Abstract
Fusarium graminearum is the primary causal agent of Fusarium head blight of wheat in Argentina. This disease affects yield losses and quality of grains, reducing the wheat end-use, also causing mycotoxin contamination. In this study, the genetic variability and deoxynivalenol (DON) potential/production of F. graminearum sensu stricto (s.s.) isolates obtained from wheat samples of the 2009, 2010, and 2011 growing seasons from a single location in Argentina were evaluated. The genetic variability detected using inter-simple sequence repeat (ISSR) was analyzed in relation to the in vitro deoxynivalenol production, the main monitored and quantified mycotoxin according to the current regulations for the international marketing of cereals. Of the 68 F. graminearum s.s. isolates obtained in this study, 95 % showed a different banding pattern with ISSR molecular markers and a high variability was detected within the population. However, no clustering was found in relation with year or DON production. All isolates amplify for the DON-related gene and a high variability in DON production was observed among the isolates, with production values between non-producers and 1741 μg/g. The results suggest that the F. graminearum s.s. population varies significantly in both genetic structure and toxin production in a limited sampled area.
This is a preview of subscription content,
to check access.


References
Alvarez CL, Azcarate MP, Fernandez Pinto V (2009) Toxigenic potential of Fusarium graminearum sensu stricto isolates from wheat in Argentina. Int J Food Microbiol 135:131–135. doi:10.1016/j.ijfoodmicro.2009.07.037
Alvarez CL, Somma S, Proctor RH, Stea G, Mulè G, Logrieco AF, Fernandez Pinto V, Moretti A (2011) Genetic diversity in Fusarium graminearum from a major wheat-producing region of Argentina. Toxins (Basel) 3:1294–1309. doi:10.3390/toxins3101294
Aoki T, Ward TJ, Kistler HC, O’Donnell K (2012) Systematics, phylogeny and trichothecene mycotoxin potential of Fusarium head blight cereal pathogens. Mycotoxins 62:91–102
Astolfi P, Reynoso MM, Ramirez ML, Chulze SN, Alves TCA, Tessmann DJ, Del Ponte EM (2012) Genetic population structure and trichothecene genotypes of Fusarium graminearum isolated from wheat in southern Brazil. Plant Pathol 61:289–295. doi:10.1111/j.1365-3059.2011.02515.x
Boutigny AL, Ward TJ, Van Coller GJ, Flett B, Lamprecht SC, O’Donnell K, Viljoen A (2011) Analysis of the Fusarium graminearum species complex from wheat, barley and maize in South Africa provides evidence of species-specific differences in host preference. Fungal Genet Biol 48:914–920. doi:10.1016/j.fgb.2011.05.005
Boutigny AL, Ward TJ, Ballois N, Iancu G, Ioos R (2014) Diversity of the Fusarium graminearum species complex on French cereals. Eur J Plant Pathol 138:133–148. doi:10.1007/s10658-013-0312-6
Burgess LW, Summerell BA, Bullock S, Gott KP, Backhouuse D (1994) Laboratory manual for Fusarium research, 3rd edn. University of Sydney, Sydney
Burlakoti RR, Neate SM, Adhikari TB, Gyawali S, Salas B, Steffenson BJ, Schwarz PB (2011) Trichothecene profiling and population genetic analysis of Gibberella zeae from Barley in North Dakota and Minnesota. Phytopathology 101:687–695. doi:10.1094/PHYTO-04-10-0101
Cainong JC, Bockus WW, Feng Y, Chen P, Qi L, Sehgal SK, Danilova TV, Koo DH, Friebe B, Gill BS (2015) Chromosome engineering, mapping, and transferring of resistance to Fusarium head blight disease from Elymus tsukushiensis into wheat. Theor Appl Genet 128:1019–1027. doi:10.1007/s00122-015-2485-1
Calzada J (2014) Publicaciones: Informativo Semanal (N° 1687): Argentina y su posicionamiento en el mercado mundial de granos, aceites y subproductos. Bolsa de Comercio de Rosario. Available online at: http://www.bcr.com.ar/Publicaciones/Informativo%20semanal/bcr2014_12_05.pdf. Accessed 16 July 2015
Castañares E, Dinolfo MI, Moreno MV, Berón C, Stenglein SA (2013) Fusarium cerealis associated with barley seeds in Argentina. J Phytopathol 161:586–589. doi:10.1111/jph.12097
Castañares E, Ramirez Albuquerque D, Dinolfo MI, Fernandez Pinto V, Patriarca A, Stenglein SA (2014) Trichothecene genotypes and production profiles of Fusarium graminearum isolates obtained from barley cultivated in Argentina. Int J Food Microbiol 179:57–63. doi:10.1016/j.ijfoodmicro.2014.03.024
Castañares E, Dinolfo MI, Del Pontec EM, Pan D, Stenglein SA (2015) Species composition and genetic structure of Fusarium graminearum species complex populations affecting the main barley growing regions of South America. Plant Pathol. Accepted for publication
Chandler EA, Simpson DR, Thomsett MA, Nicholson P (2003) Development of PCR assays to Tri7 and Tri13 trichothecene biosynthetic genes, and characterisation of chemotypes of Fusarium graminearum, Fusarium culmorum and Fusarium cerealis. Physiol Mol Plant Pathol 62:355–367. doi:10.1016/S0885-5765(03)00092-4
Cooney JM, Lauren DR, di Menna ME (2001) Impact of competitive fungi on trichothecene production by Fusarium graminearum. J Agric Food Chem 49:522–526. doi:10.1021/jf0006372
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. J Sci Food Agric 95:540–551. doi:10.1002/jsfa.6772
Del Ponte EM, Spolti P, Ward TJ, Gomes LB, Nicolli CP, Kuhnem PR, Silva CN, Tessmann DJ (2015) Regional and field-specific factors affect the composition of fusarium head blight pathogens in subtropical no-till wheat agroecosystem of Brazil. Phytopathology 105:246–254. doi:10.1094/PHYTO-04-14-0102-R
Dinolfo MI, Stenglein SA, Moreno MV, Nicholson P, Jennings P, Salerno GL (2010) ISSR markers detect high genetic variation among Fusarium poae isolates from Argentina and England. Eur J Plant Pathol 127:483–491. doi:10.1007/s10658-010-9613-1
Galich MTV (1996) Fusarium head blight in Argentina. In: Dubin HJ, Gilchrist L, Reeves J, McNab A (eds) Fusarium head scab: global status and future prospects, 1st edn. Centro Internacional de Mejoramiento de Maiz y Trigo, México, pp 19–28
Gerlach W, Nirenberg H (1982) The genus Fusarium—a pictorial atlas. Mitt Biol Bundesanst Land Forstwirtsch (Berlin-Dahlem) 209:1–406
Goswami RS, Kistler HC (2005) Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 95:1397–1404. doi:10.1094/PHYTO-95-1397
Guo XW, Fernando WGD, Seow-Brock HY (2008) Population structure, chemotype diversity, and potential chemotype shifting of Fusarium graminearum in wheat fields of Manitoba. Plant Dis 92:756–762. doi:10.1094/PDIS-92-5-0756
Hope R, Aldred D, Magan N (2005) Comparison of environmental profiles for growth and deoxynivalenol production by Fusarium culmorum and F. graminearum on wheat grain. Lett Appl Microbiol 40:295–300. doi:10.1111/j.1472-765X.2005.01674.x
Karugia GW, Suga H, Gale LR, Nakajima T, Tomimura K, Hyakumachi M (2009) Population structure of the Fusarium graminearum species complex from a single Japanese wheat field sampled in two consecutive years. Plant Dis 93:170–174. doi:10.1094/PDIS-93-2-0170
Kikot GE, Moschini R, Consolo VF, Rojo R, Salerno G, Hours RA, Gasoni L, Arambarri AM, Alconada TM (2011) Occurrence of different species of Fusarium from wheat in relation to disease levels predicted by a weather-based model in Argentina pampas region. Mycopathologia 171:139–149. doi:10.1007/s11046-010-9335-0
Lechoczki-Krsjak S, Tóth B, Kótai C, Martonosi I, Farády L, Kondrák L, Szabó-Hevér A, Mesterházy A (2008) Chemical control of fhb in wheat with different nozzle types and fungicides. Cereal Res Commun 36:677–681. doi:10.1556/CRC.36.2008.Suppl.B.59
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing, Ames
Leslie JF, Anderson LL, Bowden RL, Lee YW (2007) Inter- and intra-specific genetic variation in Fusarium. Int J Food Microbiol 119:25–32. doi:10.1016/j.ijfoodmicro.2007.07.059
Llorens A, Hinojo MJ, Mateo R, González-Jaén MT, Valle-Algarra FM, Logrieco A, Jiménez M (2006) Characterization of Fusarium spp. isolates by PCR-RFLP analysis of the intergenic spacer region of the rRNA gene (rDNA). Int J Food Microbiol 106:297–306. doi:10.1016/j.ijfoodmicro.2005.09.005
Lori GA, Sisterna MN, Haidukowski M, Rizzo I (2003) Fusarium graminearum and deoxynivalenol contamination in the durum wheat area of Argentina. Microbiol Res 158:29–35. doi:10.1078/0944-5013-00173
Malbrán I, Mourelos CA, Girotti JR, Aulicino MB, Balatti PA, Lori GA (2012) Aggressiveness variation of Fusarium graminearum isolates from Argentina following point inoculation of field grown wheat spikes. Crop Prot 42:234–243. doi:10.1016/j.cropro.2012.05.025
Malbrán I, Mourelos CA, Girotti JR, Balatti PA, Lori GA (2014) Toxigenic capacity and trichothecene production by Fusarium graminearum isolates from Argentina and their relationship with aggressiveness and fungal expansion in the wheat spike. Phytopathology 104:357–364. doi:10.1094/PHYTO-06-13-0172-R
Matny ON (2015) Fusarium head blight and crown rot on wheat & barley: losses and health risks. Adv Plants Agric Res 2:00039. doi:10.15406/apar.2015.02.00039
Mishra PK, Fox RTV, Culham A (2003) Inter-simple sequence repeat and aggressiveness analyses revealed high genetic diversity, recombination and long-range dispersal in Fusarium culmorum. Ann Appl Biol 143:291–301. doi:10.1111/j.1744-7348.2003.tb00297.x
Mishra PK, Tewari JP, Clear RM, Turkington TK (2004) Molecular genetic variation and geographical structuring in Fusarium graminearum. Ann Appl Biol 145:299–307. doi:10.1111/j.1744-7348.2004.tb00387.x
Moschini RC, Fortugno C (1996) Predicting wheat head blight incidence using models based on meteorological factors in Pergamino, Argentina. Eur J Plant Pathol 102:211–218. doi:10.1007/BF01877959
Mourelos CA, Malbrán I, Balatti PA, Ghiringhelli PD, Lori GA (2014) Gramineous and non-gramineous weed species as alternative hosts of Fusarium graminearum, causal agent of Fusarium head blight of wheat, in Argentina. Crop Prot 65:100–104. doi:10.1016/j.cropro.2014.07.013
Mugrabi de Kuppler AL, Steiner U, Sulyok M, Krska R, Oerke EC (2011) Genotyping and phenotyping of Fusarium graminearum isolates from Germany related to their mycotoxin biosynthesis. Int J Food Microbiol 151:78–86. doi:10.1016/j.ijfoodmicro.2011.08.006
Nicholson P, Simpson DR, Weston G, Rezanoor HN, Lees AK, Parry DW, Joyce D (1998) Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiol Mol Plant Pathol 53:17–37. doi:10.1006/pmpp.1998.0170
O’Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci U S A 97:7905–7910. doi:10.1073/pnas.130193297
O’Donnell K, Ward TJ, Geiser DM, Corby Kistler H, Aoki T (2004) Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet Biol 41:600–623. doi:10.1016/j.fgb.2004.03.003
O’Donnell K, Ward TJ, Aberra D, Kistler HC, Aoki T, Orwig N, Kimura M, Bjørnstad Å, Klemsdal SS (2008) Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genet Biol 45:1514–1522. doi:10.1016/j.fgb.2008.09.002
Osborne LE, Stein JM (2007) Epidemiology of Fusarium head blight on small-grain cereals. Int J Food Microbiol 119:103–108. doi:10.1016/j.ijfoodmicro.2007.07.032
Palazzini JM, Ramirez ML, Torres AM, Chulze SN (2007) Potential biocontrol agents for Fusarium head blight and deoxynivalenol production in wheat. Crop Prot 26:1702–1710. doi:10.1016/j.cropro.2007.03.004
Pan D, Calero N, Mionetto A, Bettucci L (2013) Trichothecene genotypes of Fusarium graminearum from wheat in Uruguay. Int J Food Microbiol 162:120–123. doi:10.1016/j.ijfoodmicro.2013.01.002
Pestka JJ (2007) Deoxynivalenol: toxicity, mechanisms and animal health risks. Anim Feed Sci Technol 137:283–298. doi:10.1016/j.anifeedsci.2007.06.006
Pestka JJ, Smolinski AT (2005) Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health B Crit Rev 8:39–69. doi:10.1080/10937400590889458
Qiu J, Xu J, Shi J (2014) Molecular characterization of the Fusarium graminearum species complex in Eastern China. Eur J Plant Pathol 139:811–823. doi:10.1007/s10658-014-0435-4
Ramirez ML, Chulze S, Magan N (2006a) Temperature and water activity effects on growth and temporal deoxynivalenol production by two Argentinean strains of Fusarium graminearum on irradiated wheat grain. Int J Food Microbiol 106:291–296. doi:10.1016/j.ijfoodmicro.2005.09.004
Ramirez ML, Reynoso MM, Farnochi MC, Chulze S (2006b) Vegetative compatibility and mycotoxin chemotypes among Fusarium graminearum (Gibberella zeae) isolates from wheat in Argentina. Eur J Plant Pathol 115:139–148. doi:10.1007/s10658-006-0009-1
Ramirez ML, Reynoso MM, Farnochi MC, Torres AM, Leslie JF, Chulze SN (2007) Population genetic structure of Gibberella zeae isolated from wheat in Argentina. Food Addit Contam 24:1115–1120. doi:10.1080/02652030701546487
Reynoso MM, Ramirez ML, Torres AM, Chulze SN (2011) Trichothecene genotypes and chemotypes in Fusarium graminearum strains isolated from wheat in Argentina. Int J Food Microbiol 145:444–448. doi:10.1016/j.ijfoodmicro.2011.01.020
Rohlf FJ (1998) NTSYSpc. Numerical taxonomy and multivariate analysis system, version 2.0. Applied Biostatistics, Exeter Software, New York
Sampietro DA, Marín P, Iglesias J, Presello DA, Vattuone MA, Catalan CAN, Gonzalez Jaen MT (2010) A molecular based strategy for rapid diagnosis of toxigenic Fusarium species associated to cereal grains from Argentina. Fungal Biol 114:74–81. doi:10.1016/j.mycres.2009.10.008
Sarver BAJ, Ward TJ, Gale LR, Broz K, Kistler HC, Aoki T, Nicholson P, Carter J, O’Donnell K (2011) Novel Fusarium head blight pathogens from Nepal and Louisiana revealed by multilocus genealogical concordance. Fungal Genet Biol 48:1096–1107. doi:10.1016/j.fgb.2011.09.002
Schmale DG III, Leslie JF, Zeller KA, Saleh AA, Shields EJ, Bergstrom GC (2006) Genetic structure of atmospheric populations of Gibberella zeae. Phytopathology 96:1021–1026. doi:10.1094/PHYTO-96-1021
Schneider S, Roessli D, Excoffier L (2000) Arlequin. A software for populations genetic data analysis, version 2.0. University of Geneva, Switzerland
Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Francisco
Somma S, Petruzzella AL, Logrieco AF, Meca G, Cacciola OS, Moretti A (2014) Phylogenetic analyses of Fusarium graminearum strains from cereals in Italy, and characterisation of their molecular and chemical chemotypes. Crop Pasture Sci 65:52–60. doi:10.1071/CP13314
Stenglein SA, Balatti PA (2006) Genetic diversity of Phaeoisariopsis griseola in Argentina as revealed by pathogenic and molecular markers. Physiol Mol Plant Pathol 68:158–167. doi:10.1016/j.pmpp.2006.10.001
Umpiérrez-Failache M, Garmendia G, Pereyra S, Rodríguez-Haralambides A, Ward TJ, Vero S (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. Int J Food Microbiol 166:135–140. doi:10.1016/j.ijfoodmicro.2013.06.029
van der Lee T, Zhang H, van Diepeningen A, Waalwijk C (2015) Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:453–460. doi:10.1080/19440049.2014.984244
Waalwijk C, Kastelein P, de Vries I, Kerényi Z, van der Lee T, Hesselink T, Köhl J, Kema G (2003) Major changes in Fusarium spp. in wheat in the Netherlands. Eur J Plant Pathol 109:743–754. doi:10.1007/978-94-017-1452-5_9
Xu XM, Nicholson P, Ritieni A (2007) Effects of fungal interactions among Fusarium head blight pathogens on disease development and mycotoxin accumulation. Int J Food Microbiol 119:67–71. doi:10.1016/j.ijfoodmicro.2007.07.027
Xu XM, Nicholson P, Thomsett MA, Simpson D, Cooke BM, Doohan FM, Brennan J, Monaghan S, Moretti A, Mule G, Hornok L, Beki E, Tatnell J, Ritieni A, Edwards SG (2008) Relationship between the fungal complex causing Fusarium head blight of wheat and environmental conditions. Phytopathology 98:69–78. doi:10.1094/PHYTO-98-1-0069
Zeller KA, Bowden RL, Leslie JF (2003) Diversity of epidemic populations of Gibberella zeae from small quadrats in Kansas and North Dakota. Phytopathology 93:874–880. doi:10.1094/PHYTO.2003.93.7.874
Zhao Y, Selvaraj JN, Xing F, Zhou L, Wang Y, Song H, Tan X, Sun L, Sangare L, Folly YME, Liu Y (2014) Antagonistic action of Bacillus subtilis strain SG6 on Fusarium graminearum. PLoS One 9(3):e92486. doi:10.1371/journal.pone.0092486
Acknowledgments
We thank Consejo Nacional de Investigaciones Científicas y Tecnológicas (grants PIP 0925 and PIP 0551) and FONCYT PICT PICT-2011-0851 and 030/2011 for financial support, and the technical assistance of Esteban González.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Section Editor: Marc Stadler
Rights and permissions
About this article
Cite this article
Ortega, L.M., Dinolfo, M.I., Astoreca, A.L. et al. Molecular and mycotoxin characterization of Fusarium graminearum isolates obtained from wheat at a single field in Argentina. Mycol Progress 15, 1 (2016). https://doi.org/10.1007/s11557-015-1147-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-015-1147-7