Panama disease

Panama disease (or Fusarium wilt) is a plant disease that infects banana plants (Musa spp.). It is a wilting disease caused by the fungus Fusarium oxysporum f. sp. cubense (Foc). The pathogen is resistant to fungicides and its control is limited to phytosanitary measures.[1]

Panama disease
Common namesPanama disease
Fusarium wilt of banana
Vascular wilt of banana
Causal agentsFusarium oxysporum f.sp. cubense
Hostsbanana
Vectorswater, soil residues, replanting of suckers, farming tools and transport, leaf trash
EPPO CodeFUSACB
DistributionIndonesia, China, Malaysia, Australia, the Philippines, Jordan, Vietnam, Laos, Pakistan, Lebanon, Mozambique, Oman

During the 1950s, an outbreak of Panama disease almost wiped out the commercial Gros Michel banana production. The Gros Michel banana was the dominant cultivar of bananas, and Fusarium wilt inflicted enormous costs and forced producers to switch to other, disease-resistant cultivars. Currently, a new outbreak of Panama disease caused by the strain Tropical Race 4 (TR4) threatens the production of the Cavendish banana, today's most popular cultivar.

Distribution

Not all banana-producing countries have been affected by the outbreak of Panama disease. Tropical Race 4 (TR4) was first identified in Taiwan,[2] and from there rapidly spread to Indonesia, China, Malaysia, Australia and the Philippines.[3] The disease was then identified in Jordan in 2013.[4] TR4 later spread to Vietnam[5] and Laos,[6] as well as to the Middle East being reported in Pakistan and Lebanon.[7] In 2015, the disease then spread to Africa, being informally announced in Mozambique and Oman.[3] In August 2019, TR4 arrived in Colombia, a country in Latin America, the region comprising the world's biggest banana exporters.[8]

Symptoms

Two external symptoms help characterize Panama disease of banana:

  • Yellow leaf syndrome, the yellowing of the border of the leaves which eventually leads to bending of the petiole.[1]
  • Green leaf syndrome, which occurs in certain cultivars, marked by the persistence of the green color of the leaves followed by the bending of the petiole as in yellow leaf syndrome. Internally, the disease is characterized by a vascular discoloration. This begins in the roots and rhizomes with a yellowing that proceeds to a reddish-brown color in the pseudostem, as the pathogen blocks the plant's nutrient and water transport.[1][9]
  • With proceeding infection, the banana pseudostem can split and eventually, the whole plant collapses.[1]

External symptoms often get confused with the symptoms of bacterial wilt of banana, but ways to differentiate between the two diseases include:

  • Fusarium wilt proceeds from older to younger leaves, but bacterial wilt is the opposite.
  • Fusarium wilt has no symptoms on the growing buds or suckers, no exudates visible within the plant, and no symptoms in the fruit. Bacterial wilt can be characterized by distorted or necrotic buds, bacterial ooze within the plant, and fruit rot and necrosis.[9]

Once a banana plant is infected, recovery is rare, but if it does occur, any new emerging suckers will already be infected and can propagate disease if planted.[9]

Classification and host range

Fusarium oxysporum f. sp. cubense (Foc) is a member of the Fusarium oxysporum species complex, a group of ascomycete fungi with morphological similarities.[10][11] Based on their different host species, the plant pathogenic fungi of this species complex are divided into approximately 150 special forms (formae specialis, f.sp.).[12] Fusarium oxysprorum f.sp. cubense mainly infects banana (Musa) species. The special form cubense has been subdivided into four different races, that each attack a different group of banana genotypes.

  • Race 1 was involved in the 1960s Panama disease outbreak which destroyed much of the Gros Michel banana plantations in Central America. In addition to Gros Michel, Race 1 also attacks other members of the banana AAB genomic group, including Abacá, Maqueño, the Silk subgroup, the Pome subgroup, Pisang Awak, Ducasse, and Lady Finger.[13] Cavendish cultivars are resistant to Race 1.
  • Race 2 infects cooking bananas with ABB genome and the Bluggoe subgroup.[10]
  • Race 3 infecting Heliconia spp. is no longer considered pathogenic to bananas,[1] but included into the Fusarium oxysporum f.sp. heliconiae.[10]
  • Race 4 is the causal agent of the current Panama disease outbreak since it is pathogenic to the currently used Cavendish cultivars (AAA genome). Race 4 is further subdivided into Tropical Race 4 (TR4) and Subtropical Race 4 (STR4). The latter only infects Cavendish and Race 1 and 2 susceptibles under abiotic stress.[14]

Disease cycle

Modern commercially farmed banana plants are reproduced asexually, by replanting the plant's basal shoot that grows after the original plant has been cut down. Being triploid, the fruit contains no seeds, and the male flower does not produce pollen suitable for pollination, prohibiting sexual reproduction. This causes all bananas of a single breed to be nearly genetically identical. The fungus easily spreads from plant to plant because the individual plants' defenses are nearly identical.[15]

The disease is dispersed by spores or infected material that travel in surface water or farming activities. One of the biggest issues in spreading the disease is the means by which new banana plants are planted. Suckers are taken from one plant and clonally propagated to grow new trees. About 30 to 40% of suckers from a diseased plant are infected and not all show symptoms, so the chance of growing a new, already infected plant is fairly high. Finally, the disease is known to infect certain weeds without showing symptoms, meaning it can survive in the absence of banana plants and remain undetected in a place where bananas are planted later.[16]

FOC is thought to persist only asexually, as no sexual phase (teleomorph) has been observed. Recombination events may occur via somatic hybridisation and the parasexual cycle.[17]

This means that the survival and dispersal of the disease relies on purely asexual spores and structures. The disease survives in chlamydospores which are released as the plant dies and can survive in the soil for up to 30 years. When the environment is ideal and there are host roots available (fungus is attracted to root exudates), these chlamydospores will germinate and hyphae will penetrate the roots, initiating infection. There is an increase in the number of symptomatic plants when inflorescences emerge and the highest disease incidence occurs right before harvest.[16] Once infected, microconidia are produced and proliferate within the vessels of the plant's vascular system. Macroconidia are another asexual spore that tends to be found on the surface of plants killed by Panama disease.[18] Infection is systemic, moving through the vascular system and causing yellowing and buckling that starts in older leaves and progresses to younger leaves until the entire plant dies.[16]

History

Gros Michel devastation era

The Gros Michel was the only type of banana eaten in the United States from the late 19th century until after World War II. The disease was serious and diagnosed in Panama banana plantations of Central America. Over several decades, the fungus spread from Panama to neighboring countries, moving north through Costa Rica to Guatemala and south into Colombia and Ecuador.

The banana industry was in a serious crisis, so a new banana thought to be immune to Panama disease was found and adopted, the Cavendish. In a few years, the devastated plantations resumed business as usual, and the transition went smoothly in the American market. Shortly thereafter, Malaysia entered the banana-growing business. Cavendish banana plantations were new to that country in the 1980s, but they rapidly expanded to meet the demand. Thousands of acres of rain forests and former palm oil plantations were shifted to banana production. Within a few years, though, the new plants began to die. While it took several years to find, the cause was ultimately attributed back to the Panama disease. Although the Cavendish was then thought to be immune, it was immune only to the strain of the fungus that destroyed the Gros Michel. The version that annihilated the Gros Michel was found only in the Western Hemisphere, but the version found in Malaysian soil was different, and the Cavendish is susceptible to it. It killed and spread faster, inspiring more panic than its earlier counterpart in Panama. The newly discovered strain of F. oxysporum was named tropical race 4 (TR4).

TR4 devastation era

Tropical Race 4 (TR4) was discovered in Taiwan in 1989.[19] In July 2013, members of OIRSA, a Latin American regional organisation for plant and animal health, produced a contingency plan specific to TR4 for its nine member countries (Belize, Costa Rica, Dominican Republic, El Salvador, Guatemala, Honduras, Mexico, Nicaragua and Panama), the plan is only available in Spanish.[20] In March 2015, Latin America growers met to create a regional defense effort and planned to meet again in September or October of that year. No specific regional measures are in place. Ecuadorian growers requested the government to fumigate all containers.[21]

Scientists are trying to modify the banana plant to make it resist Panama disease and many other serious banana afflictions ranging from fungal, bacterial, and viral infections to nematodes and beetles. Researchers are combing remote jungles searching for new wild bananas. Hybrid bananas are being created in the hope of generating a new variety with strong resistance to diseases. Some believe the best hope for a more resilient banana is through genetic engineering. However, the resulting fruit also needs to taste good, ripen in a predictable amount of time, travel long distances undamaged, and be easy to grow in great quantities. Currently, no cultivar or hybrid meets all of these criteria.

Australian quarantine

In Queensland, a farm in Tully, 1500 km north of Brisbane, was quarantined and some plants were destroyed after TR4 was detected on March 3, 2015. After an initial shutdown of the infected farm, truckloads of fruit left in April with harvesting allowed to resume under strict biosecurity arrangements. The government says it is not feasible to eradicate the fungus. Researchers like Wageningen's Kema say the disease will continue to spread, despite efforts to contain it, as long as susceptible varieties are being grown.[22] The disease was again detected in Tully in July 2017, prompting Biosecurity Queensland to impose quarantine conditions.[23]

Spread to Colombia

In August 2019, authorities in Colombia declared a national emergency after confirming that the Panama disease had reached Latin America. "Once you see it, it is too late, and it has likely already spread outside that zone without recognition," said one expert quoted by National Geographic.[8]

Disease management

Currently, fungicides and other chemical and biological control agents have proven fairly unsuccessful, or only successful in vitro or in greenhouses, in the face of Panama disease of bananas. The most commonly used practices include mostly sanitation and quarantine practices to prevent the spread of Panama disease out of infected fields. However, the most effective tool against Panama disease is the development of banana plants resistant to Fusarium oxysporum f. sp. cubense.[9] The clonal reproduction of banana has led to a consequential lack of other varieties. Efforts are being made to produce resistant varieties, but with bananas being triploids which do not produce seeds, this is not an easy task. Creating clones from tissue cultures, rather than suckers, has proven somewhat successful in breeding resistant varieties, although these tend to have decreased success in stress-tolerance, yield, or other beneficial traits necessary for commercial varieties.[16] Nevertheless, these efforts are leading to the best control measure for Panama disease of banana.

Recently, an R gene (RGA2) was transformed into Cavendish bananas which showed disease resistance to Fusarium wilt tropical race 4. One specific transformed line, which consisted of eight plants, showed resistance in the field for all of them. The field trial lasted three years and the plants exhibited a yield drag.[24]

Taiwanese researchers believe that the onset of TR4 was linked to soil degradation caused by the use of chemical fertilizers.[25]

Banana breeding impeded by triploidy

One major impediment to breeding bananas is polyploidy; Gros Michel and Cavendish bananas are triploid and thus attempts at meiosis in the plant's ovules cannot produce a viable gamete. Only rarely does the first reduction division in meiosis in the plants' flowers tidily fail completely, resulting in a euploid triploid ovule, which can be fertilized by normal haploid pollen from a diploid banana variety; a whole stem of bananas would contain only a few seeds and sometimes none. As a result, the resulting new banana variety is tetraploid, and thus contains seeds; the market for bananas is not accustomed to bananas with seeds. Experience showed that where both meiosis steps failed, causing a heptaploid seedling, or when the seedling is aneuploid, results are not as good.

Second-generation breeding using those new tetraploids as both parents has tended not to yield good results, because the first generation contains the Gros Michel triploid gene set intact (plus possibly useful features in the added fourth chromosome set), but in the second generation, the Gros Michel gene set has been broken up by meiosis.

The Honduras Foundation for Agricultural Research cultivates several varieties of the Gros Michel. They have succeeded in producing a few seeds by hand-pollinating the flowers with pollen from diploid seeded bananas.[26]

See also

References
  1. Ploetz, R. C. (2015). "Fusarium Wilt of Banana." Phytopathology 105(12): 1512-1521.
  2. Ploetz, R. C. (2006). "Panama disease, an old nemesis rears its ugly head: part 2, the cavendish era and beyond." Plant Health Progress: 1-17.
  3. Ordonez, N., M. F. Seidl, C. Waalwijk, A. Drenth, A. Kilian, B. P. Thomma, R. C. Ploetz and G. H. Kema (2015). "Worse comes to worst: bananas and Panama disease—when plant and pathogen clones meet." PLoS pathogens 11(11): e1005197.
  4. Garcia-Bastidas, F., N. Ordonez, J. Konkol, M. Al-Qasim, Z. Naser, M. Abdelwali, N. Salem, C. Waalwijk, R. C. Ploetz and G. H. J. Kema (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): 694-694.
  5. Hung, T. N., N. Q. Hung, D. Mostert, A. Viljoen, C.-P. Chao and A. Molina (2017). "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: PDIS-08-17-1140-PDN.
  6. Chittarath, K., D. Mostert, K. S. Crew, A. Viljoen, G. Kong, A. Molina and J. E. Thomas (2017). "First report of Fusarium oxysporum f. sp. cubense tropical race 4 (VCG 01213/16) associated with Cavendish bananas in Laos." Plant Disease: PDIS-08-17-1197-PDN.
  7. Ordonez, L. N., F. Garcia-Bastidas, H. B. Laghari, M. Y. Akkary, E. N. Harfouche, B. N. al Awar and G. H. J. Kema (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): 209-210.
  8. Karp, Myles (12 August 2019). "The banana is one step closer to disappearing". National Geographic. Retrieved 16 August 2019.
  9. Perez-Vincent, Luis; Dita, Miguel A.; Martinez-de la Parte, Einar (May 2014). Technical Manual: Prevention and diagnostic of Fusarium Wilt (Panama disease) of banana caused by Fusarium oxysporum f. sp. cubense Tropical Race 4 (TR4). Food and Agriculture Organization of the United Nations.
  10. Ploetz, R. C. (2006). "Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense." Phytopathology 96(6): 653-656.
  11. Snyder, W. C. and H. Hansen (1940). "The species concept in Fusarium." American Journal of Botany: 64- 67.
  12. Baayen, R. P., K. O'Donnell, P. J. M. Bonants, E. Cigelnik, L. Kroon, E. J. A. Roebroeck and C. Waalwijk (2000). "Gene genealogies and AFLP analyses in the Fusarium oxysporum complex identify monophyletic and nonmonophyletic formae speciales causing wilt and rot disease." Phytopathology 90(8): 891-900.
  13. Drenth, A. and D. I. Guest (2016). Fungal and Oomycete Diseases of Tropical Tree Fruit Crops. Annual Review of Phytopathology, Vol 54. J. E. Leach and S. Lindow. 54: 373-395.
  14. Ploetz, R. C. (2005). "Panama disease, an old nemesis rears its ugly head: part 1, the beginnings of the banana export trades." Plant Health Progress(December): 1-10.
  15. Burton, Reg (2015-03-04). "Panama disease threatens NQ bananas". Fairfax Media.
  16. Hwang, Shin-Chuan; Ko, Wen-Hsuing (June 2004). "Cavendish Banana Cultivars Resistant to Fusarium Wilt Acquired through Somaclonal Variation in Taiwan". Plant Disease. 88 (6): 580–588. doi:10.1094/pdis.2004.88.6.580. PMID 30812575.
  17. M J Carlile, S C Watkinson, G W Gooday, 2001, Parasites and Mutualistic Symbionts in 'The Fungi (Second Edition)' Eds: same as authors, Academic Press, pp 363-460,
  18. "Fusarium oxysporum f. sp. cubense". ProMusa. July 2017. Retrieved 25 October 2017.
  19. REYNOLDS, MATT. "A Fungus Could Wipe Out the Banana Forever". Wired. Retrieved 26 February 2020.
  20. https://www.oirsa.org/contenido/biblioteca/PlandecontingenciacontraFocR4TOIRSA.pdf
  21. "Tropical race 4 - TR4".
  22. Sedgman, Phoebe. "There Might Be No Saving the World's Top Banana". Bloomberg.com. Retrieved 2015-06-06.
  23. McKillop, Charlie (13 July 2017). "Panama disease outbreak on Queensland banana farm prompts quarantine restrictions". Australian Broadcasting Corporation. Retrieved 27 July 2017.
  24. Dale, James; et al. (November 14, 2017). "Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4". Nature Communications. 8 (1): 1496. Bibcode:2017NatCo...8.1496D. doi:10.1038/s41467-017-01670-6. ISSN 2041-1723. PMC 5684404. PMID 29133817.
  25. Chia-nan, Lin. "ICDF is helping other nations with banana disease". taipeitimes.com. Taipei Times. Retrieved 1 March 2020.
  26. Carla Helfferich (1990). "Battling for Bananas". Alaska Science Forum. Archived from the original on 2008-02-23. Retrieved 2008-06-02.

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