Review
Chemotypes and geographic distribution of the Fusarium graminearum species complex
Sebastian W. Przemieniecki, Tomasz P. Kurowski, Karol Korzekwa
Abstract The Fusarium graminearum species complex (FGSC) consists of phylogenetically distinct pathogenic species. Isolates from various regions display genetic variety worldwide. Three type B trichothecene chemotypes have been identified within the FGSC: nivalenol, 3-deoxynivalenol and 15-deoxynivalenol. The variations in morphological, genetic and virulence traits of FGSC fungi can be attributed mainly to their geographic boundaries. The geographic range of host plants, type of farming system and weather conditions also influence the prevalence of FGSC taxa. The geographic distribution of FGSC members may reflect not only their chemotype but also adaptive traits. While 15-acetyl-deoxynivalenol (15-ADON) chemotype is prevalent in most of Europe, the 3-acetyl-deoxynivalenol (3-ADON) chemotype has achieved greater prevalence in parts of North America. The Asian species F. asiaticum has spread into new territories. Isolates of F. asiaticum have been identified in North America and Europe, and the species has recently been reported to be infecting cereal crops in South America. The occurrence of numerous members of the FGSC in those regions and the introduction of F. asiaticum into new areas raise significant food safety concerns and indicate the need for monitoring mycotoxin concentrations in harvested grain.
References
Abd-Elsalam, K.A., F. Schnieder, J.A. Verreet. 2002. Population analysis of Fusarium species. Phytomedizin 3: 18–19. |
|
Abedi-Tizaki, M., S.K. Sabbagh. 2013. Detection of 3-acetyldeoxynivalenol, 15-acetyldeoxynivalenol and nivalenol-chemotypes of Fusarium graminearum from Iran using specific PCR assays. Plant Knowledge Journal 2: 38–42. |
|
Akinsanmi, O.A., D. Backhouse, S. Simpfendorfer, S. Chakraborty. 2006. Genetic diversity of Australian Fusarium graminearum and F. pseudograminearum. Plant Pathology 55: 494–504. |
|
Amarasinghe, C., J-H. Wang, Y-C. Liao, W.G.A. Fernando. 2011. Difference in TRI13 gene sequences between the 3-acetyldeoxynivalenol producing Fusarium graminearum chemotypes from Canada and China. International Journal of Molecular Sciences 12: 6164–6175. |
|
Aoki, T., K. O'Donnell. 1999. Morphological and molecular characterization of Fusarium pseudograminearum sp. nov., formerly recognized as the Group 1 population of F. graminearum. Mycologia 91: 597–609. |
|
Aoki, T., T.J. Ward., H.C. Kistler, K. O'Donnell. 2012. Systematics, phylogeny and trichothecene mycotoxin potential of Fusarium head blight cereal pathogens. Mycotoxins 62: 91–102. |
|
Astolfi, P., M.M. Reynoso, M.L. Ramirez, S.N. Chulze, T.C.A. Alves, D.J. Tessmann, E.M. Del Ponte. 2012. Genetic population structure and trichothecene genotypes of Fusarium graminearum isolated from wheat in southern Brazil. Plant Pathology 61: 289–295. |
|
Atoui, A., A. El Khoury, M. Kallassy, A. Lebrihi. 2011. Quantification of Fusarium graminearum and Fusarium culmorum by real-time PCR system and zearalenone assessment in corn. International Journal of Food Microbiology 154: 59–65. |
|
Benyon, F.H.L., L.W. Burgess, P.J. Sharp. 2000. Molecular genetic investigations and reclassification of Fusarium species in sections Fusarium and Roseum. Mycological Research 104: 1164–1174. |
|
Bowden, R.L., K.A. Zeller, J.F. Leslie. 2000. Population structure of Gibberella zeae in the Great Plains of North America. In: Proceedings of the International Symposium on Wheat Improvement for Scab Resistance, Suzhou and Nanjing, Jiangsu, China, pp. 211–213. |
|
Boutigny, A.L., T.J. Ward, G.J. van Coller, B. Flett, S.C. Lamprech, K. O'Donnell, A. Viljoen. 2011. Analysis of the Fusarium graminearum species complex from wheat, barley and corn in South Africa provides evidence of species-specific differences in host preference. Fungal Genetics and Biology 48: 914–920 |
|
Brown, D.W., R.B. Dyer, S.P. McCormick, D.F. Kenda, R.D. Plattner. 2004. Functional demarcation if the Fusarium core trichotecene gene cluster. Fungal Genetics and Biology 41: 454–462. |
|
Burlakoti, R.R., S.M. Neate, T.B. Adhikari, S. Gyawali, B. Salas, B.J. Steffenson, P.B. Schwarz. 2011. Trichothecene profiling and population genetic analysis of Gibberella zeae from barley in North Dakota and Minnesota. Phytopathology 101: 687–695. |
|
Busso, C., E.N. Kaneshima, F. De Assis Franco, C.B. Querol, M.A. De Castro-Prado. 2007. Vegetative compatibility and molecular characterization of Fusarium graminearum isolates from the State of Paraná, Brazil. Ciencia Rural 37: 1813–1816. |
|
Carter, J.P., H.N. Rezanoor, D. Holden, A.E. Desjardins, R.D. Plattner, P. Nicholson. 2002. Variation in pathogenicity associated with the genetic diversity of Fusarium graminearum. European Journal of Plant Pathology 108: 573–583. |
|
Chandler, E.A., D.R. Simpson, M.A. Thomsett, P. Nicholson. 2003. Development of PCR assays to Tri7 and Tri13 trichothecene biosynthetic genes, and characterisaton of chemotypes of Fusarium graminearum, Fusarium culmorum and Fusarium cerealis. Physiological and Molecular Plant Pathology 62: 355–367. |
|
Chen, Y, M.G. Zhou. 2009. Characterization of Fusarium graminearum isolates resistant to both carbendazim and a new fungicide JS399-19. Phytopathology 99: 441–446. |
|
Cuomo, C.A., U. Güldener, J.R. Xu, F. Trail, B.G. Turgeon, A. Di Pietro, J.D. Walton, L.J. Ma, S.E. Baker, M. Rep, G. Adam, J. Antoniw, T. Baldwin, S. Calvo, Y.L. Chang, D. Decaprio, L.R. Gale, S. Gnerre, R.S. Goswami, K. Hammond-Kosack, L.J. Harris, K. Hilburn, J.C. Kennell, S. Kroken, J.K. Magnuson, G. Mannhaupt, E. Mauceli, H.W. Mewes, R. Mitterbauer, G. Muehlbauer, M. Münsterkötter, D. Nelson, K. O'donnell, T. Ouellet, W. Qi, H. Quesneville, M.I. Roncero, K.Y. Seong, I.V. Tetko, M. Urban, C. Waalwijk, T.J. Ward, J. Yao, B.W. Birren, H.C. Kistler. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402. |
|
Desjardins, A.E., R.H. Proctor. 2011. Genetic diversity and trichothecene chemotypes of the Fusarium graminearum clade isolated from corn in Nepal and identi?cation of a putative new lineage. Fungal Biology 115: 38–48. |
|
Feng, J. 2007. Molecular characterization of a Fusarium graminearum lipase gene and its promoter. Ph.D. Thesis, Department of Plant Sciences, University of Saskatchewan, Saskatoon, 129 p. |
|
Gale, L.R., L.F. Chen, C.A. Hernick, K. Takamura, H.C. Kistler. 2002. Population analysis of Fusarium graminearum from wheat fields in eastern China. Phytopathology 92: 1315–1322. |
|
Gale, L.R., S.A. Harrison, T.J. Ward, K. O'Donnell, E.A. Milus, S.W. Gale, H.C. Kistler. 2011. Nivalenol-type populations of Fusarium graminearum and F. asiaticum are prevalent on wheat in Southern Louisiana. Phytopathology 101: 124–134. |
|
Jennings, P., M.E. Coates, K. Walsh, J.A. Turner, P. Nicholson. 2004. Determination of deoxynivalenol- and nivalenol-producing chemotypes of Fusarium graminearum isolated from wheat crops in England and Wales. Plant Pathology 53: 643–652. |
|
Kimura, M., T. Tokai, N. Takahashi-Ando, S. Ohsato, M. Fujimura. 2007. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Bioscience Biotechnology and Biochemistry 71: 2105–2123. |
|
Lee, J., I.Y. Chang, H. Kim, S.H. Yun, J. Leslie, Y.W. Lee. 2009. Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. Applied and Environmental Microbiology 75: 3289–3295. |
|
Lee, T., Y.K. Han, K.H. Kim, S.H. Yun, Y.W. Lee. 2002. Tri13 and Tri7 determine deoxynivalenol- and nivalenol-producing chemotypes of Gibberella zeae. Applied and Environmental Microbiology 68: 2148–2154. |
|
Lee, Y.W., J.J. Jeon, H. Kim, I.Y. Jang, H.S. Kim, S.H. Yun, J.-G. Kim. 2004. Lineage composition and trichothecenes production of Gibberella zeae population in Korea. In: New Horizons of Mycotoxicology for Assuring Food Safety (ed. T. Yoshizawa), pp. 117–122. Japanese Association of Mycotoxicology, Kagawa, Japan. |
|
Liu, W.C., J.H. Xi, H.Y. Li, H.Y. Pan, H.Q. Hu, Y.L. Guo, R.L. Bai. 2002. RAPD analysis of isolates from Fusarium spp. causing wheat head blight in northeast China. Mycosystema 21: 63–70. |
|
Maina, P.K., S. Okoth, C.N. Najoroge, E. Nonda. 2009. Genetic relatedness among Fusarium species isolated from Taita Taveta Region, Kanya. Tropical and Subtropical Agroecosystems 11: 337–345. |
|
McCormic, S.P., A.M. Stanley, N.A. Stover, N.J. Alexander. 2011. Trichothecenes: from simple to complex mycotoxins. Toxins 3: 802–814. |
|
McMullen, M., R. Jonem, D. Gallenberg. 1997. Scab of wheat and barley: A re-emerging disease of devastating impact. Plant Disease 81: 1340–1348. |
|
Monds, R.D., M.G. Cromey, D.R. Lauren, M. di Menna, J. Marshall. 2005. Fusarium graminearum, F. cortaderiae and F. pseudograminearum in New Zealand: Molecular phylogenetic analysis, mycotoxin chemotypes and co-existence of species. Mycological Research 109: 410–420. |
|
Mueller, U.G., L.L. Wolfenbarger. 1999. AFLP genotyping and fingerprinting. Tree 14: 389–393. |
|
Narayanasamy, P. 2008. Molecular Biology in Plant Pathogenesis and Disease Management: Microbial Plant Pathogens, 1st ed., Volume 1. 249p. Springer: New York, USA. |
|
Nicholson, P., D.R. Simpson, G. Weston, H.N. Rezanoor, A.K. Lees, D.W. Parry, D. Joyce. 1998. Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiological and Molecular Plant Pathology 53: 17–37. |
|
Nielsen, L.K., J.D. Jensen, A. Rodríguez, L.N. Jorgensen, A.F. Justesen. 2012. TRI12 based quantitative real-time 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. |
|
O'Donnell, K., H.C. Kistler, B.K. Tacke, H.H. Casper. 2000. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proceedings of the National Academy of Sciences 90: 7905–7910. |
|
O'Donnell, K., T.J. Ward, D.M. Geiser, H.C. Kistler, T. Aoki. 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. |
|
O'Donnell, K., B.J. Sarver, M. Brandt, D.C. Chang, J. Noble-Wang, B.J. Park, D.A. Sutton, L. Benjamin, M. Lindsley, A. Padhue, D.M. Geiser, T.J. Ward. 2007. Phylogenetic diversity and microsphere array-based genotyping of human pathogenic fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. Journal of Clinical Microbiology 45: 2235–2248. |
|
O'Donnell, K., T.J. Ward, D. Aberra, H.C. Kistler, T. Aoki, N. Orwig, M. Kimura, S. Bjornstad, S.S. Klemsdal. 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: 1514–1522. |
|
Ouellet, T., K.A. Seifert. 1993. Genetic characterization of Fusarium graminearum strains using RAPD and PCR amplification. Phytopathology 83: 1003–1007. |
|
Panthi, A. 2012. Characterization of chemotype and aggressiveness of Nebraska isolates of Fusarium graminearum. Ph.D. Thesis. Theses, Dissertations, & Student Scholarship: Agricultural Leadership, Education & Communication Department, University of Nebraska-Lincoln, United States of America, 93 p. |
|
Pasquali, M., F. Giraud, C. Brochot, E. Cocco, L. Hoffmann, T. Bohr. 2010. Genetic Fusarium chemotyping as a useful tool for predicting nivalenol contamination in winter wheat. International Journal of Food Microbiology 137: 246–253. |
|
Puri, K.D., S. Zhong. 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. |
|
Qu, B. 2002. Genetic diversity of Fusarium graminearum in China and its comparison with the isolates from of Nepal, Europe, and USA. Ph.D. Thesis, Hauzhong Agricultural University, Wuhan, China, 93 p. |
|
Qu, B., H.P. Li, J.B. Zhang, T. Huang, J. Carter, Y.C. Liao, P. Nicholson. 2008a. Comparison of genetic diversity and pathogenicity of Fusarium head blight pathogens from China and Europe by SSCP and seedling assays on wheat. Plant Pathology 57: 642–651. |
|
Qu, B., H.P. Li, J.P Zhang; Y.B. Xu, T. Huang, A.B. Wu, C.S. Zhao, J. Carter, P. Nicholson, Y.C. Liao. 2008b. Geographic distribution and genetic diversity of Fusarium graminearum and F. asiaticum on wheat spikes throughout China. Plant Pathology 57: 15–24. |
|
Rep, M., H.C. Kistler. 2010. The genomic organization of plant pathogenicity in Fusarium species. Current Opinion in Plant Biology 13: 420–426. |
|
Sampietro, D.A., M.E. Ficoseco, C.M. Jimenez, M.A.Vattuone, C.A.Catalán. 2012. Trichothecene genotypes and chemotypes in Fusarium graminearum complex strains isolated from corn fields of northwest Argentina. International Journal of Food Microbiology 153: 229-233. |
|
Sarver, B.A.J., T.J. Ward, L.R. Gale, K. Bronz, C. Kistler, T. Aoki, P. Nicholson, J. Carter, K. O'Donnell. 2011. Novel Fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genetics and Biology 48: 1096–1107. |
|
Schilling, A.G., E.M. Möller, H.H. Geiger. 1996. Polymerase chain reaction-based assays for species-specific detection of Fusarium culmorum, F. graminearum, and F. avenaceum. Molecular Plant Pathology 86: 515–522. |
|
Schwabe, S.H. 1839. In Flora Anhalt 2: Cryptogamia. 425p. Reimer, Berlin. |
|
Scoz, L.B., P. Astolfi, D.S. Reartes, D.G. Schmale III, M.G. Moraes, E.M. Del Ponte. 2009. Trichothecene mycotoxin genotypes of Fusarium graminearum sensu stricto and Fusarium meridionale in wheat from Southern Brazil. Plant Pathology 58: 344–351. |
|
Sivaramakrishnan, S., S. Kannan, S.D. Singh. 2002. Genetic variability of Fusarium wilt pathogen isolates of chickpea (Cicer arietinum L.) assessed by molecular markers. Mycopathologia 155: 171–178. |
|
Spolti, P., E.M. Del Ponte, Y. Dong, J.A. Cumming, G.C. Bergstrom. 2014. Triazole sensitivity in a contemporary population of Fusarium graminearum from New York wheat and competitiveness of a tebuconazole-resistant isolate. Plant Disease 98: 607–613. |
|
Stępień, Ł., D. Popiel, G. Koczyk, J. Chełkowski. 2008. Wheat-infecting Fusarium species in Poland – their chemotypes and frequencies revealed by PCR assay. Journal of Applied Genetics 49: 433–441. |
|
Starkey, D.E., T.J. Ward, T. Aoki, L.R. Gale, H.C. Kistler, D.M. Geiser, H. Suga, B. Tóth, J. Varga, K. O'Donnell. 2007. Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genetics and Biology 44: 1191–1204. |
|
Suchorzyńska, M., A. Misiewicz. 2009. Mycotoxigenic phytopathogenic fungi of Fusarium genus and their identification by PCR techniques. Postępy Mikrobiologii 48: 221–230 (in Polish). |
|
Suga, H., L.R. Gale, H.C. Kistler. 2004. Development of VNTR markers for two Fusarium graminearum clade species. Molecular Ecology Notes 4: 468–470. |
|
Suga, H., G.W. Karugia, T. Ward, L.R. Gale, K. Tomimura, T. Nakajima, A. Miyasaka, S. Koizumi, K. Kageyama, M. Hyakumachi. 2008. Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology 98: 159–166. |
|
Szécsi, A., T. Bartók, M. Varga, D. Magyar, Á. Mesterházy. 2005. Determination of trichothecene chemotypes of Fusarium graminearum strains isolated in Hungary. Journal of Phytopathology 153: 445–448. |
|
Talas, F., H.K. Parzies, T. Miedaner. 2011. Diversity in genetic structure and chemotype composition of Fusarium graminearum sensu stricto populations causing wheat head blight in individual fields in Germany. Europen Journal of Plant Pathology 131: 39–48. |
|
Talas, F., T. Würschum, J.C. Reif, H.K. Parzies, T. Miedaner. 2012. Association of single nucleotide polymorphic sites in candidate genes with aggressiveness and deoxynivalenol production in Fusarium graminearum causing wheat head blight. BMC Genetics 13 (14). http://www.biomedcentral.com/1471-2156/13/14, accessed March 2014. |
|
Tóth, B., Á. Mesterházy, Z. Horváth, T. Bartók, M. Varga, J. Varga. 2005. Genetic variability of central European isolates of the Fusarium graminearum species complex. European Journal of Plant Pathology 113: 35-45. |
|
Umpiérrez-Failache, M., G. Garmendia, S. Pereyra, A. Rodríguez-Haralambides, T.J. Ward, S. Vero. 2013. Regional differences in species composition and toxigenic potential among Fusarium head blight isolates from Uruguay indicate a risk of nivalenol contamination in new wheat production areas. International Journal of Food Microbiology 166: 135–140. |
|
Waalwijk, C., P. Kastelein, I. de Vries, Z. Kerenyi, T. van der Lee, T. Hesselink, J. Köhl, G Kema. 2003. Major changes in Fusarium spp. in wheat in the Netherlands. European Journal of Plant Pathology 109: 743–754. |
|
Waalwijk, C., T. van der Lee, I. de Vries, T. Hesselink, J. Arts, G.H.J. Kema. 2004. Synteny in toxigenic Fusarium species: The fumonisin gene cluster and the mating type region as examples. European Journal of Plant Pathology 110: 533–544. |
|
Wang, J.H., H.P. Li, B. Qu, J.B. Zhang, T. Huang, F.F. Chen, Y.C. Liao. 2008. Development of a generic PCR detection of 3-acetyldeoxynivalenol, 15-acetyldeoxynivalenol- and nivalenol-chemotypes of Fusarium graminearum clade. International Journal of Molecular Sciences 9: 2495–2504. |
|
Wang, J.H., M. Ndoye, J.B. Zhang, H.P. Li, Y.C. Liao. 2011. Population structure and genetic diversity of the Fusarium graminearum species complex. Toxins 3: 1020–1037. |
|
Ward, T.J., J.P. Bielawski, H.C. Kistler, E. Sullivan, K. O'Donnel. 2002. Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. PNAS 99 (149): 9278-9283. |
|
Ward, T.J., R.M. Clear, A.P. Rooney, K. O'Donnell, D. Gaba, S. Patrick, D.E. Starkey, J. Gilbert, D.M. Geiser. 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. |
|
Yang, L., T. van der Lee, X. Yang, D. Yu, C. Waalwijk. 2008. Fusarium populations on Chinese barley show a dramatic gradient in mycotoxin profiles. Phytopathology 98: 719–727. |
|
Yli-Mattila, T. 2010. Ecology and evolution of toxigenic Fusarium species in cereals in northern Europe and Asia. Journal of Plant Pathology 92: 7-18. |
|
Yli-Mattila, T., T. Gagkaeva, T.J. Ward, T. Aoki, H.C. Kistler, K. O'Donnell. 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. |
|
Yoder, W.T., L.M. Christianson. 1998. Species-specific primers resolve members of Fusarium section Fusarium. Taxonomic status of the edible "Quorn" fungus reevaluated. Fungal Genetics and Biology 23: 68–80. |
|
Zeller, K.A., R.L. Bowden, J.F. Leslie. 2003. Diversity of epidemic populations of Gibberella zeae from small quadrats in Kansas and North Dakota. Phytopathology 93: 874–880. |
|
Zeller, K.A., R.L. Bowden, J.F. Leslie. 2004. Population differentiation and recombination in wheat scab populations of Gibberella zeae from the United States. Molecular Ecology 13: 563–571. |
|
Zhang, H., Z. Zhang, T. van der Lee, W.Q. Chen, J. Xu, J.S. Xu, L. Yang, D. Yu, C. Waalwijk, J. Feng. 2010. Population genetic analyses of Fusarium asiaticum populations from barley suggest a recent shift favoring 3ADON producers in southern China. Phytopathology 100: 328–336. |
|
Zhang, H, T. Van der Lee, C. Waalwijk, W. Chen, W. Xu, J. Xu, Y. Zhang, J. Feng. 2012. Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. Plos One 7(2). e31722. doi:10.1371/journal.pone.0031722. |
|
Zhang, J.B., H.P. Li, F.J. Dang, B. Qu, Y.B. Xu, C.S. Zhao, Y.C. Liao. 2007. Determination of the trichothecene mycotoxin chemotypes and associated geographical distribution and phylogenetic species of the Fusarium graminearum clade from China. Mycological Research 111: 967–975. |