Fig. 1. Unrooted phylogenetic tree generated with UPGMA based on AFLP markers (Page, 1996). Solid black circles encompass strains from species identified from the field populations. Light gray circles encompass reference strains for related species. Strains deposited in the Fungal Genetics Stock Center are preceded by “FGSC”. Other strains are all from the authors’ collection at Kansas State University.
Table 1. Species, fertility and origin of Fusarium strains collected from sorghum in Thailand
Table 2. Origin and relationship of strains belonging to multi-member VCGs
Table 3. Mating type and fertility of isolates of F. verticillioides, F. proliferatum and F. thapsinum collected from sorghum in Thailand
Table 4. Analysis of molecular variance (AMOVA) of AFLPs for F. verticillioides, F. proliferatum and F. thapsinum from sorghum collected in Thailand
References
- Adeyanju, A., Little, C., Yu, J. and Tesso, T. 2015. Genome-wide association study on resistance to stalk rot diseases in grain sorghum. G3 (Bethesda) 5:1165-1175. https://doi.org/10.1534/g3.114.016394
- Al-Sadi, A. M., Al-Jabri, A. H., Al-Mazroui, S. S. and Al-Mahmooli, I. H. 2012. Characterization and pathogenicity of fungi and oomycetes associated with root diseases of date palms in Oman. Crop Prot. 37:1-6. https://doi.org/10.1016/j.cropro.2012.02.011
- Anukul, N., Maneeboon, T., Roopkham, C., Chuaysrinule, C. and Mahakarnchanakul, W. 2014. Fumonisin and T-2 toxin production by Fusarium spp. isolated from complete feed and individual agricultural commodities used in shrimp farming. Mycotoxin Res. 30:9-16. https://doi.org/10.1007/s12550-013-0182-y
- Ariyajaroenwong, P., Laopaiboon, P., Jaisil, P. and Laopaiboon, L. 2012. Repeated-batch ethanol production from sweet sorghum juice by Saccharomyces cerevisiae immobilized on sweet sorghum stalks. Energies 5:1215-1228. https://doi.org/10.3390/en5041215
- Bandyopadhyay, R., Butler, D. R., Chandrashekar, A., Reddy, R. K. and Navi, S. S. 2000. Biology, epidemiology, and management of sorghum grain mold. In: Technical and institutional options for sorghum grain mold management, eds. by A. Chandrashekar, R. Bandyopadhyay and A. J. Hall, pp. 34-71. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, India.
- Bentley, A. R., Petrovic, T., Griffiths, S. P., Burgess, L. W. and Summerell, B. A. 2007. Crop pathogens and other Fusarium species associated with Austrostipa aristiglumis. Aust. Plant Pathol. 36:434-438. https://doi.org/10.1071/AP07047
- Boon Long, T. 1992. Sorghum diseases in Thailand. In: Sorghum and millets diseases: A second world review, eds. by W. A. J. de Milliano, R. A. Frederiksen and G. D. Bengston, pp. 41-43. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, India.
- Busman, M., Desjardins, A. E. and Proctor, R. H. 2012. Analysis of fumonisin contamination and the presence of Fusarium in wheat with kernel black point disease in the United States. Food Addit. Contam. A 29:1092-1100. https://doi.org/10.1080/19440049.2012.671787
- Cartwright, R. D., Groth, D. E., Wamishe, Y. A., Greer, C. A., Calvert, L. A., Vera Cruz, C. M., Verdier, V. and Way, M. O. 2018. Compendium of rice diseases and pests. 2nd ed. APS Press, St. Paul, MN, USA. 121 pp.
- Choi, H.-W., Hong, S.-K., Lee, Y.-K. and Kim, W.-G. 2013. Diversity and pathogenicity of Fusarium species associated with grain mold of sorghum. Kor. J. Mycol. 41:142-148. https://doi.org/10.4489/KJM.2013.41.3.142
- Correll, J. C., Klittich, C. J. R. and Leslie, J. F. 1987. Nitrate nonutilizing mutants of Fusarium oxysporum and their use in vegetative compatibility tests. Phytopathology 77:1640-1646. https://doi.org/10.1094/Phyto-77-1640
- Correll, J. C., Klittich, C. J. R. and Leslie, J. F. 1989. Heterokaryon self-incompatibility in Gibberella fujikuroi (Fusarium moniliforme). Mycol. Res. 93:21-27. https://doi.org/10.1016/S0953-7562(89)80130-3
- Darnetty and Salleh, B. 2017. Morphological characteristics and mating populations of Fusarium species in Gibberella fujikuroi species complex (GFSC) associated with stalk rot disease of maize in Indonesia, Malaysia and Thailand. Pak. J. Plant Pathol. 16:33-40. https://doi.org/10.3923/ppj.2017.33.40
- del Palacio, A., Mionetto, A., Bettucci, L. and Pan, D. 2016. Evolution of fungal populations and mycotoxins in sorghum silage. Food Addit. Contam. A 33:1864-1872. https://doi.org/10.1080/19440049.2016.1244732
- Desjardins, A. E. 2006. Fusarium mycotoxins: Chemistry, genetics and biology. APS Press, St. Paul, MN, USA. 260 pp.
- Funnell-Harris, D. L, O'Neill, P. M., Sattler, S. E. and Yerka, M. K. 2016. Response of sweet sorghum lines to stalk pathogens Fusarium thapsinum and Macrophomina phaseolina. Plant Dis. 100:896-903. https://doi.org/10.1094/PDIS-09-15-1050-RE
- Geiser, D. M., Jimenez-Gasco, M. M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., Zhang, N., Kuldau, G. A. and O'Donnell, K. 2004. FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur. J. Plant Pathol. 110:473-479. https://doi.org/10.1023/B:EJPP.0000032386.75915.a0
- Hall, T. A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/Me/XP/NT. Nucleic Acids Symp. Ser. 41:95-98.
- Hsuan, H. M., Salleh, B. and Zakaria, L. 2011. Molecular identification of Fusarium species in the G. fujikuroi species complex from rice, sugarcane and maize from peninsular Malaysia. Int. J. Mol. Sci. 10:6722-6732.
- Jardine, D. J. 2006. Stalk rots of corn and sorghum. URL http://www.plantpath.k-state.edu/extension/publications/L741.pdf [5 July 2019].
- Jardine, D. J. and Leslie, J. F. 1992. Aggressiveness of Gibberella fujikuroi (Fusarium moniliforme) isolates to grain sorghum under greenhouse conditions. Plant Dis. 76:897-900. https://doi.org/10.1094/PD-76-0897
- Kavitha, A., Prabhakar, P., Narasimhulu, M., Vijayalakshmi, M., Venkateswarlu, Y., Rao, K. V. and Raju, V. B. S. 2010. Isolation, characterization and biological evaluation of bioactive metabolites from Nocardia levis MK-VL_113. Microbiol. Res. 165:199-210. https://doi.org/10.1016/j.micres.2009.05.002
- Kerenyi, Z., Zeller, K. A., Hornok, L. and Leslie, J. F. 1999. Standardization of mating-type terminology in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 65:4071-4076. https://doi.org/10.1128/AEM.65.9.4071-4076.1999
- Kerenyi, Z., Moretti, A., Waalwijk, C., Olah, B. and Hornok, L. 2004. Mating type sequences in asexually reproducing Fusarium species. Appl. Environ. Microbiol. 70:4419-4423. https://doi.org/10.1128/AEM.70.8.4419-4423.2004
- Klittich, C. J. R. and Leslie, J. F. 1988. Nitrate reduction mutants of Fusarium moniliforme (Gibberella fujikuroi). Genetics 118:417-423. https://doi.org/10.1093/genetics/118.3.417
- Klittich, C. J. R. and Leslie, J. F. 1992. Identification of a second mating population within the Fusarium moniliforme anamorph of Gibberella fujikuroi. Mycologia 84:541-547. https://doi.org/10.1080/00275514.1992.12026175
- Klittich, C. J. R., Leslie, J. F., Nelson, P. E. and Marasas, W. F. O. 1997. Fusarium thapsinum (Gibberella thapsina): A new species in section Liseola from sorghum. Mycologia 89:643-652. https://doi.org/10.1080/00275514.1997.12026829
- Laurence, M. H., Summerell, B. A., Burgess, L. W. and Liew, E. C. Y. 2011. Fusarium burgessii sp. nov. representing a novel lineage in the genus Fusarium. Fungal Divers. 49:101-112. https://doi.org/10.1007/s13225-011-0093-1
- Laurence, M. H., Walsh, J. L., Shuttleworth, L. A., Robinson, D. M., Johansen, R. M., Petrovic, T., Vu, T. T. H., Burgess, L. W., Summerell, B. A. and Liew, E. C. Y. 2015. Six novel species of Fusarium from natural ecosystems in Australia. Fungal Divers. 77:349-366. https://doi.org/10.1007/s13225-015-0337-6
- Leslie, J. F. 1991. Mating populations in Gibberella fujikuroi (Fusarium section Liseola). Phytopathology 81:1058-1060.
- Leslie, J. F. 1995. Gibberella fujikuroi: Available populations and variable traits. Can. J. Bot. 73:S282-S291. https://doi.org/10.1139/b95-258
- Leslie, J. F. 2002. Sorghum and millet diseases. Iowa State Press, Ames, IA, USA. 504 pp.
- Leslie, J. F. 2014. Mycotoxins in the sorghum grain chain. In:Mycotoxin Reduction in Grain Chains, eds. by J. F. Leslie and A. F. Logrieco, pp. 282-296. Wiley-Blackwell, Ames, IA, USA.
- Leslie, J. F. and Klein, K. K. 1996. Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics 144:557-567. https://doi.org/10.1093/genetics/144.2.557
- Leslie, J. F. and Summerell, B. A. 2006. The Fusarium laboratory manual. Wiley-Blackwell, Ames, IA, USA. 388 pp.
- Leslie, J. F., Pearson, C. A. S., Nelson, P. E. and Toussoun, T. A. 1990. Fusarium spp. from corn, sorghum, and soybean fields in the central and eastern United States. Phytopathology 80:343-350. https://doi.org/10.1094/Phyto-80-343
- Leslie, J. F., Zeller, K. A., Logrieco, A., Mule, G., Moretti, A. and Ritieni, A. 2004. Species diversity and toxin production by strains in the Gibberella fujikuroi species complex isolated from native prairie grasses in Kansas. Appl. Environ. Microbiol. 70:2254-2262. https://doi.org/10.1128/AEM.70.4.2254-2262.2004
- Leslie, J. F., Zeller, K. A., Lamprecht, S. C., Rheeder, J. P. and Marasas, W. F. O. 2005a. Toxicity, pathogenicity, and genetic differentiation of five species of Fusarium from sorghum and millet. Phytopathology 95:275-283. https://doi.org/10.1094/PHYTO-95-0275
- Leslie, J. F., Summerell, B. A., Bullock, S. and Doe, F. J. 2005b. Description of Gibberella sacchari and neotypification of its anamorph Fusarium sacchari. Mycologia 97:718-724. https://doi.org/10.1080/15572536.2006.11832801
- Leyva-Madrigal, K. Y., Larralde-Corona, C. P., Apodaca-Sanchez, M. A., Quiroz-Figueroa, F. R., Mexia-Bolanos, P. A., Portillo-Valenzuela, S., Ordaz-Ochoa, J. and Maldonado-Mendoza, I. E. 2015. Fusarium species from the Fusarium fujikuroi species complex involved in mixed infections of maize in Northern Sinaloa, Mexico. J. Phytopathol. 163:486-497. https://doi.org/10.1111/jph.12346
- Lincy, S. V., Chandrashekar, A., Narayan, M. S., Sharma, R. and Thakur, R. P. 2011. Natural occurrence of trichothecene-producing Fusaria isolated from India with particular reference to sorghum. World J. Microbiol. Biotechnol. 27:981-989. https://doi.org/10.1007/s11274-010-0542-0
- Little, C. R., Perumal, R., Tesso, T. T., Prom, L. K., Odvody, G. N. and Magill, C. W. 2012. Sorghum pathology and biotechnology-A fungal disease perspective: part I. Grain mold, head smut, and ergot. Eur. J. Plant Sci. Biotechnol. 6:10-30.
- Madania, A., Altawil, M., Naffaa, W., Volker, P. H. and Hawat, M. 2013. Morphological and molecular characterization of Fusarium isolated from maize in Syria. J. Phytopathol. 161:452-458. https://doi.org/10.1111/jph.12085
- Marasas, W. F. O., Rabie, C. J., Lubben, A., Nelson, P. E., Toussoun, T. A. and Van Wyk, P. S. 1987. Fusarium napiforme, a new species from millet and sorghum in southern Africa. Mycologia 79:910-914. https://doi.org/10.1080/00275514.1987.12025484
- Marasas, W. F. O., Rheeder, J. P., Lamprecht, S. C., Zeller, K. A. and Leslie, J. F. 2001. Fusarium andiyazi sp. nov., a new species from sorghum. Mycologia 93:1203-1210. https://doi.org/10.1080/00275514.2001.12063254
- Menkir, A., Ejeta, G., Butler, L. G., Melakeberhan, A. and Warren, H. L. 1996. Fungal invasion of kernels and grain mold damage assessment in diverse sorghum germplasm. Plant Dis. 80:1399-1402. https://doi.org/10.1094/PD-80-1399
- Mohamed Nor, N. M. I., Salleh, B. and Leslie, J. F. 2013. Fusarium species associated with mango malformation in peninsular Malaysia. J. Phytopathol. 161:617-624. https://doi.org/10.1111/jph.12109
- Munkvold, G. P. and White, D. G. 2016. Compendium of corn diseases. 4th ed. APS Press, St. Paul, MN, USA. 165 pp.
- Nelson, P. E., Toussoun, T. A. and Burgess, L. W. 1987. Characterization of Fusarium beomiforme sp. nov.. Mycologia 79:884-889. https://doi.org/10.1080/00275514.1987.12025477
- Nuanpeng, S., Laopaiboon, L., Srinophakun, P., Klanrit, P., Jaisil, P. and Laopaiboon, P. 2011. Ethanol production from sweet sorghum juice under very high gravity conditions: Batch, repeated-batch and scale up fermentation. Electronic J. Biotechnol. 14. doi: 10.2225/vol14-issue1-fulltext-2.
- O'Donnell, K., Kistler, H. C., Cigelnik, E. and Ploetz, R. C. 1998. Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies. Proc. Natl. Acad. Sci. U.S.A. 95:2044-2049. https://doi.org/10.1073/pnas.95.5.2044
- Onyike, N. B. N. and Nelson, P. E. 1992. Fusarium species associated with sorghum grain from Nigeria, Lesotho, and Zimbabwe. Mycologia 84:452-458. https://doi.org/10.1080/00275514.1992.12026159
- Page, R. D. M. 1996. TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
- Palmero, D., Gil-Serna, J., Galvez, L., Curt, M. D. de Cara, M. and Tello, J. 2012. First report of Fusarium verticillioides causing stalk and root rot of sorghum in Spain. Plant Dis. 96:584.
- Peakall, R. and Smouse, P. E. 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-An update. Bioinformatics 28:2537-2539. https://doi.org/10.1093/bioinformatics/bts460
- Pedrozo, R. and Little, C. R. 2014. First report of seedborne Fusarium thapsinum and its pathogenicity on soybean (Glycine max) in the United States. Plant Dis. 98:1745. https://doi.org/10.1094/PDIS-08-14-0806-PDN
- Petrovic, T., Walsh, J. L., Burgess, L. W. and Summerell, B. A. 2009. Fusarium species associated with stalk rot of grain sorghum in the northern grain belt of eastern Australia. Aust. Plant Pathol. 38:373-379. https://doi.org/10.1071/AP09011
- Petrovic, T., Burgess, L. W., Cowie, I., Warren, R. A. and Harvey, P. R. 2013. Diversity and fertility of Fusarium sacchari from wild rice (Oryza australiensis) in Northern Australia, and pathogenicity tests with wild rice, rice, sorghum and maize. Eur. J. Plant Pathol. 136:773-788. https://doi.org/10.1007/s10658-013-0206-7
- Pitt, J. I., Hocking, A. D., Bhudhasamai, K., Miscamble, B. F., Wheeler, K. A. and Tanboon-Ek, P. 1994. The normal mycoflora of commodities from Thailand: 2. Beans, rice, small grains and other commodities. Int. J. Food Microbiol. 23:35-43. https://doi.org/10.1016/0168-1605(94)90220-8
- Prom, L. K., Perumal, R., Jin, Z., Radwan, G., Isakeit, T. and Magill, C. 2015. Mycoflora analysis of hybrid sorghum grain collected from different locations in south Texas. Am. J. Exp. Agric. 6:1-6. https://doi.org/10.9734/AJEA/2015/14590
- Quazi, S. A. J., Burgess, L. W. and Smith-White, J. 2010. Colonization type of Gibberella zeae in Sorghum bicolor. J. Plant Pathol. 92:261-265.
- Salleh, B., Nurdijati, S., Sudjadi, M. S., Tangonan, N. C. and Chuenchit, S. 1995. Current status of sorghum cultivation and diseases in Southeast Asia. In: Disease analysis through genetics and biotechnology: Interdisciplinary bridges to improved sorghum and millet crops, eds. by J. F. Leslie and R. A. Frederiksen, pp. 105-115. Iowa State Press, Ames, IA, USA.
- Sampietro, D. A., Marin, P., Iglesias, J., Presello, D. A., Vattuone, M. A., Catalan, C. A. N. and Gonzalez-Jaen, M. T. 2010. A molecular based strategy for rapid diagnosis of toxigenic Fusarium species associated to cereal grains from Argentina. Fungal Biol. 114:74-81. https://doi.org/10.1016/j.mycres.2009.10.008
- Seifert, K. A., Aoki, T., Baayen, R. P., Brayford, D., Burgess, L. W., Chulze, S., Gams, W., Geiser, D., de Gruyter, J., Leslie, J. F., Logrieco, A., Marasas, W. F. O., Nirenberg, H. I., O'Donnell, K., Rheeder, J., Samuels, G. J., Summerell, B. A., Thrane, U. and Waalwijk, C. 2003. The name Fusarium moniliforme should no longer be used. Mycol. Res. 107:643-644. https://doi.org/10.1017/S095375620323820X
- Sharma, R., Thakur, R. P., Senthilvel, S., Nayak, S., Reddy, S. V., Rao, V. P. and Varshney, R. K. 2011. Identification and characterization of toxigenic Fusaria associated with sorghum grain mold complex in India. Mycopathologia 171:223-230. https://doi.org/10.1007/s11046-010-9354-x
- Steenkamp, E. T., Wingfield, B. D., Coutinho, T. A., Zeller, K. A., Wingfield, M. J., Marasas, W. F. O. and Leslie, J. F. 2000. PCR-based identification of MAT-1 and MAT-2 in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 66:4378-4382. https://doi.org/10.1128/AEM.66.10.4378-4382.2000
- Tarekegn, G., McLaren, N. W. and Swart, W. J. 2006. Effects of weather variables on grain mould of sorghum in South Africa. Plant Pathol. 55:238-245. https://doi.org/10.1111/j.1365-3059.2006.01333.x
- Tesfaendrias, M. T., McLaren, N. W. and Swart, W. J. 2011. Grain mold fungi and their effect on sorghum grain quality. S. Afr. J. Plant Soil 28:172-180.
- Upadhyaya, H. D., Wang, Y. H., Sharma, R. and Sharma, S. 2013. SNP markers linked to leaf rust and grain mold resistance in sorghum. Mol. Breed. 32:451-462. https://doi.org/10.1007/s11032-013-9883-3
- Vos, P., Hogers, R., Bleeker, M., Reijans, M., van der Lee, T., Hornes, M., Friters, A., Pot, J., Paleman, J., Kuiper, M. and Zabeau, M. 1995. AFLP: A new technique for DNA fingerprinting. Nucleic Acids Res. 23:4407-4414. https://doi.org/10.1093/nar/23.21.4407
- Walsh, J. L., Laurence, M. H., Liew, E. C. Y., Sangalang, A., Burgess, L. W., Summerell, B. A. and Petrovic, T. 2010. Fusarium:Two endophytic novel species from tropical grasses in northern Australia. Fungal Divers. 44:149-159. https://doi.org/10.1007/s13225-010-0035-3