Interactions of Maize-Pathogenic Fusarium Species with Macrophomina phaseolina Shed Light on Host Preference in Crop Rotation

Document Type : Original Research

Authors
Ayşe Görmez 1
Semiha Yüceer 2
Talap Talapov 1
Canan Can 1
1 Department of Biology, Faculty of Arts and Sciences, Gaziantep University, Gaziantep, Türkiye.
2 Biological Control Research Institute, Adana, Türkiye.
Abstract
Survey studies during the 2021–2022 maize growing season in Türkiye’s Central and Southeastern Anatolia Regions identified Fusarium species in seven provinces (Eskişehir, Konya, Karaman, Gaziantep, Şanlıurfa, Mardin, and Diyarbakır). Pathogenicity tests revealed 31 pathogenic isolates among 115 Fusarium spp., with three isolates causing the highest disease severity at a 50% infection rate. These isolates showed moderate pathogenicity in stems and weak pathogenicity in roots. For species identification, EF-1alpha and RPB2 regions of 28 isolates were amplified, and sequences were compared to the NCBI database via BLAST analysis. Results indicated Fusarium proliferatum, F. subglutinans, and F. verticillioides as the dominant species. Cross-pathogenicity tests with F. proliferatum, F. subglutinans, F. verticillioides, and Macrophomina phaseolina, alone and in combinations, were performed on barley, wheat, bean, corn, garlic, sorghum, and oat genotypes. All tested plants showed varying disease severity, with garlic being the most affected. M. phaseolina exhibited the least pathogenicity, while its combination with F. verticillioides caused the greatest damage. These findings are particularly significant considering the pathogens' disease impacts and mycotoxin production capacities.
Keywords
Cross pathogenicity, Mycotoxin production capacities, ">Zea mays L
Subjects
1.       Aktaş, A., Bolat, N., Keser, M. and İnce, T. 2000. Identification of Wheat Root Rot Pathogens in Eskişehir Province and Determination of Wheat and Barley Genotypes Resistant to Drechslera sorokiniana (Sacc.) Subram. and Jain. Plant Prot. Bull., 40(1-2): 71-83.
2.       Altınok, H. H. and Can, C. 2010. Characterization of Fusarium oxysporum f. sp. melongenae Isolates from Eggplant in Türkiye by Pathogenicity, VCG, and RAPD Analysis. Phytoparasitica, 38(2): 149-157.
3.       Altınok, H. H. and Kamberoğlu, M. A. 2005. Prevalence and Severity of Fusarium and Verticillium Wilt Diseases in Eggplant Production Areas in Adana and Mersin Provinces. Çukurova Univ. J. Agric. Fac., 19(4): 1-8.
4.       Anisimova, O. K., Shchennikova, A. V., Kochieva, E. Z. and Filyushin, M. A. 2021. Pathogenesis-Related Genes of PR1, PR2, PR4, and PR5 Families Are Involved in the Response to Fusarium Infection in Garlic (Allium sativum L.). Int. J. Mol. Sci., 22: 6688.
5.       Aoki, T., O’Donnell, K. and Geiser, D. M. 2014. Systematics of Key Phytopathogenic Fusarium Species: Current Status and Future Challenges. J. Gen. Plant Pathol., 80: 189–201.
6.       Bağcı, S. A., Hekimhan, H., Arısoy, R. Z., Taner, A., Büyük, O., Nicol, J. and Aydoğdu, M. 2010. Effect of Different Rotation Systems on Wheat Root and Crown Rot Disease. Plant Res. J., 2: 25–30.
7.       Bangar, S. P., Sandhu, K. S., Trif, M., Manjunatha, V. and Lorenzo, J. M. 2022. Germinated Barley Cultivars: Effect on Physicochemical and Bioactive Properties. Food Anal. Methods, 15: 2505–2512.
8.       Biles, C. L. and Martyn, R. D. 1989. Local and Systemic Resistance Induced in Watermelons by Formae Speciales of Fusarium oxysporum. Phytopathology, 79: 856–860.
9.       Booth, C. 1971. The Genus Fusarium. Commonwealth Mycological Institute, Kew, England.
10.    Burgess, L. W., Summerell, B. A., Bullock, S., Gott, K. P. and Backhouse, D. 1994. Laboratory Manual for Fusarium Research. 3rd Edition, Department of Crop Sciences, University of Sydney.
11.    Can, C., Elekçioğlu, H., Yücel, S. and Özaslan, M. 2003. Identification of Fusarium Species Causing Wilt in Tomatoes in Greenhouses, Their Relationship with Nematodes in Disease Development, and Control Options. Final Report, TÜBİTAK (TOGTAG Project No: TARP-2371).
12.    Cengiz, R. 2016. Maize Research of Public Sector in Türkiye. Field Crops Res. Cent. Res. Inst., 25 (Special Issue-1): 304-310.
13.    Crous, P. W., Lombard, L., Sandoval-Denis, M., Seifert, K. A., Schroers, H. J., Chaverri, P., Gené, J., Guarro, J., Hirooka, Y., Bensch, K., Kema, G. H. J., Lamprecht, S. C., Cai, L., Rossman, A. Y., Stadler, M., Summerbell, R. C., Taylor, J. W., Ploch, S., Visagie, C. M., Yilmaz, N., Frisvad, J. C., Abdel-Azeem, A. M., Abdollahzadeh, J., Abdolrasouli, A., Akulov, A., Alberts, J. F., Araújo, J. P. M., Ariyawansa, H. A., Bakhshi, M., Bendiksby, M., Ben Hadj Amor, A., Bezerra, J. D. P., Boekhout, T., Câmara, M. P. S., Carbia, M., Cardinali, G., Castañeda-Ruiz, R. F., Celis, A., Chaturvedi, V., Collemare, J., Croll, D., Damm, U., Decock, C. A., de Vries, R. P., Ezekiel, C. N., Fan, X. L., Fernández, N. B., Gaya, E., González, C. D., Gramaje, D., Groenewald, J. Z., Grube, M., Guevara-Suarez, M., Gupta, V.K, Guarnaccia V, Haddaji, A., Hagen, F., Haelewaters, D., Hansen, K., Hashimoto, A., Hernández-Restrepo, M., Houbraken, J., Hubka, V., Hyde, K. D., Iturriaga, T., Jeewon, R., Johnston, P. R., Jurjević, Ž., Karalti, I., Korsten, L., Kuramae, E. E., Kušan, I., Labuda, R., Lawrence, D. P., Lee, H. B., Lechat, C., Li, H. Y., Litovka, Y. A., Maharachchikumbura, S. S. N., Marin-Felix, Y., Matio Kemkuignou, B., Matočec, N., McTaggart, A. R., Mlčoch, P., Mugnai, L., Nakashima, C., Nilsson, R. H., Noumeur, S. R., Pavlov, I. N., Peralta, M. P., Phillips, A. J. L., Pitt, J. I., Polizzi, G., Quaedvlieg, W., Rajeshkumar, K. C., Restrepo, S., Rhaiem, A., Robert, J., Robert, V., Rodrigues, A. M., Salgado-Salazar, C., Samson, R. A., Santos, A. C. S., Shivas, R.G., Souza-Motta, C. M., Sun, G. Y., Swart, W. J., Szoke, S., Tan, Y. P., Taylor, J.E., Taylor, P. W. J., Tiago, P. V., Váczy, K. Z., van de Wiele, N., van der Merwe, N. A., Verkley, G. J. M., Vieira W. A. S., Vizzini A., Weir B. S., Wijayawardene N. N., Xia J. W., Yáñez-Morales M. J., Yurkov A., Zamora J. C., Zare R., Zhang, C. L. and Thines, M. 2021. Fusarium: More than a Node or a Foot-Shaped Basal Cell. Stud. Mycol., 98: 100-116.
14.    Dixon, R. A. and Paiva, N. L. 1995. Stress-Induced Phenylpropanoid Metabolism. Plant Cell, 7(7): 1085-1097.
15.    Early, R. 2009. Pathogen Control in Primary Production: Crop Foods. In: “Foodborne Pathogens”. 2nd Edition, Woodhead Publishing, UK, PP. 205-279.
16.    Ekwomadu, T. I., 2019. Occurrence and Variation of Fusarium Free and Masked Mycotoxins in Maize from Agriculture Regions of South Africa. Doctoral Dissertation, North-West University, Potchefstroom, South Africa.
17.    Erper, I., Karaca, G. H. and Özkoç, I. 2008. Root Rot Disease Incidence and Severity on Some Legume Species Grown in Samsun and the Fungi Isolated from Roots and Soils. Arch. Phytopathol. Plant Prot., 41(7): 501-506.
18.    Eslahi, M. R., Safaie, N., Saidi, A., Shams-bakhsh, M. and Jafary, H. 2021. cDNA-AFLP Analysis of Plant Defense Genes Expressed in Wheat (cv. Chamran) Infected with Mycosphaerella graminicola. J. Agric. Sci. Technol., 23(3): 699-710.
19.    Farooqui, A. S., Syed, H. M., Talpade, N. N., Sontakke, M. D. and Ghatge, P. U. 2018. Influence of Germination on Chemical and Nutritional Properties of Barley Flour. J. Pharmacogn. Phytochem., 7(2): 3855-3858.
20.    Hammerschmidt, R. 1999. Phytoalexins: What Have We Learned after 60 Years? Ann. Rev. Phytopathol., 37: 285-306.
21.    Haware, M. P. and Nene, Y. L. 1982. Races of Fusarium oxysporum f. sp. ciceri. Plant Dis., 66: 809-810.
22.    Hekimhan, H., Bağcı, S. A., Nicol, J. and Tunalı, B. 2005. Effects of Root and Root Rot Disease Agents on Some Winter Cereal Yields. Proceedings of the VIth Field Crops Congress of Türkiye, September 5–9, 2005, Antalya, Research Presentation, I: 201–206,
23.    Ismail, M. A., Abdel-Hafez, S. I. I., Hussein, N. A. and Abdel-Hameed, N. A. 2015. Contributions to the Genus Fusarium in Egypt with Dichotomous Keys for Identification of Species. 1st. Edition, Tmkarpiński Publisher, Suchy Las, Poland, 179 PP.
24.    Jain, P. K., Gupta, V. K., Misra, A. K., Gaur, R., Bajpai, V. and Issar, S. 2011. Current Status of Fusarium Infection in Human and Animal. Asian J. Anim. Vet. Adv., 6: 201–227.
25.    Kabak, B. and Var, I. 2005. Fusarium Toxins. Food Feed Sci. Technol., 8: 30-42.
26.    Karlsson, I., Edel-Hermann, V., Gautheron, N., Durling, M. B., Kolseth, A. K., Steinberg, C., Persson, P. and Friberg, H. 2016. Genus-Specific Primers for Study of Fusarium Communities in Field Samples. Appl. Environ. Microbiol., 82: 491–501.
27.    Lampkin, N., 1997. Organic farming. Reprint Edition, Farming Press Books, Ipswich.
28.    Leslie, J. F. and Summerell, B. A. 2006. The Fusarium Laboratory Manual. Blackwell Publishing: Hoboken, NJ, ABD.
29.    National Center for Biotechnology Information. 2024. Standard Nucleotide BLAST. June 10, 2024, from https://www.ncbi.nlm.nih.gov/”.
30.    Ma, L. J., Geiser, D. M., Proctor, R. H., Rooney, A. P., O’Donnell, K., Trail, F., Gardiner, D. M., Manners, J. M. and Kazan, K. 2013. Fusarium Pathogenomics. Ann. Rev. Microbiol., 67: 399-416.
31.    Makoi, J. H. J. R. and Ndakidemi, P. A. 2007. Biological, Ecological and Agronomic Significance of Plant Phenolic Compounds in Rhizosphere of the Symbiotic Legumes. Afr. J. Biotechnol., 6: 1358–1368.
32.    Mittler, R., 2002. Oxidative Stress, Antioxidants and Stress Tolerance. Trends Plant Sci., 7(9): 405-410.
33.    Munkvold, G., 2003. Epidemiology of Fusarium Diseases and Their Mycotoxins in Maize Ears. Euro. J. Plant Pathol., 109(7): 705-713.
34.    Munkvold, G. P. and Leslie, J. F. 1999. Fusarium Root Rot Diseases. In: White D. G. “Compendium of Corn Diseases”, (Ed.): White D. G. 3rd Edition, The American Phytopathological Society, 13 PP.
35.    Muyolo, N. G., Lipps, P. E. and Schmitthenner, A. F. 1993. Anastomosis Grouping and Variation in Virulence among Isolates of Rhizoctonia solani Associated with Dry Bean and Soybean in Ohio and Zaire. Phytopathology, 83(4): 438-444.
36.    Nelson, P. E., Toussoun, T. A. and Marasas, W. F. O. 1983. Fusarium species: An Illustrated Manual for Identification. Pennsylvania State University Press.
37.    O’Donnell, K., Ward, T. J., Robert, V., Crous, P. W., Geiser, D. M. and Kang, S. 2015. DNA Sequence-Based Identification of Fusarium: Current Status and Future Directions. Phytoparasitica, 43(5): 583–595.
38.    Özgönen, H., 2011. Arbüsküler Mikorizal Fungusların Pamukta Bitki Gelişimine ve Verticillium Solgunluğu Verticillium dahliae Kleb Üzerine Etkileri. SDÜ Fen Bilimleri Enstitüsü Dergisi, 15: 171-177.
39.    Palmero, D., Gálvez, L., García, M., Gil-Serna, J. and Benito, S. 2013. The Effects of Storage Duration, Temperature and Cultivar on the Severity of Garlic Clove Rot Caused by Fusarium proliferatum. Postharvest Biol. Technol., 78: 34–39.
40.    Płażek, A. 2013. Induced Resistance in Plants to Fungal Diseases. Postępy Nauk Rolniczych, 6(1): 59-75.
41.    Saremi, H. and Burgess, L. W. 2000. Effect of Soil Temperature on Distribution and Population Dynamics of Fusarium Species. J. Agric. Sci. Technol., 2(2): 119-125.
42.    Seifert, K. 1996. Fuskey-Fusarium interactive key. Agriculture and AgriFood Canada.
43.    Skadhauge, B., Thomsen, K. K. and Von Wettstein, D. 1997. The Role of the Barley Testa Layer and its Flavonoid Content in Resistance to Fusarium Infections. Hereditas, 126: 147-160.
44.    "Smith, J. E. 2001. Mycotoxins. In: “Food Chemical Safety: Contaminants”, (Ed.): Watson, D. H. Woodhead Publishing and CRC Press LLC, 1: 332.
45.    Su, G., Suh, S. O., Schneider, R. W. and Russin, J. S. 2001. Host Specialization in the Charcoal Rot Fungus, Macrophomina phaseolina. Phytopathology, 91(1): 120-126.
46.    Townsend, G. R. and Heuberger, I. W. 1943. Methods of Estimating Losses Caused by Diseases in Fungicide Experiments. Plant Dis. Rep., 27: 340–343.
47.    U.S. Department of Agriculture (USDA). 2024. Grain: World Markets and Trade. Retrieved January 30, 2024, From: https://www.usda.gov/”.
48.    Van Loon, L. C., Rep, M. and Pieterse, C. M. J. 2006. Significance of Induced Resistance in Plants for Sustainable Crop Protection. Ann. Rev. Phytopathol., 44: 309-332.
49.    Vural, S. and Soylu, S. 2012. Prevalence and Incidence of Fungal Disease Agents Affecting Bean (Phaseolus vulgaris L.) Plants. Res. Crops, 13(2): 634-640.
50.    Yıldırım, A. F., Araz, A., Turgay, B., Ünal, F. and Büyük, O. 2016. Root and Root Collar Past, Present and Struggle in Cool Climate Cereals. General Directorate of Agricultural Research and Policies, Agricultural Control Central Research Institute, PP. 1-104.
Journal of Agricultural Science and Technology
Volume 28, Issue 4
July and August 2026
Pages 963-979