Panama Disease in Bananas

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Background

Figure 1. A Cavendish banana plant exhibiting the discolred rot characteristic of Panama disease. [17]
Figure 2. A plate showing F. oxysporum growth. [18]

Dylan Barrett-Smith

Panama disease is a fungal borne pathogen first reported on an Australian banana farm in 1876 [1]. The disease causes fusarium wilt in banana plants, ultimately leading the death of the crop. Panama disease is caused by the fungal pathogen Fusarium oxysporum, of the Ascomycota phylum. There are different strains, or "races", of the fungus known to infect specific types of banana plants [1]. The disease has been responsible for two worldwide die-offs of banana plants, the second of which is ongoing. These epidemics have been responsible for the loss of hundreds of thousands of hectares of plantation land area and millions of dollars worth of dead crops [1,7,10].

To date, there is not a fungicide or other method known to be effective in combatting F. oxysporum [1]. The disease is subject to a large amount of current agricultural research in an attempt to deter or stop the further spread of the disease to non-infected areas, as well as devising a genetic resistance to the pathogen [1-11]. As of 2017, Panama disease infected Cavendish banana plants have been reported in East Africa, Asia, the Middle East, and Australia [4]. Without significant progress in effective treatments for the disease, the pathogen is expected to continue to cause further economic and agricultural damage to the banana industry as well as endanger the Cavendish banana variety as a world food staple [2,4].

History

Panama disease was first reported in Australia in 1876. However, the widespread appearance of the fusarium wilt was first noted in Panama, thus giving the disease its name [1]. At this time, the dominant dessert banana variety was the "Gros Michel". Widely cultivated in the Americas, Asia, Australia and Africa, the "Gros Michel' was ubiquitous in the banana industry [1]. Throughout the first half of the 20th century, large scale epidemics occurred throughout the Banana growing agricultural region located on either side of the equator [7]. The recognition that F. oxysporum was the microbial cause of the fusarium wilt in banana plants occurred in 1910 [1]. By the halfway point of the 20th century, the disease had rendered a vast amount of banana plantation acreage unusable. Plantations were abandoned, other fruits were instead cultivated, or new lands were planted that were still considered to be free of the fungus [1]. The advent of large scale agricultural transportation via trains, cargo ships, and paved roadways aided in the spread of the disease to previously non-infected areas as the century progressed [1].

The 1950s brought about the near collapse of the commercial dessert banana industry. However, at this time a different variety of bananas, known as the Cavendish variety, were discovered to be growable on plantations previously devastated by the disease. The United Fruit Company, which recently had devoted a large amount of research funds to limiting the spread of the disease, scaled back such efforts with the emergence of the Cavendish as a viable alternative [1]. The Cavendish is more fragile to environmental stressors, and to damage from transport, as compared to the 'Gros Michel' [4]. Additionally, the Cavendish banana was seen as less sweet, and therefor less desirable in Western markets. However, selective breeding gave the Cavendish the distinctive flavor it is currently known for [4]. Cavendish bananas rapidly became the dominant variety cultivated due to the perception that the variety was entirely resistant to F. oxysporum infection. Contrary to this belief, Cavendish bananas were already being infected by a different strain of the fungus in the 1960s in Taiwan. This new strain, known as Tropical Race 4 (TR4), has caused the demise of banana plantations throughout Southeast Asia and China [1]. It has additionally been reported in the Australian province of Queensland since the beginning of the 2000s. Today, nearly all exported dessert bananas are of the Cavendish variety. Panama disease has not been reported on Cavendish plantations in Latin America at this point in time [14].

Fusarium oxysporum and Banana Cultivation

Figure 3. A phylogenetic tree constructed based on mapped VGCs showing a split into two distinct clades. (From Ordonez et al., 2015) [1]

Fusarium oxysporum is a fungal species that is nearly ubiquitous in the world's soils [13]. The fungus can be neutral, beneficial, or pathogenic to local plant species depending on the ecological makeup of the habitat [13]. In appearance, the fungus is generally white, forming meshed clusters upon growth through asexual reproduction (Figure 2). There are dozens of strains of the fungus, including those characterized that affect pea, sweet potatoes, tomatoes, and other crops [13]. In particular, Fusarium oxysporum f.sp. cubense (FoC) causes the fusarium wilt known to infect banana plants [1]

F. Oxysporum f.sp. cubense has further been divided into strains, or "races" based on disease susceptibility in different types of banana plants [1]. The races are divided as follows:

Race 1: Affects 'Gros Michel', lady finger, sugar, and Ducasse banana plants [10]

Race 2: Affects "cooking" banana plants [10]

Race 3: Does not affect banana plants [8]

Race 4: Affects Cavendish banana plants, among other types [10]

Race 1 is responsible for the large scale die-off of 'Gros Michel' banana plants during the first half of the 20th century [10]. Race 2 holds importance for local banana markets, the final destination for the majority of bananas grown worldwide today [12]. Cooking bananas are a staple in many subtropical and tropical countries around the world. Because of this, the infection of cooking banana plants from the fungus represents a loss of a dietary staple for many areas [10]. Race 4 can further be broken down into two strains of the fungus. Subtropical race 4 fungus is present in eponymous regions, but does not pose an immediate threat to the banana industry at this time [10]. Tropical Race 4 (TR4) is the strain of the fungus currently subject to the most scientific research, industry concern and media scrutiny [1-5]. As previously noted, the strain has caused massive destruction of plantations in Asia and Australia, up to 100,000 hectares by one estimate [1]. The TR4 has been responsible for collapse of the Taiwanese banana industry [14]. Recent genetic research has shown that TR4 is a single pathogen clone [1]. This finding is based on the fact that a comparison of TR4 cultures from the Middle East and the Philippines showed an extremely small single nucleotide polymorphisms (SNPs) incidence of approximately .01% [1]. In addition, DarTseq markers between the samples were highly shared [1]. These findings support the hypothesis among scientists that the race emerged at single location, most likely Taiwan, before spreading across the Asian continent [1]. Different categorization methods have been used by scientists in lieu of the "race" categorization of FoC strains to generate a more complete phylogenetic tree [1]. To date, 24 vegetative compatibility groups (VCGs) have been noted [1]. These VCGs can further be divided into two distinct clades (Figure 3).

Banana plants belong to the genus Musa and are grown in more than 100 countries around the world [12]. Bananas are the largest herbaceous flowering plant with heights of more than 20 feet, depending on the variety [15]. Plants of the Musa genus are originally native the area presently called Indonesia but have been cultivated in Southeast Asia for 7,000 years [3]. There are approximately 70 species of bananas and plantains, a distinction that is common in some countries and absent in others [15]. They represent a dietary staple in many of the world's tropical and subtropical countries [4]. Each year, more than 140 million tons of bananas are produced with the vast majority not being exported [12].

Pathogenesis and Disease Management

Figure 4. A banana plantation in South Africa being fumigated using a combination of methyl bromide and chloropin. [7]
Figure 5. A sign in Queensland, Australia warning workers and farmers that the pictured plantation is under quarantine. Similar measures have been implemented in a number of countries. [16]

F. oxysporum can spread through a variety of channels. The most important of these is via infected plants [8]. As plant material is moved around plantation areas, on both a local and international level, oxysoporum spores can infect previously healthy plants. The fungus can also spread through soil, or through roots, causing the rapid movement of the disease across agricultural settings [8]. Additionally, agricultural equipment, clothing, packing boxes, and other non-living materials can spread the fungus [1,8]. Spores of the fungus have been reported to live for more than 30 years within certain soil types [8].The mode of infection for the fungus is through the vascular root system of the plant [7,8]. The fungus may then spread through the xylem of the banana plant, affecting the plants ability to remain hydrated. The fungus clogs the channels through which water normally travels. This water deficiency leads to what is commonly known as Fusarium wilt [7]. Plant leaves appear yellow in color, and display signs of intense wilting. Stems can also show splitting at the base or farther up the trunk. The presence of environmental stressors increases the efficacy of the infection, and the large amount of energy devoted to developing fruit can cause the first external symptoms of wilt to emerge [8]. Internally, the vasculature of the plant is rotted and discolored (Figure 1) [8].

Because banana plants are reproduced asexually in agricultural settings through tissue culture, each popular strain is a genetic clone. This widespread monoculture practice leaves Cavendish banana crops worldwide highly susceptible to TR4. Because of this, F. Oxysporum will be equally effective in infecting a banana plantation in Thailand, as the fungus would be in infecting a plantation in China [1]

Because there is not a known cure for Panama disease in bananas, managing the disease is extremely difficult. Instead, agricultural departments often stress prevention as the best defense against disease infection [8]. Laws and regulations limiting the movement of plant materials in known infected and vulnerable areas helps to prevent the spread of the disease to non-infected plantations and regions [8]. Biosecurity practices also aid in preventing the spread of disease. The frequent washing of equipment, farm personnel clothes, and other materials that can carry the fungus are some measures currently in place (Figure 5) [1,8]. It is further recommended that trees suspected to be infected by oxysporum not be cut down as the slicing of the plant xylem promotes the spread of the fungal spores [8].

Certain partially resistant strains of the Cavendish variety have been used in conjunction with responsible farming practices to a certain degree of success in parts of Asia. However, these practices also incur higher costs on the farms themselves [4]. One extreme form of F. oxysporum eradication has been practiced in South Africa in recent years. By covering specific areas of the plantation with tarps and subsequently fumigating the ground with methyl bromide, and chloropin, one site eradicated the fungus for 3 years (Figure 4) [11]. However, the field was soon recolonized by oxysporum, revealing the ineffectiveness of this practice [11]. Other management methods that have been attempted include heat treatment of ground soil, and the injection of banana plants with a variety of anti-fungal compounds [7].Certain soil types have been reported to be less susceptible to Panama disease proliferation. Clay based soils have shown high levels of disease suppression in certain areas [7]. Additionally, certain biological based controls, such as the introduction of other fungal species, have been attempted to mixed results [7].

Current Research

Figure 6. The effect of different siRNA techniques on F. Oxysporum conidiospore count. VEL and FtF1 show a signifigant reduction in spore count which the authors consider a sign of resistance in the plants. (From Ghag et al., 2014) [9]

The importance of the banana as both global cash crop and as a local food staple has meant that agricultural departments, agricultural companies, and other entities involved in the banana business have begun to support research into the TR4 strain and the possibility of genetic resistance [5,8,9,10]. Because early detection of the disease is essential to limiting its spread, and the cutting of trees to examine for internal signs (which appear prior to external symptoms) is not recommended, a fast and efficient method is needed to determine pathogen presence [6,8]. In 2010, a molecular test was published which was described as the "best option for rapid and reliable detection and monitoring of TR4" [6]. The test is based on presence of two SNPs in the IGS region of the genome. Using PCR, this test can detect specifically the presence of TR4 and allows agricultural departments to work in conjunction with local farmers to quickly determine if a plantation is infected [6].

Over the course of the last decade, genetic engineering has emerged as the most viable solution to the TR4 pandemic [9]. There have been attempts made at altering genes in the Cavendish genome that suppress fungal activity. However, because of the high rate of mutation in fungus pathogens such as F. oxysporum, such transgenic plants are unlikely to continuously remain resistant [9]. To overcome this predicament, researchers in India instead attempted to silence genes in F. oxysporum through siRNAs. Previous research in the field of plant pathogen siRNAs engineering has shown that such RNAs transfer from host to the fungus. Thus, by selecting for essential F. oxysporum genes to be silenced via intron hairpin RNA (ihpRNA)-mediated expression of small interfering RNAs (siRNAs), resistance can be conferred [9]. Researchers selected two crucial proteins, velvet (VEL), and Fusarium transcriptase factor 1 (FTF1), to be the target of silencing. Following the insertion of siRNAs, banana plants were grown followin in lab conditions. As seen in Figure 6, both VEL and FTF1 silenced plants showed continued resistance through 8 months of monitoring, on the basis of a signifigantly reduced spore count. Using transgenic hairpin RNAs to silence pathogenic genes has previously been used to confer disease resistance from other agricultural diseases [9]. Because this engineering strategy targets genes which are vital and inherently necessary for the fungus to cause Panama disease, it is extremely unlikely that resistance can be evolved to overcome these silencings [9]. A difficulty in engineering or discovering new cultivars of TR4-resistant plants lies in consumer approval. By altering genetic sequences, researchers may be inadvertently changing the taste of the crop. Cooking bananas, which are resistant to TR4, would not sell in Western markets as they do not possess the 'dessert' taste that consumers are used to from Cavendish varieties. The balance of a sweet tasting banana that is resistant to TR4 and agriculturally viable is the eventual goal of researchers altering genetic sequences [7].

Other current research involves the sequencing of genomes of cavendish varieties that appear to be more resistant to oxysporum infection [5]. By sequencing genomes and looking for differences in the genetic code, resistance mechanisms can be discovered which can then be implemented into genetic engineering strategies [5]. In 2013, a research team of Chinese scientists published findings of this sequencing [5]. Comparing the highly susceptible 'Brazilian' cultivar and the more resistant 'Yueyoukang 1" cultivar, the researchers determined differences in transcription at different timeframes following infection. The 'Yueyoukang 1' cultivar showed a more intense and efficient defense response when compared to the 'Brazilian' cultivar. This is based on the activation of defense genes associated with 'plant-pathogen interaction' as well as 'plant hormonal signal transduction' [5]. The fast activation of these genes allows for the plant to stave off infection from the fungus. Additionally, genes associated with 'hypersensitive' (HR) reaction were found in greater number in the 'Brazilian' variety. The researchers believed that this increased presence of HR genes may be negatively associated with warding off oxysporum infection [5].

Another area of research has been with that of wild varieties of banana that may possess partial or full resistance to the disease. There are more than 70 recognized species of bananas with more likely to be unnamed or discovered in the wild [3,15]. By identifying genetic differences between wild banana species and domesticated varieties, it is possible that researchers can insert genes that confer resistance into domestic varieties. In 2012, Musa acuminata malaccensis, a wild species of banana, was discovered to be TR4-resistant [3]. The 523-mega base genome of the species was published, representing a trove of genetic data for research into resistance genes [3].

Future Prospects and Conclusion

As of 2017, no viable cure has been found for Panama disease [1]. Because of this, many researchers believe that the future prospects of the Cavendish banana remaining the most popular exported dessert variety of banana are diminishing [2,4]. Of particular concern are small-scale local banana farming operations which depend on the Cavendish as the sole source of income [4]. Were TR4 to reach Latin America and the Caribbean, where more than 80% of the world's exported bananas are grown, the economic effects would be devastating [4]. Additionally, a report published on the potential economic impact of TR4 in Australia puts annual loses at more than $138 USD per year in the near future [2]. These unfortunate economic prospects are likely to spread to other parts of the banana producing world if a true solution to the Panama disease pandemic is not found in the near future [2]. The TR4 strain of F. oxysporum has been identified in three of the ten largest banana producing countries [4]. Many countries have imposed strict guidelines on the transport of bananas in addition to other quarantine measures [4, 8].

References


[1] Ordonez, N., Seidl, M.F., Waalwijk, C., André, D., Kilian, A., Thomma, B.P.H., Ploetz, R.C., Kema, G.H.J. "Worse Comes to Worst: Bananas and Panama Disease- When Plant and Pathogen Clones Meet." PLOS Pathogens. 2015. Volume 11(11). p. 1-7.

[2] Cook, D.C., Taylor, S.T., Meldrum, R.A., Drenth, A. "Potential Economic Impact of Panama Disease (Tropical Race 4) on the Australian Banana Industry." Journal of Plant Diseases and Protection. 2015. Volume 122(5), p. 229-237.

[3] D'Hont, A. et al. "The Banana (Musa acuminata) genome and the evolution of monocotyledonous plants." Nature. 2012. Volume 488, p. 213-217.

[4] Butler, D. "Fungus Threatens Top Banana. News, Nature. 2013. Volume 504, p. 195-196.

[5] Bai, T.T., Xie, W.B., Zhou, P.P., Wu, Z.L., Xiao, W.C., Zhou, L., Sun, J., Ryan, X.L., Li, H.P. "Transcriptome and Expression Profile Analysis of Highly Resistant and Susceptible Banana Roots Challenged with Fusarium oxysporum f. sp. cubense Tropical Race 4." PLOS One. 2013. Volume 8(9), e73945

[6] Dita, M. A., Waalwijk, C., Buddenhagen, I. W., Souza Jr, M. T. and Kema, G. H. J. "A molecular diagnostic for tropical race 4 of the banana fusarium wilt pathogen." Plant Pathology. 2010. Volume 59, p. 348–357.

[7] Ploetz, R.C. "Panama Disease: A Classic and Destructive Disease of Banana." Plant Health Progress. 2000.

[8] "Panama Disease Overview" Queensland Government: Department of Agriculture and Fisheries.

[9] Ghag, S.B., Shekhawat, U.K.S., Ganapathi, T.R. "Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana." Plant Biotechnology Journal. 2014. Volume 12, p. 541-553.

[10] Ploetz, R.C. "Panama Disease: An Old Nemesis Rears its Ugly Head Part 2: The Cavendish Era and Beyond" American Phytopathology Society. 2005.

[11] Herbert, J. A., and Marx, D. 1990. "Short-term control of Panama disease in South Africa." Phytophylactica. 1990. Volume 22, p.339-340.

[12] FAOSTAT (2013) FAO statistical database.

[13] Michielse, C.B., Rep, M. "Pathogen Profile Update: Fusarium oxysporum." Molecular Plant Pathology. 2009. Volume 10(3), p. 311-324.

[14] Molina, A.B., Fabregar, E., Sinohin, V.G., Yi, G. and Viljoen, A. 2009. "Recent occurrence of Fusarium oxysporum f. sp. cubense Tropical Race 4 in Asia. Proceedings of the International ISHS-ProMusa Symposium on Recent Advances in Banana Crop Protection for Sustainable Production and Improved Livelihoods" White River, South Africa, 10-14 September 2007. Jones, D.R. and Van den Bergh, I. (eds). Acta Horticulturae 828:109-116.

[15] "World Checklist of Selected Plant Families." Royal Botanic Gardens, Kew. Keyword: "Musa"

[16] Vlasic, Kimberly. "Panama Disease Spread another Blow to Tully Banana Farmers" The Cairn Post. October 8, 2015.

[17] "Panama Disease in Bananas: Frequently Asked Questions." Government of Western Australia: Department of Agricultural and Food. 2015.

[18] Tilley, Nicola. "Panama Disease" Edible Geography. March 4, 2010.



Authored for BIOL 238 Microbiology, taught by Joan Slonczewski, 2017, Kenyon College.