Vol. 63 No. 2 (2024)
Articles

Fusarium wilt caused by Fusarium oxysporum f. sp. cubense tropical race 4 in banana plantations in Türkiye

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  • Mümine ÖZARSLANDAN,
  • Davut Soner AKGÜL
Mümine ÖZARSLANDAN
Biological Control Research Institute, Ministry of Agriculture and Forestry, 01321, Yüreğir, Adana
Davut Soner AKGÜL
Department of Plant Protection, Agriculture Faculty, University of Çukurova, 01330, Balcalı, Adana
DOI: https://doi.org/10.36253/phyto-15133
Categories

Published 2024-07-17

Keywords

  • Fusarium sacchari,
  • Grand-Naine,
  • Collar-rot,
  • identification

How to Cite

[1]
M. ÖZARSLANDAN and D. S. AKGÜL, “Fusarium wilt caused by Fusarium oxysporum f. sp. cubense tropical race 4 in banana plantations in Türkiye”, Phytopathol. Mediterr., vol. 63, no. 2, pp. 207–221, Jul. 2024.

Copyright (c) 2024 Mümine ÖZARSLANDAN, Davut Soner AKGÜL

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Abstract

important disease for banana production. Presence and prevalence of FocTR4 in banana plantations on the Mediterranean coast of Türkiye were assessed during 2018 to 2020 in a total of 117 banana plantations in open fields and protected plastic greenhouses. Rhizome, pseudostem, and root samples were taken from plants showing typical symptoms associated to the disease and from suspected affected plants. Fungi were isolated from the plant internal tissues, and Fusarium oxysporum-like colonies were sub-cultured for further analyses. Phylogenetic analyses of 36 isolates showed that they belonged to four different Fusarium species: F. musae, F. oxysporum, F. sacchari, and F. solani. Eight representative F. oxysporum isolates were identified as FocTR4 by specific PCR and qPCR tests. Pathogenicity tests were carried out on tissue-cultured ‘Cavendish’ type banana seedlings (‘Grand Naine’) for 36 Fusarium isolates, and their virulence was assessed based on the internal necrosis observed in the rhizomes. Approx. 40 to 65 d after inoculations, FocTR4, F. oxysporum, and F. sacchari isolates caused severe to mild necroses in the seedling rhizomes. This is the first report of F. sacchari associated with root and collar rot of bananas in Türkiye. This study showed that Fusarium wilt caused by FocTR4 is present, but at low incidence (6.8%) in Turkish banana plantations.

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References

  1. Acuna R., Rouard M., Leiva A.M., Marquez C., Olortegui J.A., … Dita M., 2022. First report of Fusarium oxysporum f. sp. cubense tropical race 4 causing Fusarium wilt in Cavendish bananas in Peru. Plant Disease 106 (8): 2268. https://doi.org/10.1094/PDIS-09-21-1951-PDN DOI: https://doi.org/10.1094/PDIS-09-21-1951-PDN
  2. Aguayo J., Cerf-Wendling I., Folscher A.B., Fourrier-Jeandel C., Ioos R., … Viljoen A., 2021. First report of Fusarium oxysporum f. sp. cubense tropical race 4 (TR4) causing banana wilt in the Island of Mayotte. Plant Disease 105 (1): 219. https://doi.org/10.1094/PDIS-06-20-1196-PDN DOI: https://doi.org/10.1094/PDIS-06-20-1196-PDN
  3. Anonymous, 2021. Tarım ürünleri piyasaları; muz (in Turkish). Tarım ve Orman Bakanlığı, Tarımsal Ekonomi ve Politika Geliştirme Enstitüsü resmi internet sitesi, https://arastirma.tarimorman.gov.tr/tepge Accession Date 21.01.2024
  4. Anonymous, 2022. Crop production statistics, Turkish Statistical Institute, https://www.data.tuik.gov.tr/Kategori/GetKategori?p=Tarim-111 Accession Date 31.01.2024.
  5. Bregard C., Baptista P., Chatzivassiliou E., Di Serio F., Gonthier P., … Reignault P.L., 2022. Pest categorisation of Fusarium oxysporum f. sp. cubense Tropical Race 4. EFSA Journal 20 (1): 7092. https://doi.org/10.2903/j.efsa.2022.7092 DOI: https://doi.org/10.2903/j.efsa.2022.7092
  6. Chittaraht K., Mostert D., Crew K.S., Viljoen A., Kong G., … Thomas J.E., 2018. First report of Fusarium oxysporum f. sp. cubense tropical race 4 (VCG 01213/16) associated with Cavendish bananas in Laos. Plant Disease 102 (2): 449. https://doi.org/10.1094/PDIS-08-17-1197-PDN DOI: https://doi.org/10.1094/PDIS-08-17-1197-PDN
  7. Conde B.D., Pitkethley R.N., 2001. The discovery, identification and management of banana Fusarium wilt outbreaks in the Northern Territory of Australia. In: Banana Fusarium wilt management: towards sustainable cultivation (A.B., Molina, N.H., Nik Masdek K.W., Liew, ed.) Proceedings of the International workshop on the banana Fusarium wilt disease, Genting Highlands Resort, Malaysia, 18–20 October 1999. INIBAP, Montpellier. pp. 260–265.
  8. Crous P.W., Lombard L., Sondoval-Denis M., Seifert K.A., Schroers H.J., … Thines M., 2021. Fusarium: more than a node or a foot-shaped basal cell. Studies in Mycology 98: 100116. https://doi.org/10.1016%2Fj.simyco.2021.100116 DOI: https://doi.org/10.1016/S2590-0064(21)00024-7
  9. Czislowski E., Zeil-Rolfe I., Aitken E.A.B., 2021. Effector profiles of endophytic Fusarium associated with asymptomatic banana (Musa sp.) Hosts. International Journal of Molecular Sciences 22: 2508. https://doi.org/10.3390/ijms22052508 DOI: https://doi.org/10.3390/ijms22052508
  10. Cui Y., Wu B., Peng A., Song X., Chen X., 2021. The genome of banana leaf blight pathogen Fusarium sacchari str. FS66 harbors widespread gene transfer from Fusarium oxysporum. Frontiers in Plant Science 12: 629859. https://doi.org/10.3389/fpls.2021.629859 DOI: https://doi.org/10.3389/fpls.2021.629859
  11. Dale J., James A., Paul J.Y., Khanna H., Smith M., … Harding R., 2017. Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4. Nature Communications 8: 1496. https://doi.org/10.1038/s41467-017-01670-6 DOI: https://doi.org/10.1038/s41467-017-01670-6
  12. Dean R.D., Van Kan J.A.L., Pretorius Z.A., Hammond-Kosack K.E., Di Pietro A., Foster G.D., 2012. The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13 (4): 414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x DOI: https://doi.org/10.1111/j.1364-3703.2011.00783.x
  13. Dita M.A., Waalwick C., Buddenhagen I.W., Souza M.T., Kema G.H.J., 2010. A molecular diagnostic for tropical race 4 of the banana fusarium wilt pathogen. Plant Pathology 59: 348–357. https://doi.org/10.1111/j.1365-3059.2009.02221.x DOI: https://doi.org/10.1111/j.1365-3059.2009.02221.x
  14. Dita M., Barquero M., Heck D., Muzubuti E.S.G., Staver C.P., 2018. Fusarium wilt of banana: current knowledge on epidemiology and research needs toward sustainable disease management. Frontiers in Plant Sciemce 9: 1468. https://doi.org/10.3389/fpls.2018.01468 DOI: https://doi.org/10.3389/fpls.2018.01468
  15. Dong X., Wang M., Ling N., Shen Q., and Guo S., 2016. Potential role of photosynthesis-related factors in banana metabolism and defense against Fusarium oxysporum f. sp. cubense. Environmental and Experimental Botany 129: 4–12. https://doi.org/10.1016/j.envexpbot.2016.01.005 DOI: https://doi.org/10.1016/j.envexpbot.2016.01.005
  16. Edel-Hermann V., Lecomte C., 2019. Current status of Fusarium oxysporum Formae Speciales and Races. Phytopathology 109: 512–530. https://doi.org/10.1094/PHYTO-08-18-0320-RVW DOI: https://doi.org/10.1094/PHYTO-08-18-0320-RVW
  17. Fourie G., Steenkamp E.T., Gordon T.R., Viljoen A., 2009. Evolutionary relationships among the Fusarium oxysporum f.sp. cubense vegetative compatibility groups. Applied and Environmental Biology 75: 4770–4781. https://doi.org/10.1128/AEM.00370-09 DOI: https://doi.org/10.1128/AEM.00370-09
  18. García-Bastidas F.A., Ordonez N., Konkol J., Al-Qasim M., Naser Z., … Kema G.H.J., 2014. First report of Fusarium oxysporum f. sp. cubense tropical race 4 associated with Panama disease of banana outside Southeast Asia. Plant Disease 98(5): 694. https://doi.org/10.1094/pdis-09-13-0954-pdn DOI: https://doi.org/10.1094/PDIS-09-13-0954-PDN
  19. García-Bastidas F.A., van der Veen A.J.T., Nakasato-Tagami G., Meijer H.J.G., Arango-Isaza R.E., Kema G.H.J., 2019. An improved phenotyping protocol for Panama disease in banana. Frontiers in Plant Science 10: 1006. https://doi.org/10.3389/fpls.2019.01006 DOI: https://doi.org/10.3389/fpls.2019.01006
  20. García-Bastidas F.A., Quintero-Vargas J.C., Ayala-Vasquez M., Schermer T., Seidl M.F., … Kema G.H.J., 2020. First report of Fusarium wilt tropical race 4 in Cavendish bananas caused by Fusarium odoratissimum in Colombia. Plant Disease 104 (3): 994. https://doi.org/10.1094/PDIS-09-19-1922-PDN DOI: https://doi.org/10.1094/PDIS-09-19-1922-PDN
  21. Gomez K.A., Gomez, A.A., 1984. Statistical procedures for agricultural research (2nd ed.). Wiley 680 pp.
  22. Hasegawa M., Kishino H., Yano T., 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22(2): 160–174. https://doi.org/10.1007/BF02101694 DOI: https://doi.org/10.1007/BF02101694
  23. Herbert J.A., Marx D., 1990. Short-term control of Panama disease of bananas in South Africa. Phytoparasitica 22: 339–340. https://journals.co.za/doi/pdf/10.10520/AJA03701263_1354
  24. Hung N.T., Hung N.Q., Mostert D., Viljoen A., Chao C.P., … Molina A.B., 2018. First report of Fusarium wilt on Cavendish bananas, caused by Fusarium oxysporum f. sp. cubense tropical race 4 (VCG 01213/16), in Vietnam. Plant Disease 102 (2): 448. https://doi.org/10.1094/PDIS-08-17-1140-PDN DOI: https://doi.org/10.1094/PDIS-08-17-1140-PDN
  25. Karangwa P., Blomme G., Beed F., Niyongere C., Viljoen A., 2016. The distribution and incidence of banana Fusarium wilt in subsistence farming systems in east and central Africa. Crop Protection 84: 132–140. https://doi.org/10.1016/j.cropro.2016.03.003 DOI: https://doi.org/10.1016/j.cropro.2016.03.003
  26. Karangwa P., Mostert D., Ndayihanzamaso P., Dubois T., Niere B., … Viljoen A., 2018. Genetic Diversity of Fusarium oxysporum f. sp. cubense in East and Central Africa. Plant Disease 102: 552–560. https://doi.org/10.1094/PDIS-02-17-0282-RE DOI: https://doi.org/10.1094/PDIS-02-17-0282-RE
  27. Leslie F.J, Summerell A.B., 2006. The Fusarium Laboratory Manual. Blackwell Publishing, London, UK. pp 220. DOI: https://doi.org/10.1002/9780470278376
  28. Li W.M., Dita M., Wu W., Hu G.B., Xie J.H., … Ge X.J., 2015. Resistance sources to Fusarium oxysporum f. sp. cubense tropical race 4 in banana wild relatives. Plant Pathology 64: 1061–1067. https://doi.org/10.1111/ppa.12340 DOI: https://doi.org/10.1111/ppa.12340
  29. Lin Y.H., Chang J.Y., Liu E.T., Chao C.P., Huang J.W., … Chang P.F.L., 2009. Development of a molecular marker for specific detection of Fusarium oxysporum f. sp. cubense race 4. European Journal of Plant Pathology 123: 353–365. https://doi.org/10.1007/s10658-008-9372-4 DOI: https://doi.org/10.1007/s10658-008-9372-4
  30. Lombard L., Sandoval-Denis M., Cai L., Crous P.W., 2019. Changing the game: resolving systematic issues in key Fusarium species complexes. Persoonia 43: 1–2. https://doi.org/10.3767/persoonia.2019.43.00 DOI: https://doi.org/10.3767/persoonia.2019.43.00
  31. Maryani N., Lombard L., Poerba Y.S., Subandiyah S., Crous P., … Kema H.J.G. 2019a. Phylogeny and genetic diversity of the banana Fusarium wilt pathogen Fusarium oxysporum f. sp. cubense in the Indonesian centre of origin. Studies in Mycology 92: 155–194. https://doi.org/10.1016/j.simyco.2018.06.003 DOI: https://doi.org/10.1016/j.simyco.2018.06.003
  32. Maryani N., Sandoval-Denis M., Lombard L., Crous P.W., Kema G.H.J., 2019b. New endemic Fusarium species hitch-hiking with pathogenic Fusarium strains causing Panama disease in small-holder banana plots in Indonesia. Persoonia 43: 48–69. https://doi.org/10.3767/persoonia.2019.43.02 DOI: https://doi.org/10.3767/persoonia.2019.43.02
  33. Maymon M., Shpatz U., Harel Y.M., Levy E., Elkind G., … Freeman S., 2018. First report of Fusarium oxysporum f. sp. cubense tropical race 4 causing Fusarium Wilt of Cavendish bananas in Israel. Plant Disease 102 (12): 2655. https://doi.org/10.1094/PDIS-05-18-0822-PDN DOI: https://doi.org/10.1094/PDIS-05-18-0822-PDN
  34. Mejias Herrera R., Hernandez Y., Magdama F., Mostert D., Bothma S., … Maryse E.E. 2023. First report of Fusarium wilt of Cavendish bananas caused by Fusarium oxysporum f. sp. cubense tropical race 4 in Venezuela. Plant Disease 107 (10) 3297. https://doi.org/10.1094/PDIS-04-23-0781-PDN DOI: https://doi.org/10.1094/PDIS-04-23-0781-PDN
  35. Nelson P.E., Tousson T.A., Marassas W.F.O., 1983. Fusarium species: An Illustrated Manual for Identification. The Pennsylvania State University Press, University Park and London. pp. 193.
  36. O’Donnell K., Cigelnik E., Nirenberg H.I., 1998. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90 (3): 465–493. https://doi.org/10.1080/00275514.1998.12026933 DOI: https://doi.org/10.1080/00275514.1998.12026933
  37. O’Donnell K., Whitaker B.K., Laraba I., Proctor R.H., Brown D.W., … Geiser D.M., 2022. DNA sequence-based ıdentification of Fusarium: a work in progress. Plant Disease 106: 1597–1609. https://doi.org/10.1094/PDIS-09-21-2035-SR DOI: https://doi.org/10.1094/PDIS-09-21-2035-SR
  38. Ordóñez N., García-Bastidas F., Laghari H.B., Akkary M.Y., Harfouche E.N., … Kema G.H.J., 2016. First report of Fusarium oxysporum f.sp. cubense tropical race 4 causing Panama disease in Cavendish bananas in Pakistan and Lebanon. Plant Disease, 100(1): 209. https://doi.org/10.1094/PDIS-12-14-1356-PDN DOI: https://doi.org/10.1094/PDIS-12-14-1356-PDN
  39. Özarslandan M., Akgül D.S., 2020. First report of Fusarium oxysporum f. sp. cubense race 4 causing Fusarium wilt disease of banana in Turkey. Plant Disease 104(3): 974. https://doi.org/10.1094/PDIS-09-19-1881-PDN DOI: https://doi.org/10.1094/PDIS-09-19-1881-PDN
  40. Pegg K.G., Coates L.M., O’Neill W.T.O., Turner D.W., 2019. The epidemiology of Fusarium wilt of banana. Frontiers in Plant Science 10: 1395. https://doi.org/10.3389/fpls.2019.01395 DOI: https://doi.org/10.3389/fpls.2019.01395
  41. Perez-Vicente L., Dita M.A., 2014. Fusarıum wilt of banana or Panama disease by Fusarium oxysporum f. sp. cubense: A review on history, symptoms, biology, epidemıology and management. In: FAO Technical Manual, Prevention and Diagnostic of Fusarium wilt (Panama disease) of Banana Caused by Fusarium oxysporum f. sp. cubense Tropical Race 4 (L., Perez-Vicente, M., Dita., E., Martínez- de la Parte ed.), 6–30.
  42. Ploetz R.C., 2006. Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense. Phytopathology 96: 653–656. https://doi/pdf/10.1094/PHYTO-96-0653 DOI: https://doi.org/10.1094/PHYTO-96-0653
  43. Ploetz R.C., 2015. Fusarium wilt of banana. Phytopathology 12: 1512–1521. http://dx.doi.org/10.1094/PHYTO-04-15-0101-RVW DOI: https://doi.org/10.1094/PHYTO-04-15-0101-RVW
  44. Ploetz R.C., Pegg K., 1997. Fusarium wilt of banana and Wallace’s line: was the disease originally restricted to his Indo-Malayan region? Australasian Plant Pathology 26: 239–249. https://doi.org/10.1071/AP97039 DOI: https://doi.org/10.1071/AP97039
  45. Qi Y.X., Zhang X., Pu J.J., Xie Y.X., Zhang H.Q., … Huang S.L., 2008. Race 4 identification of Fusarium oxysporum f. sp. cubense from Cavendish cultivars in Hainan province, China. Australasian Plant Disease Notes 3 (1): 46–47. https://doi.org/10.1007/BF03211234 DOI: https://doi.org/10.1007/BF03211234
  46. Seifert K.A., 1996. Fusarium interactive key. Agriculture and Agri-Food Canada. 65 pp.
  47. Stover R.H., 1962. Fusarial wilt (Panama disease) of bananas and other Musa species. UK: Commonwealth Mycological Institute. 117 pp.
  48. Tava V., Prigitano A., Cortesi P., Espoto M.A., Pasquali M., 2021. Fusarium musae from diseased bananas and human patients: susceptibility to fungicides used in clinical and agricultural settings. Journal of Fungi 7: 784. https://doi.org/10.3390/jof7090784 DOI: https://doi.org/10.3390/jof7090784
  49. Thangavelu R., Mostert D., Gopi M., Ganga Devi P., Padmanaban M., Viljoen A., 2019. First detection of Fusarium oxysporum f. sp. cubense tropical race 4 (TR4) on Cavendish banana in India. European Journal of Plant Pathology 154: 777–786. https://doi.org/10.1007/s10658-019-01701-6 DOI: https://doi.org/10.1007/s10658-019-01701-6
  50. Thi L.L., Mertens A., Vu D.T., Vu T.D., Anh Minh P.L., … Janssens S.B., 2022. Diversity of Fusarium associated banana wilt in northern Viet Nam. MycoKeys 87: 53–76. https://doi.org/10.3897/mycokeys.87.72941 DOI: https://doi.org/10.3897/mycokeys.87.72941
  51. Townsend G.R., Heuberger J.W., 1943. Methods for estimating losses caused by diseases in fungicide experiments. The Plant Disease Reporter 27: 340–343.
  52. Ujat A.H., Vadamalai G., Hattori Y., Nakashima C., Wong C.K.F., … Zulperi D., 2021. Current classification and diversity of Fusarium species complex, the causal pathogen of Fusarium wilt disease of banana in Malaysia. Agronomy 11: 955. https://doi.org/10.3390/agronomy11101955 DOI: https://doi.org/10.3390/agronomy11101955
  53. Viljoen A. 2020. Emerging Plant Diseases and Global Food Security. American Phytopathological Society, St. Paul, MN, United States of America. 159 pp.
  54. Vlaardingerbroek I., Beerens B., Rose L., Fokkens L., Cornelissen B.J., … Rep M., 2016. Exchange of core chromosomes and horizontal transfer of lineage-specific chromosomes in Fusarium oxysporum. Environmental Microbiology 18: 3702–3713. https://doi.org/10.1111/1462-2920.13281 DOI: https://doi.org/10.1111/1462-2920.13281
  55. Wu K., Chen W., Yang S., Wen Y., Zheng Y., … Wang Z., 2019. Isolation and identification of Fusarium oxysporum f. sp. cubense in Fujian Province, China. Journal of Integrative Agriculture 18(8): 1905–1913. https://doi.org/10.1016/S2095-3119(18)62149-5 DOI: https://doi.org/10.1016/S2095-3119(18)62149-5
  56. Zheng S.J., Garcia-Bastidas F.A., Li X., Zeng L., Bai T., … Kema G.H.J., 2018. New geographical insights of the latest expansion of Fusarium oxysporum f.sp. cubense tropical race 4 Into the Greater Mekong Subregion. Frontiers in Plant Science 9: 457. https://doi.org/10.3389/fpls.2018.00457 DOI: https://doi.org/10.3389/fpls.2018.00457