Morpho-Molecular Identification, Pathogenicity Variation, Mating Biology, and Fumonisin Production of Fusarium Species in Zea mays L.

Narges Atabaki, Vahid Rahjoo, Mohamed M. Hanafi, Rambod Abiri, Hamidreza Z. Zadeh, Majid Zamani, Mahbod Sahebi, Alireza Valdiani


Fusarium verticillioides and Fusarium proliferatum cause a wide range of maize diseases.  These fungi produce dangerous mycotoxins, such as fumonisin B1, which are important threats to humans and animals. Given this predicament, the present study aimed to identify the fungi both molecular-morphologically and also investigate the pathogenicity variation and mating type of 41 Fusarium strains in maize (Zea mays L.) samples with sifting their fumonisin contents.  Furthermore, species-specific primers for the molecular identification of distinct strains amplified 2 fragments of 578 and 800 bp in Fusarium verticillioides, while a single 585 bp band was amplified in Fusarium proliferatum.  Accordingly, 24 isolates out of 41 were identified as F. verticillioides, and 13 isolates were identified as F. proliferatum.  The fumonisin-producing and non-producing Fusarium strains were identified using the VERTF-1/VERTF-2 primers.  A total of 24 isolates of F. verticillioides were positively scored based on the amplification of a single 400 bp fragment.  The highest and lowest fumonisin content, as measured using an enzyme-linked immunosorbent assay (ELISA), belonged to strains MS1 and MG3, respectively, and ranged from 960-12673 and 4.07-23 ppm, respectively.  Additionally, the mating type test showed that the sexual form of the studied Fusarium species could possibly belong to the A and D mating populations.  In vivo and in vitro pathogenicity tests revealed a high susceptibility.


Fusarium verticillioides; Fusarium proliferatum; fumonisin; ELISA


Abiri, R., A. Valdiani, M. Maziah, N. A. Shaharuddin, M. Sahebi, Z. N. B. Yusof, N. Atabaki and D. Talei. 2015. A critical review of the concept of transgenic plants: Insights into pharmaceutical biotechnology and molecular farming. Current Issues on Molecular Research, 18: 21-42.

Alizadeh, A. M., G. Roshandel, S. Roudbarmohammadi, M. Roudbary, H. Sohanaki, S. A. Ghiasian, A. Taherkhani, S. Semnani and M. Aghasi. 2012. Fumonisin B1 contamination of cereals and risk of esophageal cancer in a high risk area in northeastern Iran. Asian Pacific Journal of Cancer Prevention, 13: 2625-2628.

Babič, M. N., P. Zalar, B. Ženko, H.-J. Schroers, S. Džeroski and N. Gunde-Cimerman. 2015. Candida and Fusarium species known as opportunistic human pathogens from customer-accessible parts of residential washing machines. Fungal Biology, 119: 95-113.

Bentley, A. R., J. F. Leslie, E. C. Y. Liew, L. W. Burgess and B. A. Summerell. 2008. Genetic structure of Fusarium pseudograminearum populations from the Australian grain belt. Phytopathology, 98: 250-255.

Burger, H. M., G. S. Shephard, W. Louw, J. P. Rheeder and W. C. A. Gelderblom. 2013. The mycotoxin distribution in maize milling fractions under experimental conditions. International Journal of Food Microbiology, 165: 57-64.

Bush, B. J., M. L. Carson, M. A. Cubeta, W. M. Hagler and G. A. Payne. 2004. Infection and Fumonisin Production by Fusarium verticillioides in developing maize kernels. Phytopathology, 94: 88-93.

Chelkowski, J. 2014. Fusarium: Mycotoxins, Taxonomy, Pathogenicity. Elsevier.

Ciarmiello, L. F., P. Woodrow, A. Fuggi, G. Pontecorvo and P. Carillo. 2011. Plant Genes for Abiotic Stress, Abiotic Stress in Plants-Mechanisms and Adaptations. InTech Publishers.

Cumagun, C. J. R. 2008. Female fertility and mating type distribution in a Philippine population of Fusarium verticillioides. Journal of Applied Genetics, 49: 123-126.

Da Silva, V. N., F. M. C. Fernandes, A. Cortez, D. H. B. Ribeiro, A. P. de Almeida, R. H. Hassegawa and B. Corrêa. 2006. Characterization and genetic variability of Fusarium verticillioides strains isolated from corn and sorghum in Brazil based on fumonisins production, microsatellites, mating type locus, and mating crosses. Canadian Journal of Microbiology, 52: 798-804.

Danielsen, Meyer and J. Funck. 1998. Genetic characteristics of Fusarium verticillioides isolates from maize in Costa Rica. Plant Pathology, 47: 615-622.

De Curtis, F., V. De Cicco, M. Haidukowski, M. Pascale, S. Somma and A. Moretti. 2011. Effects of agrochemical treatments on the occurrence of Fusarium ear rot and fumonisin contamination of maize in Southern Italy. Field Crops Research, 123: 161-169.

Desjardins, A. E., G. P. Munkvold, R. D. Plattner and R. H. Proctor. 2002. FUM1-A gene required for fumonisin biosynthesis but not for maize ear rot and ear infection by Gibberella moniliformis in field tests. Molecular Plant-Microbe Interactions, 15: 1157-1164.

Gargees, M. T. and A. M. Shareef. 2009. Reducing liver aflatoxin M1 residues in chicks with mycofix plus 3.0 during aflatoxicosis. Iraqi Journal of Veterinary Sciences, 23.

Geiser, D. M., M. del Mar Jiménez-Gasco, S. Kang, I. Makalowska, N. Veeraraghavan, T. J. Ward, N. Zhang, G. A. Kuldau and K. O’Donnell. 2004. Fusarium-ID v. 1.0: A DNA sequence database for identifying Fusarium. Molecular diversity and PCR-detection of toxigenic Fusarium species and ochratoxigenic fungi. Springer Netherlands, p. 473-479.

Harrigan, W. F. 1998. Laboratory Methods in Food Microbiology. Gulf Professional Publishing.

Hsuan, H., L. Zakaria and B. Salleh. 2010. Characterization of Fusarium isolates from rice, sugarcane and maize using RFLP-IGS. Journal of Plant Protection Research, 50.

Ingle, A., A. Gade, S. Pierrat, C. Sonnichsen and M. Rai. 2008. Mycosynthesis of silver nanoparticles using the fungus Fusarium acuminatum and its activity against some human pathogenic bacteria. Current Nanoscience, 4: 141-144.

Karami-Osboo, R., M. Mirabolfathi and F. Aliakbari. 2010. Natural deoxynivalenol contamination of corn produced in Golestan and Moqan areas in Iran. Journal of Agricultural Science and Technology, 12: 233-239.

Karbancioglu-Guler, F. and D. Heperkan. 2009. Comparison of enzyme linked immunoassay and high performance liquid chromatography for determination of fumonisin in dried figs. Zbornik Matice srpske za prirodne nauke: 37-43.

Kim, J.-A., G. K. Agrawal, R. Rakwal, K.-S. Han, K.-N. Kim, C.-H. Yun, S. Heu, S.-Y. Park, Y.-H. Lee and N.-S. Jwa. 2003. Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signalling pathways and development. Biochemical and Biophysical Research Communications, 300: 868-876.

King, S. B. 1981. Time of infection of maize Kernels by Fusarium moniliforme and Cephalosporium acremonium. Phytopathology, 71: 796.

Kouadio, J. H., S. D. Dano, S. Moukha, T. A. Mobio and E. E. Creppy. 2007. Effects of combinations of Fusarium mycotoxins on the inhibition of macromolecular synthesis, malondialdehyde levels, DNA methylation and fragmentation, and viability in Caco-2 cells. Toxicon, 49: 306-317.

Kovacevic, T., J. Levic, S. Stankovic and J. Vukojevic. 2013. Mating populations of Gibberella fujikuroi (Sawada) S. Its species complex isolating from maize, sorghum and wheat in Serbia. Genetika, 45: 749-760.

Kuhnem, P. R., P. Spolti, E. M. Del Ponte, J. A. Cummings and G. C. Bergstrom. 2015. Trichothecene genotype composition of Fusarium graminearum not differentiated among isolates from maize stubble, maize ears, wheat spikes, and the atmosphere in New York. Phytopathology, 105: 695-699.

Leslie, J. F. and K. K. Klein. 1996. Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics, 144: 557-567.

Leslie, J. F. and B. A. Summerell. 2008. The Fusarium Laboratory Manual. John Wiley and Sons.

Lim, C. J., J. E. Hwang, H. Chen, J. K. Hong, K. A. Yang, M. S. Choi, K. O. Lee, W. S. Chung, S. Y. Lee and C. O. Lim. 2007. Over-expression of the Arabidopsis DRE/CRT-binding transcription factor DREB2C enhances thermotolerance. Biochemical and Biophysical Research Communications, 362: 431-436.

Lim, S.-H., S.-H. Yun and Y.-W. Lee. 2001. Mating behavior, mycotoxin production, and vegetative compatibility of Gibberella fujikuroi species complex from sorghum in Korea. The Plant Pathology Journal, 17: 276-280.

Melake-Berhan, A., L. G. Butler, G. Ejeta and A. Menkir. 1996. Grain mold resistance and polyphenol accumulation in sorghum. Journal of Agricultural and Food Chemistry, 44: 2428-2434.

Minervini, F., A. Giannoccaro, A. Cavallini and A. Visconti. 2005. Investigations on cellular proliferation induced by zearalenone and its derivatives in relation to the estrogenic parameters. Toxicology Letters, 159: 272-283.

Mulè, G., A. Susca, G. Stea and A. Moretti. 2004. A species-specific PCR assay based on the calmodulin partial gene for identification of Fusarium verticillioides, F. proliferatum and F. subglutinans. Molecular Diversity and PCR-detection of Toxigenic Fusarium Species and Ochratoxigenic Fungi. Springer Netherlands, p. 495-502.

Nelson, P. E., T. A. Toussoun and W. F. O. Marasas. 1983. Fusarium species, An illustrated manual for identification.

Okamoto, S., K. Furuya, S. Nozaki, K. Aoki and H. Niki. 2013. Synchronous activation of cell division by light or temperature Stimuli in the dimorphic yeast Schizosaccharomyces japonicus. Eukaryotic Cell, 12: 1235-1243.

Peng, X.-C., D.-W. Qiu, H.-M. Zeng, L.-H. Guo, X.-F. Yang and Z. Liu. 2014. Inducible and constitutive expression of an

elicitor gene Hrip1 from Alternaria tenuissima enhances stress tolerance in Arabidopsis. Transgenic Research, 24: 135-145.

Rahjoo, V., J. Zad, M. Javan-Nikkhah, A. M. Gohari, S. M. Okhovvat, M. R. Bihamta, J. Razzaghian and S. S. Klemsdal. 2008. Morphological and molecular identification of Fusarium isolated from maize ears in Iran. Journal of Plant Pathology: 463-468.

Reid, L. M., R. W. Nicol, T. Ouellet, M. Savard, J. D. Miller, J. C. Young, D. W. Stewart and A. W. Schaafsma. 1999. Interaction of Fusarium graminearum and F. moniliformein maize ears: Disease progress, fungal biomass and mycotoxin accumulation. Phytopathology, 89: 1028-1037.

Reid, L. M. and X. Zhu. 2005. Screening Corn for Resistance to Common Diseases in Canada. Agriculture and Agri-Food Canada.

Reyneri, A. 2006. The role of climatic condition on micotoxin production in cereal. Veterinary Research Communications, 30: 87-92.

Santiago, R., A. Cao and A. Butrón. 2015. Genetic factors involved in fumonisin accumulation in maize kernels and their implications in maize agronomic management and breeding. Toxins, 7: 3267-3296.

Seifert, K. A., T. Aoki, R. P. Baayen, D. Brayford, L. W. Burgess, S. Chulze, W. Gams, D. Geiser, J. de Gruyter, J. F. Leslie, A. Logrieco, W. F. O. Marasas, H. I. Nirenberg, K. O'Donnell, J. Rheeder, G. J. Samuels, B. A. Summerell, U. Thrane and C. Waalwijk. 2003. The Name Fusarium Moniliforme should no longer be used. Mycological Research, 107: 643-644.

Sforza, S., C. Dall'Asta and R. Marchelli. 2006. Recent advances in mycotoxin determination in food and feed by hyphenated chromatographic techniques/mass spectrometry. Mass Spectrometry Reviews, 25: 54-76.

Somma, S., C. Alvarez, V. Ricci, L. Ferracane, A. Ritieni, A. Logrieco and A. Moretti. 2010. Trichothecene and beauvericin mycotoxin production and genetic variability in Fusarium poaeisolated from wheat kernels from northern Italy. Food Additives and Contaminants: Part A, 27: 729-737.

Steenkamp, E. T., B. D. Wingfield, A. E. Desjardins, W. F. O. Marasas and M. J. Wingfield. 2002. Cryptic speciation in Fusarium subglutinans. Mycologia, 94: 1032-1043.

Summerell, B. A., L. W. Burgess, S. Bullock, D. Backhouse and N. D. Tri. 1998. Occurrence of perithecia of gibberella fujikuroi mating population a (Fusarium moniliforme) on maize stubble in northern Vietnam. Mycologia, 90: 890.

Summerell, B. A., M. H. Laurence, E. C. Y. Liew and J. F. Leslie. 2010. Biogeography and phylogeography of Fusarium: A review. Fungal Diversity, 44: 3-13.

Summerell, B. A. and J. F. Leslie. 2011. Fifty years of Fusarium: How could nine species have ever been enough? Fungal Diversity, 50: 135-144.

Summerell, B. A., B. Salleh and J. F. Leslie. 2003. A utilitarian approach to Fusarium identification. Plant Disease, 87: 117-128.

Torelli, E., G. Firrao, G. Bianchi, F. Saccardo and R. Locci. 2012. The influence of local factors on the prediction of fumonisin contamination in maize. Journal of the Science of Food and Agriculture, 92: 1808-1814.

Venturini, G., G. Assante, S. L. Toffolatti and A. Vercesi. 2011. Mating behavior of a northern Italian population of Fusarium verticillioides associated with maize. Journal of Applied Genetics, 52: 367-370.

Vigier, B., L. M. Reid, K. A. Seifert, D. W. Stewart and R. I. Hamilton. 1997. Distribution and prediction of Fusarium species associated with maize ear rot in Ontario. Canadian Journal of Plant Pathology, 19: 60-65.

Wan, L. Y. M., P. C. Turner and H. El-Nezami. 2013. Individual and combined cytotoxic effects of Fusarium toxins (deoxynivalenol, nivalenol, zearalenone and fumonisins B1) on swine jejunal epithelial cells. Food and Chemical Toxicology, 57: 276-283.

Full Text: PDF XPS

DOI: 10.33687/phytopath.007.01.2528


  • There are currently no refbacks.

Copyright (c) 2018 Narges Atabaki, Vahid Rahjoo, Mohamed M. Hanafi, Rambod Abiri, Hamidreza Z. Zadeh, Majid Zamani, Mahbod Sahebi, Alireza Valdiani

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.