., O’Donnell, K., Milus, E.A., Gale, S.W., & Kistler, H.C. (2011). Nivalenoltype populations of Fusarium graminearum and F. asiaticum are prevalent on wheat in southern Louisiana. Phytopathology, 101, 124-134.

Gale, L.R., Ward, T.J., Balmas, V., & Kistler, H.C. (2007). Population subdivision of Fusarium graminearum sensu stricto in the upper Midwestern United States. Phytopathology, 97, 1434-1439.

Goswami, R.S., & Kistler, H.C. (2005). Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology, 95, 1397-1404.

Guo, X.W., Fernando, W.G.D., & Seow-Brock. H.Y. (2008). Population structure, chemotype diversity, and potential chemotype shifting of Fusarium graminearum in wheat fields of Manitoba. Plant Disease, 92, 756-762.

Imathiu, M.S., Ray. V.R., Back, M., Hare, C.M., & Edwards, G.S. (2009). Fusarium langsethiae pathogenicity and aggressiveness towards oats and wheat in wounded and unwounded in vitro detached leaf assays. European Journal of Plant Pathology, 124, 117-126.

Jennings, P., Coates, M.E., Walsh, K., Turner, J.A., & Nicholson, P. (2004). Determination of deoxynivalenoland nivalenol-producing chemotypes of Fusarium graminearum isolated from wheat crops in England and Wales. Plant Pathology, 53, 643-652.

Kuhnem, P.R., Del Ponte, E.M., Dong, Y., & Bergstrom, G.C. (2015). Fusarium graminearum isolates from wheat and maize in New York show similar range of aggressiveness and toxigenicity in cross-species pathogenicity tests. Phytopathology, 105, 441-448.

Lee, T., Paek, J.S., Lee, K.A., Lee, S., Choi, J.H., Ham, H. ... Ryu, J.G. (2016). Occurrence of Toxigenic Fusarium vorosii among Small Grain Cereals in Korea. The Plant Pathology Journal, 32, 407-413.

Lee, T., Zhang, H., Diepeningen, A., & Waalwijk, C. (2015). Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Additives and Contaminants, Part A, 32, 453-460.

Li, W., Hu, Y.C., Chen. Y., Zhang, A.X., & Chen, H.G. (2010). Phylogenetic analysis, chemotype diversity, and pathogenicity of the Fusarium graminearum clade in the Yangtze basin. Mycosystema, 29, 51-58.

Lindblad, M., Gidlund, A., Sulyok, M., Borjesson, T., Krska, R., Olsen, M., & Fredlund, E. (2013). Deoxynivalenol and other selected Fusarium toxins in Swedish wheat−Occurrence and correlation to specific Fusarium species. International Journal of Food Microbiology, 167, 284-291.

Logrieco, A., Moretti A., Ritieni, A., Bottalico, A., & Corda, P. (1995). Occurrence and toxigenicity of F. proliferatum from preharvest maize ear rot and associated mycotoxins in Italy. Plant Disease, 79, 727-723.

Logrieco, A., Mule, G., Moretti, A., & Bottalico, A. (2002). Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. European Journal of Plant Pathology, 108, 597-609.

Luongo, D., Severino, L., Bergamo, P., D’Arienzo, R., & Rossi, M. (2010). Trichothecenes NIV and DON modulate the maturation of murine dendritic cells. Toxicon, 55, 73-80.

McCormick, S. (2003). The role of DON in pathogenicity. In Leonard. K.J. Bushnell. W.R. (Eds.), Fusarium head blight of wheat and barley (pp 165-183). St. Paul, MN, USA: American Phytopathological Society.

Mesterhazy, A., Bartok, T., Mirocha, C.G., & Komoroczy, R. (1999). Nature of wheat resistance to Fusarium head blight and the role of deoxynivalenol for breeding. Plant Breeding, 118, 97-110.

Miller, J. D., Greenhalgh, R., Wang, Y. Z., & Lu, M. (1991). Trichothecene chemotypes of three Fusarium species. Mycologia, 83, 121-130.

Moretti, A., Panzarini, G., Somma, S., Campagna, C., Ravaglia, S., Logrieco, A.F., & Solfrizzo, M. (2014). Systemic growth of F. graminearum in wheat plants and related accumulation of deoxynivalenol. Toxins, 6, 1308-1324.

Moretti, A., Pascale, M., & Logrieco, A.F. (2018). Mycotoxin risks under a climate change scenario in Europe. Trends in Food Science and Technology, 84, 38-40.

Nielsen, L.K., Jensen, J.D., Rodriguez, A., Jorgensen, L.N., & Justesen, A.F. (2012). TRI12 based quantitative realtime PCR assays reveal the distribution of trichothecene genotypes of F. graminearum and F. culmorum isolates in Danish small grain cereals. International Journal of Food Microbiology, 157, 384-392.

Obradović, A., Stanković, S., Krnjaja, V., Nikolić, A., Ignjatović-Micić, D., Stepanović, J., & Duduk, B. (2017). Trichothecene chemotype diversity of Fusarium graminearum isolated from wheat, maize and barley in Serbia. Genetika, 49(1), 355-364.

O’Donnell, K., Kistler, H.C., Tacke, B.K., & Casper, H.H. (2000). Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. In Proceedings of the National Academy of Sciences of the USA, 97(14), 7905-7910.

O’Donnell, K., Ward, T.J., Aberra, D., Kistler, H.C., Aoki, T., Orwig, N. ... Klemsdal, S.S. (2008). Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genetics and Biology, 45(11), 1514-1522.

O’Donnell, K., Ward, T.J., Geiser, D.M., Kiestler, H.C, & Aoki, T. (2004). Genealogical concordance between mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genetics and Biology, 41, 600-623.

Prodi, A., Purahong, W., Tonti, S., Salomoni, D., Nipoti, P., Covarelli, L., & Pisi, A. (2011). Difference in chemotype composition of Fusarium graminearum populations isolated from durum wheat in adjacent areas separated by the Apennines in NorthernCentral Italy. Plant Pathology Journal, 27, 354-359.

Puri, D.K., & Zhong, S. (2010). The 3ADON population of Fusarium graminearum found in North Dakota is more aggressive and produces a higher level of DON than the prevalent 15ADON population in spring wheat. Phytopathology, 100, 1007-1014.

Reid, L.M., Hamilton, R.I., & Mather, D.E. (1996). Screening maize for resistance to gibberella ear rot (Technical Bulleten 5E). Canada: Research Branch Agriculture and Agri-Food Canada.

Sarver, B.A.J., Ward, T.J., Gale, L.R., Broz, K., Kistler, H.C., Aoki, T. ... O’Donnell, K. (2011). Novel Fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genetics and Biology, 48, 1096-1107.

Schmale, D.G., Wood-Jones, A.K., Cowger, C., Bergstrom, G.C., & Arellano, C. (2011). Trichothecene genotypes of Gibberella zeae from winter wheat fields in the eastern USA. Plant Pathology, 60, 909-917.

Somma, S., Petruzzella, A.L., Logrieco, A.F., Meca, G., Cacciola, O.S., & Moretti, A. (2014). Phylogenetic analyses of Fusarium graminearum strains from cereals in Italy and characterisation of their molecular and chemical chemotypes. Crop and Pasture Science, 65, 52-60.

Starkey, D.E., Ward, T.J., Aoki, T., Gale, L.R., Kistler, H.C., Geiser, D.M. O’Donnell, K. (2007). Global molecular survelliance reveals novel Fusarium head blight species and trichotecene toxin diversity. Fungal Genetics and Biology, 44, 1191-1204.

Tančić, S., Stanković, S., Lević, J., & Krnjaja, V. (2015). Correlation of deoxynivalenol and zearalenone production by Fusarium species originating from wheat and maize grain. Pesticides and Phytomedicine, 30, 99-105.

Toth, B., Mesterhazy, A., Horvath, Z., Bartok, T., Varga, M., & Varga, J. (2005). Genetic variability of central European isolates of the Fusarium graminearum species complex. European Journal of Plant Pathology, 113, 35-45.

Villafana, R.T., Ramdass, A.C., & Rampersad, S.N. (2019). Selection of Fusarium trichothecene toxin genes for molecular detection depends on TRI gene cluster organization and fene function. Toxins, 11(1), 36.

Von der Ohe, C., Gauthier, V., Tamburic-Ilincic, L., Brule-Babel, A., Fernando, W.G.D., Clear, R. ... Miedaner, T. (2010). A comparison of aggressiveness and deoxynivalenol production between Canadian Fusarium graminearum isolates with 3-acetyl and 15-acetyldeoxynivalenol chemotypes in field-grown spring wheat. European Journal of Plant Pathology, 127, 407-417.

Ward, T.J., Clear, R.M., Rooney, A.P., O’Donnell, K., Gaba, D., Patrick, S. ... Nowicki, T.W. (2008). An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genetics and Biology, 45, 473-484.

Yli-Mattila, T., Gagkaeva, T., Ward, T.J., Aoki, T., Kistler, H.C., & O’Donnell, K. (2009). A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from the Russian Far East. Mycologia, 101, 841-852.

Zhang, H., van der Lee, T., Waalwijk, C., Chen, W., Xu, J., Xu, J. ... Feng, J. (2012). Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. PlosOne, 7(2). e31722.

Zhang, H., Zhang, Z., van der Lee, T., Chen, W.Q., Xu, J., Xu, J.S.... Feng, J. (2010). Population genetic analyses of Fusarium asiaticum populations from barley suggest a recent shift favoring 3ADON producers in Southern China. Phytopathology, 100, 328-336.

Published
2021/06/17
Section
Original Scientific Paper