Skip to main content
Log in

Isolation and characterization of Fusarium verticillioides from maize in eastern China

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

In 2012, we isolated mycotoxigenic fungi from maize kernels sourced in Jiangsu and Anhui provinces, China. Fusarium spp. accounted for most isolates detected, followed by Aspergillus and Penicillium spp. Of the Fusarium species, Fusarium verticillioides was the most prevalent, as revealed by direct PCR of DNA from kernel samples, followed by F. proliferatum and F. graminearum. Most F. verticillioides strains contained the FUM1 gene, the product of which plays a key role in fumonisin biosynthesis. In terms of mating type idiomorphs, about 80 % of all strains carried the MAT-1 allele, and 20 % carried MAT-2. The genetic structures of 192 representative F. verticillioides isolates were determined via an analysis of eight simple sequence repeat markers. This analysis revealed high-level gene diversity but low linkage disequilibrium in three populations grouped by the geographical areas in which they were collected. The three populations exhibited low-level genetic differentiation and high gene flow, indicating that geographical differences minimally influenced population differentiation; all three populations were potentially components of a larger, randomly mating population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1(1–2), 101–102.

    Article  CAS  Google Scholar 

  • Aguín, O., Cao, A., Pintos, C., Santiago, R., Mansilla, P., & Butrón, A. (2013). Occurrence of Fusarium species in maize kernels grown in northwestern Spain. Plant Pathology. doi:10.1111/ppa.12151.

    Google Scholar 

  • Arino, A., & Bullerman, L. B. (1994). Fungal colonization of corn grown in Nebraska in relation to year, genotype and growing conditions. Journal of Food Protection, 57(12), 1084–1087.

    Google Scholar 

  • Baird, R., Abbas, H. K., Windham, G., Williams, P., Baird, S., Ma, P., et al. (2008). Identification of select fumonisin forming Fusarium species using PCR application of the polyketide synthase gene and its relationship to fumonisin production in vitro. International Journal of Molecular Science, 9, 554–570.

    Article  CAS  Google Scholar 

  • Balmas, V., Santori, A., & Corazza, L. (2000). Le specie di Fusarium più comuni in Italia. Petria, 10(S1), 1–60.

    Google Scholar 

  • Bankole, S. A., & Mabekoje, O. O. (2004). Occurrence of aflatoxin and fumonisins in preharvest maize in Nigeria. Food Additives and Contaminants, 21(3), 251–255.

    Article  CAS  PubMed  Google Scholar 

  • Bottalico, A. (1998). Fusarium diseases of cereals: species complex and related mycotoxin profiles in Europe. Journal of Plant Pathology, 80(2), 85–103.

    CAS  Google Scholar 

  • Cooney, J. M., Lauren, D. R., & di Menna, M. E. (2001). Impact of competitive fungi on trichothecene production by Fusarium graminearum. Journal of Agricultural and Food Chemistry, 49(1), 522–526.

    Article  CAS  PubMed  Google Scholar 

  • Covarelli, L., Beccari, G., & Salvi, S. (2011). Infection by mycotoxigenic fungal species and mycotoxin contamination of maize grain in Umbria, central Italy. Food and Chemical Toxicology, 49(9), 2365–2369.

    Article  CAS  PubMed  Google Scholar 

  • Covarelli, L., Stifano, S., Beccari, G., Raggi, L., Lattanzio, V. M. T., & Albertini, E. (2012). Characterization of Fusarium verticillioides strains isolated from maize in Italy: Fumonisin production, pathogenicity and genetic variability. Food Microbiology, 31(1), 17–24.

    Article  CAS  PubMed  Google Scholar 

  • Desjardins, A. E., Manandhar, G., Plattner, R. D., Margos, C. M., Shrestha, K., & McCormick, S. P. (2000). Occurrence of Fusarium species and mycotoxins in Nepalese maize and wheat and the effect of traditional processing methods on mycotoxin levels. Journal of Agricultural and Food Chemistry, 48(4), 1377–1383.

    Article  CAS  PubMed  Google Scholar 

  • Dorn, B., Forrer, H. R., Jenny, E., Wettstein, F. E., Bucheli, T. D., & Vogelgsang, S. (2011). Fusarium species complex and mycotoxins in grain maize from maize hybrid trials and from grower’s fields. Journal of Applied Microbiology, 111(3), 693–706.

    Article  CAS  PubMed  Google Scholar 

  • Dowd, P. F., & Johnson, E. T. (2010). Field incidence of mycotoxins in commercial popcorn and potential environmental influences. Mycotoxin Research, 26(1), 15–22.

    Article  CAS  PubMed  Google Scholar 

  • Evanno, G., Regnaut, G., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14(8), 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., Smouse, P., & Quattro, J. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes, application to human mitochondrial DNA restriction data. Genetics, 131(1), 479–491.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Feng, Y. Z., Lu, X. H., Tao, B., Pang, M. H., Liu, Y. C., & Dong, J. G. (2011). Natural occurrence of fumonisins b1 and b2 in corn from three main production provinces in China. Journal of Food Protection, 74(8), 1374–1378.

    Article  CAS  PubMed  Google Scholar 

  • Gale, L. R., Chen, L. F., Hernick, C. A., Takamura, K., & Kistler, H. C. (2002). Population analysis of Fusarium graminearum from wheat fields in eastern China. Phytopathology, 92(12), 1315–1322.

    Article  CAS  PubMed  Google Scholar 

  • Goertz, A., Zuehlke, S., Spiteller, M., Steiner, U., Dehne, H. W., Waalwijk, C., et al. (2010). Fusarium species and mycotoxins profiles on commercial maize hybrids in Germany. European Journal of Plant Pathology, 128(1), 101–111.

    Article  CAS  Google Scholar 

  • Gong, H. Z., Ji, R., Li, Y. X., Zhang, H. Y., Li, B., Zhao, Y., et al. (2009). Occurrence of fumonisin B1 in corn from the main corn–producing areas of China. Mycopathologia, 167(1), 31–36.

    Article  PubMed  Google Scholar 

  • Hawa, M. M., Salleh, B., & Latiffah, Z. (2013). Characterization and pathogenicity of Fusarium proliferatum causing stem rot of Hylocereus polyrhizus in Malaysia. Annals of Applied Biology, 163(2), 269–280.

    Article  CAS  Google Scholar 

  • Ho, J. A., & Durst, R. A. (2000). Preparation of reagents for the determination of fumonisin B1 by flow-injection immunoanalysis. Analytica Chimica Acta, 414(1–2), 51–60.

    Article  CAS  Google Scholar 

  • IARC. (1993). IARC monographs on the evaluation of carcinogenic risks to humans. Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins, international agency for research on cancer. Lyon, 56, 397–446.

    Google Scholar 

  • Jurado, M., Marín, P., Calleja, C., Moretti, A., Vázquez, C., & González-Jaén, M. T. (2010). Genetic variability and fumonisin production by Fusarium proliferatum. Food Microbiology, 27(1), 50–57.

    Article  PubMed  Google Scholar 

  • Karugia, G. W., Suga, H., Gale, L. R., 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 Disease, 93(2), 170–174.

    Article  CAS  Google Scholar 

  • Kong, L. X., & Luo, P. C. (1995). Identification of pathogen of corn ear rot and its pathogenicity. Corrosion Science, 3, 29–31.

    Google Scholar 

  • Leslie, J. F., & Klein, K. K. (1996). Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics, 144(2), 557–567.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual. Ames: Blackwell Professional.

    Book  Google Scholar 

  • Li, S. D., & Huang, Y. X. (1998). Occurrence and damage of Diplodia ear rot of corn in Yuxi area. Plant Protection, 24, 20–21.

    CAS  Google Scholar 

  • Li, X. F., Wang, J. M., Zhang, Z. G., Gao, J. M., Hao, X. J., & He, Y. C. (2012). Isolation and identification of the Pathogen Fusarium causing maize ear rot in Shanxi Province. Journal of Shanxi Agricultural University, 32(3), 218–223.

    Google Scholar 

  • Logrieco, A., Mulé, G., Moretti, A., & Bottalico, A. (2002). Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. European Journal of Plant Pathology, 108(7), 597–609.

    Article  CAS  Google Scholar 

  • Marin, S., Magan, N., Ramos, A. J., & Sanchis, V. (2004). Fumonisin–producing strains of Fusarium: a review of their ecophysiology. Journal of Food Protection, 67(8), 1792–1805.

    CAS  PubMed  Google Scholar 

  • Moretti, A., Mulè, G., Susca, A., González–Jaén, M. T., & Logrieco, A. (2004). Toxin profile, fertility and AFLP analysis of Fusarium verticillioides from banana fruits. Molecular Diversity and PCR-detection of Toxigenic Fusarium Species and Ochratoxigenic Fungi, 601–609.

  • Mule, 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(5–6), 495–502.

    Article  CAS  Google Scholar 

  • Munkvold, G.P. (2003). Epidemiology of Fusarium diseases and their mycotoxins in maize ears. Epidemiology of Mycotoxin Producing Fungi, 705–713.

  • Munkvold, G. P., & Desjardins, A. E. (1997). Fumonisins in maize, can we reduce their occurrence. Plant Disease, 81(6), 556–565.

    Article  CAS  Google Scholar 

  • Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proceedings of National Academy of Sciences of the United States of America, 70(12), 3321–3323.

    Article  CAS  Google Scholar 

  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89(3), 583–590.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nicholson, P., Simpson, D. R., Weston, G., Rezanoor, H. N., Lees, A. K., Parry, D. W., et al. (1998). Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiological and Molecular Plant Pathology, 53(1), 17–37.

    Article  CAS  Google Scholar 

  • Pamphile, J. A., & Azevedo, J. L. (2002). Molecular characterization of endophytic strains of Fusarium verticillioides (= Fusarium moniliforme) from maize (Zea mays L.). World Journal of Microbiology and Biotechnology, 18(5), 391–396.

    Article  CAS  Google Scholar 

  • Patiño, B., Mirete, S., Gonzàlez-Jaèn, M. T., Mulè, G., Rodrìguez, T., & Vàzquez, C. (2004). PCR detection assay of the fumonisin producing Fusarium verticillioides strains. Journal of Food Protection, 67(6), 1278–1283.

    PubMed  Google Scholar 

  • Peakall, R., & Smouse, P. E. (2006). GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295.

    Article  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Proctor, R. H., Desjardins, A. E., Plattner, R. D., & Hohn, T. M. (1999). A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genetics and Biology, 27(1), 100–112.

    Article  CAS  PubMed  Google Scholar 

  • Reid, L. M., Nicol, R. W., Ouellet, T., Savard, M., Miller, J. D., Young, J. C., et al. (1999). Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopatholoy, 89(11), 1028–1037.

    Article  CAS  Google Scholar 

  • Ren, X., Zhu, Z. D., Li, H. J., Duan, C. X., & Wang, X. M. (2012). SSR marker development and analysis of genetic diversity of Fusarium verticillioides isolated from maize in China. Scientia Agricultura Sinica, 45(1), 52–66.

    CAS  Google Scholar 

  • Reynoso, M. M., Chulze, S. N., Zeller, K. A., Torres, A. M., & Leslie, J. F. (2009). Genetic structure of Fusarium verticillioides populations isolated from maize in Argentina. European Journal of Plant Pathology, 123(2), 207–215.

    Article  CAS  Google Scholar 

  • Rocha, L. O., Reis, G. M., da Silva, V. N., Braghini, R., Teixeira, M. M. G., & Corrêa, B. (2011). Molecular characterization and fumonisin production by Fusarium verticillioides isolated from corn grains of different geographic origins in Brazil. International Journal of Food Microbiology, 145(1), 9–21.

    Article  CAS  Google Scholar 

  • Samapundo, S., Devlieghere, F., Meulenaer, B. D., Lamboni, Y., Osei-Nimoh, D., & Debevere, J. M. (2007). Interaction of water activity and bicarbonate salts in the inhibition of growth and mycotoxin production by Fusarium and Aspergillus species of importance to corn. International Journal of Food Microbiology, 116(2), 266–274.

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Rangel, D., San Juan-Badillo, A., & Plasencia, J. (2005). Fumonisin production by Fusarium verticillioides strains isolated from maize in Mexico and development of a polymerase chain reaction to detect potential toxigenic strains in grains. Journal of Agricultural and Food Chemistry, 53(22), 8565–8571.

    Article  PubMed  Google Scholar 

  • Schaafsma, A. W., Limay-rios, V., & Tamburic-illincic, L. (2008). Mycotoxins and Fusarium species associated with maize ear rot in Ontario, Canada. Cereal Research Communication, 36, 525–527.

    Google Scholar 

  • Silva, V. N. S., Fernandes, F. M. C., Cortez, A., Ribeiro, D. H. B., Almeida, A. P., Hassegawa, R. H., et al. (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(8), 798–804.

    Article  PubMed  Google Scholar 

  • Steenkamp, E. T., Wingfield, B. D., Coutinho, T. A., Zeller, K. A., Wingfield, M. J., Marasas, W. F. O., et al. (2000). PCR-based identification of Mat-1 and Mat-2 in the Gibberella fujikuroi species complex. Applied Environmental Microbiology, 66(10), 4378–4382.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stewart, D. W., Reid, L. M., Nicol, R. W., & Schaafsma, A. W. (2002). A mathematical simulation of growth of Fusarium in maize ears after artificial inoculation. Phytopatholoy, 92(5), 534–541.

    Article  CAS  Google Scholar 

  • Torres, A. M., Reynoso, M. M., Rojo, F. G., Ramirez, M. L., & Chulze, S. N. (2001). Fusarium species (section Liseola) and its mycotoxins in maize harvested in northern Argentina. Food Additives Contaminants, 18(9), 836–843.

    Article  CAS  PubMed  Google Scholar 

  • Velluti, A., Marín, S., Bettucci, L., Ramos, A. J., & Sanchis, V. (2000). The effect of fungal competition on colonization of maize grain by Fusarium moniliforme, F. proliferatum and F. graminearum and on fumonisin B1 and zearalenone formation. International Journal of Food Microbiology, 59(1–2), 59–66.

    Article  CAS  PubMed  Google Scholar 

  • Vigier, B., Reid, L. M., Seifert, K. A., Stewart, D. W., & Halminton, R. I. (1997). Distribution and prediction of Fusarium species associated with maize ear rot in Ontario. Canadian Journal of Plant Pathology, 19(1), 60–65.

    Article  Google Scholar 

  • Visentin, I., Tamietti, G., Valentino, D., Portis, E., Karlovsky, P., Moretti, A., et al. (2009). The ITS region as a taxonomic discriminator between Fusarium verticillioides and Fusarium proliferatum. Mycological Research, 113(10), 1137–1145.

    Article  CAS  PubMed  Google Scholar 

  • Wei, T., Zhu, W., Pang, M., Liu, Y., & Dong, J. (2013). Natural occurrence of fumonisins B1 and B2 in corn in four provinces of China. Food Additives and Contaminants: Part B, 6(4), 270–274.

    Article  CAS  Google Scholar 

  • Zeller, K. A., Bowden, R. L., & Leslie, J. F. (2003). Diversity of epidemic populations of Gibberella zeae from small quadrats in Kansas and North Dakota. Phytopathology, 93(7), 874–880.

    Article  PubMed  Google Scholar 

  • Zeller, K. A., Bowden, R. L., & Leslie, J. F. (2004). Population differentiation and recombination in wheat scab population of Gibberella zeae from the United States. Molecular Ecology, 13(3), 563–571.

    Article  PubMed  Google Scholar 

  • Zhao, J. R., & Wang, R. H. (2009). Factors promoting the steady increase of American maize production and their enlightenments for China. Journal of Maize Science, 17(5), 156–159.

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant no. 31271988), the Special Fund for Agro-scientific Research in the Public Interest (grant no. 201303016), the Special Fund for Risk Assessment of China (GJFP201500702), Science and Technology Planning Project of Jiangsu Province (BE2014738), and the Jiangsu Agriculture Science and Technology Innovation Fund [grant no. CX(14)2126].

Compliance with ethical standards

This article does not contain any research involving human participants or animals.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jianrong Shi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qiu, J., Xu, J., Dong, F. et al. Isolation and characterization of Fusarium verticillioides from maize in eastern China. Eur J Plant Pathol 142, 791–800 (2015). https://doi.org/10.1007/s10658-015-0652-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0652-5

Keywords

Navigation