Fusarium oxysporum f.sp. cubense

Fusarium oxysporum f. sp. cubense Pronunciation is a fungal plant pathogen that causes Panama disease of banana (Musa spp.), also known as fusarium wilt of banana. The fungi and the related disease are responsible for widespread pressure on banana growing regions, destroying the economic viability of several commercially important banana varieties.

Fusarium oxysporum f.sp. cubense
Fusarium oxysporum f.sp. cubense race 1 growing for several days on brown rice
Fusarium oxysporum f.sp. cubense race 1 growing for several days on brown rice
Scientific classificationEdit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Sordariomycetes
Order: Hypocreales
Family: Nectriaceae
Genus: Fusarium
Species: F. oxysporum
Forma specialis: F. o.  f.sp. cubense
Trionomial name
Fusarium oxysporum f.sp. cubense
E.F.Sm., W.C.Snyder & H.N.Hansen (1940)
Synonyms
  • Fusarium cubense E.F.Sm. (1910)
  • Fusarium oxysporum var. cubense (E.F.Sm.) Wollenw. (1935)
  • Fusarium oxysporum f. cubense (E.F.Sm.) W.C.Snyder & H.N.Hansen (1940)

Description

Fusarium oxysporum is a common inhabitant of soil[1] and produces three types of asexual spores: macroconidia, microconidia and chlamydospores.[2]

The macroconidia are nearly straight, slender and thin-walled. They usually have three or four septa, a foot-shaped basal cell and a curved and tapered apical cell. They are generally produced from phialides on conidiophores by basipetal division. They are important in secondary infection.[3]

The microconidia are ellipsoidal and have either a single septum or none at all. They are formed from phialides in false heads by basipetal division. They are important in secondary infection.[3]

The chlamydospores are globose with thick walls. They are either formed from hyphae or by the modification of hyphal cells. They endure in soils for long periods and act as inocula in primary infection.[3]

The macroconidia and chlamydospores are normally only formed on dead or dying host plants. Chlamydospores are the most significant survival structures of this pathogen.[4]

The teleomorph or sexual reproductive stage of F. oxysporum is unknown.[5]

Four races of this pathogen have been described which attack different banana cultivars:

  • Race 1 attacks cultivars in the Musa (AAA group) 'Gros Michel'[1] and caused the 20th century epidemic.[6] It also attacks 'Ducasse',[1] 'Lady Finger',[1] Musa (AAB group) 'Pome' and its subgroups, Musa (AAB group) 'Silk'[1] and Musa (ABB group) 'Pisang Awak'. (See § Race 1.)
  • Race 2 attacks Musa (ABB group) 'Bluggoe'[1] and its close relatives. (See § Race 2.)
  • Race 3 attacks Heliconia spp.[7][1] (See § Race 3.)
  • Race 4 attacks Musa (AAA group) 'Dwarf Cavendish'[8][9] as well as the hosts of races 1 and 2.[8][9][1] (See § Race 4.)

Taxonomy

A ribosomal intergenic spacer analysis by Kurtz and Schouten 2009 failed to distinguish some F. oxysporum isolates merely endophytic on Musa from pathogenic Foc strains.[10]

Dispersal

Splash by rainfall, movement of contaminated soil, and movement of contaminated propagation materials are the major means of dispersal of Foc. Dispersal by wind alone remains unproven and while animals can test positive for Foc on their outer surfaces, it remains unproven whether they can be effective vectors.[6] Although it is a soil-borne pathogen, it does not compete well against other soil microbes for growth on dead buried tissue. It is nonetheless able to produce infection in living Musa hosts after a complete absence of hosts for 20 years - despite a population decline of 97% within the first three years. This is thought to be due to durable chlamydospores and due to persistence as an asymptomatic infection.[11]

Infection process

Anigorufone is a phytoalexin produced by Musa. It is a nematicidal compound and so infection with Foc induces an anti-nematode defense. Anigorufone is the only nematicidal or nematistatic compound known among the phytoalexins.[10] Foc rapidly invades cortical cells as do many other Fo f.sp..[11]

Reproduction

There is some debate as to whether Foc is sexual and this is investigated by studying its history of recombination - or lack of it. One study of the linkage disequilibrium of gametes showed relatively high disequilibrium and another a high degree of correlation between independent genetic markers, both of which are diagnostic for a lack of recombination and thus a clonal population. Other post-sequencing data analysis performed by the disequilibrium study also failed to reject recombination however this could be consistent with horizontal transfer. Horizontal transfer has been experimentally induced and appears to have been proven in Focs past and so seems the more likely explanation.[11] Both Fo mating types have been observed in Foc and protoperithecia-like structures are produced, but not the sexual structures. This does not necessarily mean that the sexual process has degenerated however, instead this may be a defect of the experiment.[11]

Spores germinate at a higher rate in the presence of Musa root secondary metabolites from susceptible cultivars than those from resistant cultivars. This suggests that inhibition of germination is an important part of host resistance.[11]

Tropical Race 1/TR1

Tropical Race 1/TR1 is also found in Paspalum fasciculatum, Panicum purpurescens, Ixophorus unisetus, and Commelina diffusa in Central America.[12] These weeds may be acting as an inoculum source.[6]

Tropical Race 2/TR2

Tropical Race 3/TR3

Tropical Race 3/TR3 is a pest of Heliconia ornamental flowers.[7][13] Formerly reported to be a lesser pest of Musa balbisiana seedlings and of Gros Michel, but that is no longer thought to be true.[13][9] Now renamed Fusarium oxysporum f. sp. heliconiae.[14][13]

Race 4

Tropical Race 4/TR4

Fusarium odoratissimum
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Sordariomycetes
Order: Hypocreales
Family: Nectriaceae
Genus: Fusarium
Species:
F. odoratissimum
Binomial name
Fusarium odoratissimum
Maryani et al., 2019 [15]
Synonyms

Foc strain TR4

[16][17] Tropical Race 4/TR4 belongs to vegetative compatibility group 01213/16. All cultivars which are susceptible to Race 1 and Race 2 are susceptible to TR4 (see § Race 1 and § Race 2).[18] Starting in 2019 some authorities are following Maryani et al., 2019 in regarding this strain as Fusarium odoratissimum.[15] However, the validity of this taxonomic change has been challenged.[19]

Subtropical Race 4/STR4

Subtropical Race 4/STR4 is a subtropical race and does not become symptomatic on Cavendish until the trees are stressed by cold.[20][1] Also found in Paspalum spp. and Amaranthus spp. in Australia.[16] These weeds may be acting as sources of inoculum.[6]

Research

Much research is being undertaken because of the urgency in formulating effective control methods for Panama disease and breeding resistant banana cultivars. Researchers at University Sains Malaysia are examining variability in the genome of the pathogen and its genetic variability is being studied, as are the evolutionary relationships within vegetative compatibility groups of the pathogen.[21]

Research into the phylogenetic relationships among the different strains of F. oxysporum that cause wilt of banana has been undertaken to determine whether the strains that are specific to the banana have descended from a common ancestor or have developed independently. Results of this study show that it is not monophyletic and appears to have multiple evolutionary origins.[22] The largest lineages of F. oxysporum f. sp. cubense (§ Race 1 and § Race 2) are genetically distinct from a lineage originating from East Africa (§ Race 5) and developed pathogenicity for bananas independently from one another.[23]

Identification, differentiation, and usage of vegetative compatibility groups is useful and valid within Foc because there are relatively few VCGs.[24]

Management

Segura-Mena et al., 2021 finds that Foc § R1 and § TR4 are highly sensitive to pH.[25] They find that this is a potential management method in this disease.[25]

See also

References

  1. Drenth, André; Guest, David I. (2016-08-04). "Fungal and Oomycete Diseases of Tropical Tree Fruit Crops". Annual Review of Phytopathology. Annual Reviews. 54 (1): 373–395. doi:10.1146/annurev-phyto-080615-095944. ISSN 0066-4286. PMID 27491435.
  2. "Fusarium Wilt of Chickpea". Pests and Diseases Image Library. Archived from the original on 2011-03-21. Retrieved 2011-01-03.
  3. Couteaudier, Y. and C. Alabouvette, 1990 Survival and inoculum potential of conidia and chlamydospores of Fusarium oxysporum f. sp. lini in soil. Can. J. Microbiol. 36:551-556
  4. Ploetz, Randy C. (2000). "Panama Disease:A Classic and Destructive Disease of Banana". Plant Health Progress. American Phytopathological Society. 1: 10. doi:10.1094/PHP-2000-1204-01-HM. S2CID 12228953.
  5. Leslie JF, Summerell BA (2006) The Fusarium Laboratory manual. (Blackwell Publishing: Iowa, USA)
  6. Dita, Miguel; Barquero, Marcia; Heck, Daniel; Mizubuti, Eduardo S. G.; Staver, Charles P. (2018-10-19). "Fusarium Wilt of Banana: Current Knowledge on Epidemiology and Research Needs Toward Sustainable Disease Management". Frontiers in Plant Science. Frontiers. 9: 1468. doi:10.3389/fpls.2018.01468. ISSN 1664-462X. PMC 6202804. PMID 30405651.
  7. Waite, B.H (1963). "Wilt of Heliconia spp. caused by Fusarium oxysporum f. sp. cubense Race 3". Tropical Agriculture (Trinidad). 40: 299–305.
  8. Crop Protection Compendium 2005 Edition. Fusarium oxysporum f.sp. cubense (Panama disease of banana). (CAB International: Wallingford, UK).
  9. Ploetz, R.C.; Pegg, K.G. (2000). Jones, D. R. (ed.). Diseases of Banana, Abacá, and Enset. Wallingford, Oxfordshire, England, United Kingdom: CABI (Centre for Agriculture and Bioscience International). p. 143-159. ISBN 978-0-85199-355-3. OCLC 41347037.
  10. Schouten, Alexander (2016-08-04). "Mechanisms Involved in Nematode Control by Endophytic Fungi". Annual Review of Phytopathology. Annual Reviews. 54 (1): 121–142. doi:10.1146/annurev-phyto-080615-100114. ISSN 0066-4286. PMID 27296146.
  11. Gordon, Thomas R. (2017-08-04). "Fusarium oxysporum and the Fusarium Wilt Syndrome". Annual Review of Phytopathology. Annual Reviews. 55 (1): 23–39. doi:10.1146/annurev-phyto-080615-095919. ISSN 0066-4286. PMID 28489498.
  12. Waite, B.H.; Dunlap, V.C. (1953). "Preliminary host range studies with Fusarium oxysporum f. sp. cubense". Plant Disease Reporter. United States Department of Agriculture. 37: 79–80.
  13. Edel-Hermann, V.; Lecomte, C. (2019). "Current Status of Fusarium oxysporum Formae Speciales and Races". Phytopathology. American Phytopathological Society. 109 (4): 512–530. doi:10.1094/phyto-08-18-0320-rvw. ISSN 0031-949X. PMID 30461350.
  14. Ploetz, Randy C. (2006). "Fusarium Wilt of Banana Is Caused by Several Pathogens Referred to as Fusarium oxysporum f. sp. cubense". Phytopathology. American Phytopathological Society. 96 (6): 653–656. doi:10.1094/phyto-96-0653. ISSN 0031-949X. PMID 18943184.
  15. Pittaway, P. A.; Nasir, Nasril; Pegg, K. G. (1999). "Soil receptivity and host - pathogen dynamics in soils naturally infested with Fusarium oxysporum f. sp. cubense, the cause of Panama disease in bananas". Australian Journal of Agricultural Research. CSIRO Publishing (Commonwealth Scientific and Industrial Research Organisation). 50 (4): 623. doi:10.1071/a98152. ISSN 0004-9409.
  16. Hennessy, Chelsea; Walduck, Geoff; Daly, Andrew; Padovan, Anna (2005). "Weed hosts of Fusarium oxysporum f. sp. cubense tropical race 4 in northern Australia". Australasian Plant Pathology. Springer Science and Business Media LLC. 34 (1): 115. doi:10.1071/ap04091. ISSN 0815-3191. S2CID 13097833.
  17. Molina, A.B.; Fabregar, E.; Sinohin, V.G.; Yi, G.; Viljoen, A. (2009). "Recent occurrence of Fusarium oxysporum f.sp. cubense tropical race 4 in Asia". Acta Horticulturae. International Society for Horticultural Science (ISHS) (828): 109–116. doi:10.17660/actahortic.2009.828.10. hdl:2263/12191. ISSN 0567-7572.
  18. Regional strategy and action plan for the prevention, preparedness, response and recovery of Latin America and the Caribbean to Fusarium wilt of Musaceae tropical race 4. FAO (Food and Agriculture Organization of the United Nations). 2022. doi:10.4060/cb8674en. ISBN 978-92-5-136494-9. S2CID 252425659.
    Bragard, Claude; Baptista, Paula; Chatzivassiliou, Elisavet; Di Serio, Francesco; Gonthier, Paolo; Jaques Miret, Josep Anton; Justesen, Annemarie Fejer; MacLeod, Alan; Magnusson, Christer Sven; Milonas, Panagiotis; Navas‐Cortes, Juan A; Parnell, Stephen; Potting, Roel; Stefani, Emilio; Thulke, Hans‐Hermann; Van der Werf, Wopke; Civera, Antonio Vicent; Yuen, Jonathan; Zappalà, Lucia; Migheli, Quirico; Vloutoglou, Irene; Maiorano, Andrea; Streissl, Franz; Reignault, Philippe Lucien (2022). "Pest categorisation of Fusarium oxysporum f. sp. cubense Tropical Race 4". EFSA Journal. Wiley-VCH GmbH. 20 (1): e07092. doi:10.2903/j.efsa.2022.7092. hdl:11380/1280747. ISSN 1831-4732. PMC 8780018. PMID 35079290. S2CID 246179769. European Food Safety Authority (EFSA).
    These reviews cite this research.
    Torres, Eliana; Bebber, Daniel; Studholme, David (2021). "Taxonomic Revision of the Banana Fusarium Wilt TR4 Pathogen Is Premature". Phytopathology. American Phytopathological Society (APS). 111 (12): 2141–2145. doi:10.1094/phyto-03-21-0089-le. hdl:10871/126077. ISSN 0031-949X. PMID 34100303. S2CID 235371340.
  19. "Panama disease tropical race 4 (TR4) - Business Queensland". Queensland Agriculture Department. 2020-11-13. Archived from the original on 22 December 2018. Retrieved 2021-02-06.
  20. 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 Microbiology. 75 (14): 4770–81. Bibcode:2009ApEnM..75.4770F. doi:10.1128/AEM.00370-09. PMC 2708428. PMID 19482953.
  21. O'Donnell, K; Kistler, H. C; Cigelnik, E; Ploetz, R. C (1998-03-03). "Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies". Proceedings of the National Academy of Sciences. 95 (5): 2044–2049. Bibcode:1998PNAS...95.2044O. doi:10.1073/pnas.95.5.2044. PMC 19243. PMID 9482835.
  22. Koenig, R L; et al. (1997). "Fusarium oxysporum f. sp. cubense consists of a small number of divergent and globally distributed clonal lineages". Phytopathology. 87 (9): 915–923. doi:10.1094/phyto.1997.87.9.915. PMID 18945062.
  23. Moore, N.Y.; BENTLEY, S.; BUDDENHAGEN, I.W.; PEGG, K.G. (2001). B.A. Summerell; J.F. Leslie; D. Backhouse; W.L. Bryden; L.W. Burgess (eds.). "Fusarium wilt of banana, a diverse clonal pathogen of a domesticated clonal host". Alianza SIDALC. Fusarium – Paul E. Nelson Memorial Symposium. Saint Paul, Minnesota: American Phytopathological Society Press: 212–224. Retrieved 2021-01-05.
  24. Memon, Komal; Umrani, Fahim Aziz; Baqai, Attiya; Syed, Zafi Sherhan (2023). A Review Based On Comparative Analysis of Techniques Used in Precision Agriculture. 2023 4th International Conference on Computing, Mathematics and Engineering Technologies (iCoMET). IEEE. doi:10.1109/icomet57998.2023.10099182. S2CID 258260664.
    This review cites this research.
    Segura-Mena, R.; Stoorvogel, J.; García-Bastidas, F.; Salacinas-Niez, M.; Kema, G.; Sandoval, J. (2021). "Evaluating the potential of soil management to reduce the effect of Fusarium oxysporum f. sp. cubense in banana (Musa AAA)". European Journal of Plant Pathology. Springer Science and Business Media LLC. 160 (2): 441–455. doi:10.1007/s10658-021-02255-2. ISSN 0929-1873. S2CID 233648418. Royal Netherlands Society of Plant Pathology (KNPV)+European Foundation for Plant Pathology (EFPP).

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