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.
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Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1(1–2), 101–102.
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.
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.
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.
Balmas, V., Santori, A., & Corazza, L. (2000). Le specie di Fusarium più comuni in Italia. Petria, 10(S1), 1–60.
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.
Bottalico, A. (1998). Fusarium diseases of cereals: species complex and related mycotoxin profiles in Europe. Journal of Plant Pathology, 80(2), 85–103.
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.
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.
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.
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.
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.
Dowd, P. F., & Johnson, E. T. (2010). Field incidence of mycotoxins in commercial popcorn and potential environmental influences. Mycotoxin Research, 26(1), 15–22.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Kong, L. X., & Luo, P. C. (1995). Identification of pathogen of corn ear rot and its pathogenicity. Corrosion Science, 3, 29–31.
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.
Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual. Ames: Blackwell Professional.
Li, S. D., & Huang, Y. X. (1998). Occurrence and damage of Diplodia ear rot of corn in Yuxi area. Plant Protection, 24, 20–21.
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.
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.
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.
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.
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.
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.
Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89(3), 583–590.
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.
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.
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.
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.
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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].
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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
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DOI: https://doi.org/10.1007/s10658-015-0652-5