Loading...
 

Fusarium oxysporum f. sp. cubense


Foc at a glance

 
Photo by Monica Lanzoni Rossi
Photo by Monica Lanzoni Rossi
Name of pathogen
Fusarium oxysporum f. sp. cubense (Foc)
Disease
Distribution
Race 1: pan-tropical
TR4: Southeast Asia, northern Australia, Jordan and Mozambique
Protocols
Source: FAO
 
Photo by Miguel Dita
Photo by Miguel Dita
Microconidia
 
Photo by Miguel Dita
Photo by Miguel Dita
Macroconidia
 
Photo by Miguel Dita
Photo by Miguel Dita
Chlamydospores

Fusarium oxysporum f. sp. cubense (Foc) is one of more than 100 formae speciales (special forms) of the soil-borne Fusarium oxysporum species complex of morphologically similar filamentous fungi. The cubense special form comprises the pathogenic strains that cause Fusarium wilt in cultivated bananas, as well as strains that affect species in the Musaceae and Heliconeaceae families. However, it does not follow that the strains of F. oxysporum f. sp. cubense are necessarily related genetically1. F. oxysporum has no known sexual stage. Variation in the fungus is thought to result from mutations.

The pathogenic strains are commonly classified into four races that are meant to reflect differences in the cultivars on which they cause disease. In reality, there are more variants of the fungus than the number of races suggests. Progress in understanding the pathogen's diversity was made possible with the development of a method to classify Fusarium oxysporum strains into vegetative compatibility groups (VCGs), based on the ability of their hyphae to fuse and form stable heterokaryons (cells containing two distinct nuclei)2. Each VCG has its own characteristics in terms of aggressiveness and the banana cultivars that it attacks most readily.

Contents

History

In 1876, the author of the first report of the disease, J. Bancroft, speculated that it was caused by a fungus3. Unaware of Bancroft's work, a horticulturist at the Hawaii Agricultural Experiment Station also proposed in 1904 that a fungus caused the disease4. The plant pathologist Erwin F. Smith became the first person to isolate the pathogen from banana tissues he had received from Cuba5. He reported his results at the first meeting of the American Phytopathological Society held in Boston in 19086. Smith recognized that the fungus was in the genus Fusarium and named it Fusarium cubense because of its Cuban source. The study confirming that the fungus was indeed the causal agent was published in 19197. Fusarium cubense was recognized as a variant of Fusarium oxysporum and renamed Fusarium oxysporum f. sp. cubense in 19358.

Morphology

Three types of asexual spores have been identified: microconidia, macroconidia and chlamydospores, with macroconidia and chlamydospores being normally formed on dead or dying host plants.

Microconidia are one or two celled and oval- to kidney-shaped. They are the type of spore most frequently produced within the vessels of infected plants.

Macroconidia are four to eight celled, sickle-shaped, thin-walled and delicate. These spores are commonly found on the surface of plants killed by the fungus.

Chlamydospores are round, thick-walled spores. They can persist in the soil for long periods of time (more than 30 years).

Australian scientists have established that 20 minutes in 65º C water is the minimum condition for killing race 4 hyphae, microconidia and macroconidia in banana plant tissue, whereas chlamydospores require autoclaving9.

No sexual stage has been observed.

Mode of action

Scientists used to think that the fungus injected toxins into the plant, killing its cells. Instead, evidence suggests that the fungus tricks the plant into killing its cells by triggering the natural process of programmed cell death, which eliminates unwanted, damaged or used cells. The decaying plant tissues are then used by the fungus as a food source10.

The hypothesis is being tested in a banana that has been genetically modified to prevent the fungus from co-opting the plant’s cell death pathways. Deprived of food, the fungus eventually stops growing and fails to colonize and infect the tissues of the transgenic plant11.

Races

The pathogenic strains of Foc are classified into races based on the differential response of cultivars. Traditionally, four races are recognized, although certain situations suggest that more races may exist12. Extensive inoculation studies are needed to clearly define the various pathotypes, but these are expensive and time-consuming. The results may also be equivocal because of variability in growing conditions and/or in planting material. The race concept has been criticized for being an imperfect measure of pathogenic diversity and for not reflecting genetic relationships, but is nonetheless considered useful to describe host reaction and new disease outbreaks.

Race 1

Race 1 strains cause disease in Gros Michel, Silk, Pome and Pisang awak cultivars.

Race 2

Race 2 strains prey on Bluggoe and closely related cooking cultivars.

Race 3

Race 3 was reported to affect Heliconia species, and to a lesser extent Gros Michel and seedlings of Musa balbisiana13. However, the disease has not been reported since14.

Race 4

Race 4 was originally coined to designate the strains that attack Cavendish cultivars. Prior to the 1990s, symptoms of Fusarium wilt on Cavendish cultivars had been observed in the subtropical growing areas of Australia, Canary Islands and South Africa, as well as in some tropical growing areas such as Taiwan15, Jamaica and Guadeloupe. Circumstantial evidence suggested that, with the exception of Taiwan, the limited damage was due to predisposing factors: low temperatures in the subtropics and edaphic factors in the tropics16. Originally classified as race 4, these pathogenic isolates were later reclassified as subtropical race 4 (STR4) to distinguish them from the isolates that cause Fusarium wilt in the tropics in the absence of predisposing factors, which then became known as tropical race 4 (TR4). The isolates in Taiwan were later shown to be associated with TR417. In India, symptoms of Fusarium wilt have also been observed on the Cavendish cultivar 'Grande Naine' in the absence of predisposing factors, except that the isolate was not associated with either STR4 or TR418.

STR4 has been reported in the subtropical regions of Australia (southeast Queensland and northeast New South Wales), South Africa and Canary Islands19.

In addition to Taiwan, TR4 has been reported in peninsular Malaysia20 and Sarawak, Indonesia (Papua province21, Kalimantan22, Halmahera, Java, Sulawesi and Sumatra), mainland China (Guangdong23, Guangxi, Hunan, Hainan24), the Philippines25 and Australia's Northern Territory2627. In 2013, it was reported to be in Jordan, where it had been present since 2006 according to the disease report28, and Mozambique29, where it might have arrived 2-3 years earlier30. There are also reports that it is in Oman31.

TR4 is said to also attack cultivars susceptible to races 1 and 2, and additional cultivars such as Barangan (Lakatan subgroup, AAA genome group)22 and Pisang Mas. The wide host range of TR4 makes it difficult to diagnose outbreaks. For example, while a Cavendish with Fusarium wilt would immediately raise alarm, a Gros Michel infected with TR4 would not because the assumption would be it is infected with a race 1 strain.

Vegetative compatibility

Vegetative compatibility is used to classify into vegetative compatibility groups (VCGs) isolates that share the same form (allele) of the genes that control the formation of an heterokaryon (a cell with two distinct nuclei). Since alleles at each locus (the location of the gene on the chromosome) must be identical in order for isolates to be vegetatively compatible, isolates within a VCG are assumed to be clonally derived. On the other hand, since a mutation in one of those genes would make closely related isolates vegetatively incompatible, isolates that share a common ancestor could occur in different VCGs.

Each VCG is given a four to five digit code. The first three numbers refer to the forma specialis to which the strain belongs, 012 in the case of the banana-specific f. sp. cubense. The following digit(s) represents the order in which the VCGs were identified (e.g. 0120, 0121, 0122 etc.). Some 24 VCGs have been characterized worlwide. Tropical race 4 isolates belong to the VCG 01213/16 complex, although other VCGs, such as VCG 0121, are also known to cause Fusarium wilt on Cavendish cultivars.

The results of a survey published in 2013 documented 11 VCGs in the five banana-producing regions of mainland China32.

Isolates within a VCG can belong to more than one race. For example, VCG 0120 isolates have been extracted from both race 1 and race 4 hosts. In India, VCG 0124 isolates have also been extracted from Cavendish bananas exhibiting Fusarium wilt symptoms18. In Latin America, VCG 0124 isolates are classified as race 1 because they infect Gros Michel but not Cavendish bananas.

References


1. Ploetz, R.C. and Pegg, K.G. 1997. Fusarium wilt of banana and Wallace's line: was the disease originally restricted to his Indo-Malayan region? Australasian Plant Pathology 26(4):239-249.
2. Puhalla, J.E. 1985. Classification of strains of Fusarium oxysporum on the basis of vegetative compatibility. Canadian Journal of Botany, 63(2):179-183.
3. Bancroft, J. 1876. Report of the board appointed to inquire into the cause of disease affecting livestock and plants. In: Votes and Proceedings 1877, Vol 3, Queensland, pp. 1011-1038
4. Higgins, J.E. 1904. The banana in Hawaii. Bulletin No. 7, Hawaii Agricultural Experiment Station, University of Hawaii. Honolulu, Hawaii.
5. Smith, E.F. 1910. A Cuban banana disease. Science 31: 754-755.
7. Brandes, E.W. 1919. Banana wilt. Phytopathology 9: 339-389.
8. Wollenweber, H.W., Reinking, O.W. 1935. Die Fusarien. Berlin, DE. Paul Parey. 355 p.
9. Walduck, G. and Daly, A. 2007. Banana Tropical Race 4 Management Disease Management. Pp. 7-11 In Northern Territory Department of Primary Industry, Fisheries and Mines. Australia. www.nt.gov.au
10. Dickman, M.B. 2004. Can model plants help banana improvement through biotechnology? InfoMusa, France, 13(2):6-11.
11. Paul, J-Y., Becker, D., Dickman, M.B., Harding,R., Khanna, H. and Dale, J. 2011. Apoptosis-related genes confer resistance to Fusarium wilt in transgenic 'Lady Finger' bananas. Plant Biotechnology Journal 9(9):1141-1148.
12. Ploetz, R.C., Pegg, K.G. 2000. Fusarium wilt. pp. 143-159. In: Jones, D.R. (ed.) Diseases of Banana, Abacá and Enset. CABI Publishing, Wallingford, UK.
13. Waite, B.H. 1963. Wilt of Heliconia spp. caused by Fusarium oxysporum f. sp. cubense Race 3. Tropical Agriculture (Trinidad) 40:299-305.
14. Ploetz, R.C. and Pegg, K.G. 2000.Fungal diseases of the root, corm and pseudostem: Fusarium wilt. p. 143-159. In: Jones, D.R. (ed.) Diseases of Banana, Abacá and Enset. CABI Publishing, Wallingford, UK.
17. Occurrence of various Vegetative Compatibility Groups (VCG) of Fusarium oxysporum f. sp. cubense in Asia, a poster presented at the10th International Congress of Plant Pathology in Beijing, China, 25-30 August 2013.
18. A new threat to Cavendish bananas? in the March 2011 issue of InfoMus@
19. Ploetz, R.C., Herbert, J., Sebasigari, K., Hernandez, J.H., Pegg, K.G., Ventura, J.A. and Mayato, L.S. 1990. Importance of fusarium wilt in different banana-growing regions. p.9-26. In: Ploetz, R.C. (ed.). Proceedings of International Conference on Fusarial Wilt of Banana, Miami (USA), 1989/08/27-30. Fusarium wilt of banana. American Phytopathological Society (APS Press), St Paul (USA).
20. Ong Kim Pin. 1996. Fusarium wilt of Cavendish banana in a commercial farm in Malaysia. p.211-217. In: Frison, E.A., Horry, J. and De Waele, D. (eds.). Proceedings of New Frontiers in Resistance Breeding for Nematode, Fusarium and Sigatoka, Kuala Lumpur (MYS), 1995/10/2-5. New frontiers in resistance breeding for nematode, Fusarium and Sigatoka. INIBAP, Montpellier (FRA).
21. Davis, R.I., Moore, N.Y., Bentley, S., Gunua, T.G. and Rahamma, S. 2000. Further records of Fusarium oxysporum f. sp. cubense from New Guinea. Australasian Plant Pathology 29(3):224.
22. Hermanto, C., Sutanto, A., HS, E., Daniells, J.W., O'Neill, W.T., Sinohin, V.G.O., Molina, A.B. and Taylor, P.. 2011. Incidence and Distribution of Fusarium Wilt Disease of Banana in Indonesia. Proceedings of the International ISHS-ProMusa Symposium on Global Perspectives on Asian Challenges held in Guangzhou, China, 14-18 September 2009. Van den Bergh, I., Smith, M. and Swennen, R. (eds). Acta Horticulturae 897:313-322.
23. Qi, P. 2001. Status report of banana Fusarium wilt disease in china. p.119-120. In: Molina, A.B., Nik Masdek, N.H. and Liew, K.W. (eds.). Proceedings of International Workshop on the Banana Fusarium Wilt Disease, Genting Highlands Resort, 1999/10/18-20. Banana Fusarium wilt management: Towards sustainable cultivation. INIBAP, Los Banos, Philippines.
24. Qi, Y.X., Zhang, X., Pu, J.J., Xie, Y.X., Zhang, H.Q. and 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
25. Molina, A., Fabregar, E., Sinohin, V.G., Herradura, L., Fourie, G. and Viljoen, A. 2008. Confirmation of tropical race 4 of Fusarium oxysporum f. sp. cubense, infecting Cavendish bananas in the Philippines. Abstract of presentation to the 2008 Centennial Meeting of the American Phytopathological Society
26. Moore, N. 1998. Bananatopics 25:12-14.
27. Conde, B.D. and Pitkethley, R.N. 2001. The discovery, identification and management of banana fusarium wilt outbreaks in the northern territory of Australia. p.260-265. In: Molina, A.B., Nik Masdek, N.H. and Liew, K.W. (eds.). Proceedings of International Workshop on the Banana Fusarium Wilt Disease, Genting Highlands Resort, 1999/10/18-20. Banana Fusarium wilt management: Towards sustainable cultivation. INIBAP, Los Banos, Philippines.
28. Garcia, F.A., Ordonez, N., Konkol, J., AlQasem, M., Naser, Z., Abdelwali, M., Salem, N.M., Waalwijk, C., Ploetz, R.C. and Kema, G. 2013. First Report of Fusarium oxysporum f. sp. cubense Tropical Race 4 associated with Panama Disease of banana outside Southeast Asia. Plant Disease.
29. IITA press release on TR4 being found in Mozambique.
30. Butler, D. 2013. Fungus threatens top banana. Nature 504(7479):195-196.
31. News on agricultural quarantine measures on bananas in the 5 September 2012 edition of muscatdaily.com
32. Li, C.Y., Mostert, G., Zuo, C.W., Beukes, I., Yang, Q.S., Sheng, O., Kuang, R.B., Wei, Y.R., Hu, C.H., Rose, L., Karangwa, P., Yang, J., Deng, G.M., Liu, S.W., Gao, J., Viljoen, A. and Yi, G.J. 2013. Diversity and Distribution of the Banana Wilt Pathogen Fusarium oxysporum F. Sp. cubense in China. Fungal Genomics and Biology 03(02).

See also on this website

Photos on the symptoms of Fusarium wilt in the Musarama image bank
Video on the symptoms, transmission and prevention of Fusarium wilt in the Musarama video bank
Musapedia page on an INREF-funded research project managed by Wageningen University & Research Centre - Panama disease: Multi-level solutions for a global problem

Further reading

Diagnostic manual and links to presentations given at a 2014 FAO-CARDI regional workshop on the prevention and diagnostic of Fusarium wilt
Contingency plan (in Spanish) on TR4 for OIRSA countries
Fact sheet on Panama disease (8MB PDF) on the Plant Health Australia website
Fusarium wilt of banana laboratory diagnostics manual (1.8MB PDF) on the Plant Health Australia website
Datasheet on Fusarium oxysporum f. sp. cubense in CABI's Invasive Species Compendium
Panama disease: an old nemesis rears its ugly head, Part 1: The beginnings of the banana export trades Part 2: the Cavendish era and beyond
Website for the research projects on Fusarium wilt that are managed by Wageningen University & Research Centre: panamadisease.org>>>-/div>
Banana Fusarium wilt in Africa website (under development)