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Tropical race 4


Tropical race 4
Credit: ABGC
Credit: ABGC

Tropical race 4 (TR4) is the name of the fungal strain that causes Fusarium wilt (aka Panama disease) in Cavendish cultivars under the race concept, an informal rank under the one of forma specialis (special form). The special form for pathogens that cause Fusarium wilt on banana is Fusarium oxysporum f. sp. cubense. The concept of race was later introduced to distinguish the strains that are pathogenic to specific cultivars. In 2019, a taxonomic revision included TR4 as part of a new species, Fusarium odoratissimum.1 2

The term TR4 was coined to distinguish the strains that readily cause disease in Cavendish cultivars from the ones that need the presence of predisposing factors, such as low temperatures, to cause disease. The latter are known as subtropical race 4 (STR4). TR4 is associated with a particular vegetative compatibility group called VCG 01213, although other VCGs have also been reported to cause Fusarium wilt in Cavendish cultivars in the absence of predisposing factors3 .

TR4 has spread to most banana-producing countries in Asia. In 2013, it was reported in Mozambique4 and in 2019 in Colombia5 .

TR4 has a wider host range than just Cavendish cultivars. In addition to hitherto unaffected cultivars, such as 'Lakatan' and 'Pisang mas', it also causes disease in groups of cultivars susceptible to races 1 and 2, such as Gros Michel, Silk, Pome and Bluggoe.

Like all other soil-dwelling Foc strains, TR4 cannot be controlled using fungicides and cannot be eradicated from soil using fumigants. The capacity of TR4 to survive decades in the soil, along with its lethal impact and wide host range, are among the main reasons it was ranked as the greatest threat to banana production6 . To avoid further losses to the pathogen, the United Nations' Food and Agriculture Organization (FAO) has called on banana-producing countries to step up monitoring and reporting, and to contain suspected incursions to prevent the fungus from getting established7 .

Origin

There is no evidence that TR4 originated from a strain that overcame the resistance of Cavendish cultivars8 . The strain that became known as TR4 took scientists by surprise in the early 1990s when newly established commercial Cavendish plantations where promptly destroyed by Fusarium wil in areas of Malaysia and Indonesia with no history of Cavendish banana cultivation9 . The theory developped by Ivan Buddenhagen is that TR4 evolved as an endophyte in a local Musa acuminata ssp. malaccensis, one of the wild ancestors of domesticated bananas, and was in the soil when the plantation was set up10 .

Distribution

In Taiwan, symptoms of Fusarium wilt on Cavendish cultivars were first observed in 196711 . In 1972, the results of pathogenicity tests suggested that the isolates belonged to race 112 , but isolates tested in 1977 were designated as race 411 . In 1989, a previously undescribed VCG, designated VCG 01213, was identified in samples from Taiwan13 .

The vulnerability of Cavendish cultivars to  what would become known as TR4 was underscored in the early 1990s, when Fusarium wilt decimated newly established plantations of Cavendish bananas in Indonesia and Malaysia9 . The TR4 isolates introduced to Taiwan probably came from one of those places9 .

By the end of the 20th century, TR4 had been found in Taiwan, Malaysia14 , Indonesia (Java, Sumatra, Sulawesi, Halmahera, Kalimantan15 on the island of Borneo, and Papua Province16 on the island of New Guinea), mainland China (Guangdong17 , Hainan18 , Guangxi19 , Fujian20 21 and Yunnan22 ), and Australia (Northern Territory23 ). In 2008, it was reported to be in the Philippines' island of Mindanao since at least 200524

Since then, the number of first reports has increased exponentially, although they have not all been formally published.

Though not formally published, TR4 is in Oman25 26 . It seems to have been present since at least 2012.

In 2013, TR4 was reported to be in Jordan, the first official report of TR4 outside the Southeast Asia-Pacific region27 . A 2014 survey revealed another infected area north of the original outbreak28 .

At the end of 2013, TR4 was also reported to be in Africa, where it was confirmed to be in an export banana plantation located in northern Mozambique29 . The Matanuska farm in Nampula province filed for insolvency in 2018, after which it was bought by Jacaranda Agricultura Lda and renamed Jacaranda Monapo. In 2014, TR4 was reported to be present in two other Jacaranda farms (Lúrio, in Nampula, and Ocua, in Cabo Delgado province)30 .

In 2015, TR4 was reported to be in Queensland, Australia31 32 , as well as in Lebanon and Pakistan33 34 . An analysis of isolates from Pakistan and the Phillipines showed that they were closely related35 . The incursion in Lebanon has also been shown to be associated with the one in Jordan35 .

In 2017, TR4 was reported in Laos36 and Vietnam37 .

In 2018, TR4 was confirmed to be in  Myanmar35 . The analysis of isolates from Laos, Vietnam and Myanmar provided evidence that the particular TR4 strain in these countries was likely introduced from China35 .

In 2018, Israel's National Plant Protection Organization (NPPO) officially announced that TR4 had been found in two farms in Israel (the Carmel coastal plain and the eastern shores of Lake Galilee) in 201638 . After taking measures to contain the incursions, the NPPO declared that the fungal strain had been eradicated from Israel39 . The declaration drew comments that TR4 had been contained rather than eradicated40 . In 2019, the pest status was amended to "actionable, under eradication" following the discovery of TR4 at a number of sites close to the eastern/southern Lake Galilee area41 .

In 2018, TR4 was officially reported to be in India, based on isolates collected in the state of Uttar Pradesh in 201742 . However, wilting symptoms on Cavendish cultivars had previously been observed, in 2015, by a  banana grower from Barari village in the state of Bihar. Samples were collected in 2016 and TR4's presence in Bihar's Katikar and Purnea districts published in 201943 , by which time it had spread to the states of Uttar Pradesh, Madhya Pradesh and Gujarat44 .

In August 2019, the Instituto Colombiano Agropecuario (ICA) confirmed the presence of TR4 in an area of 175 ha in Colombia's La Guajira department5 . Symptomatic plants had been spotted earlier and the area quarantined on 11 June. It is the first report of TR4 in Latin America45 .

A suspected case of TR4 in a plantation operated by a Chinese company was reported in June 2019 in the Chiang Rai province of Thailand46 .

In 2019, TR4 was confirmed to be in Turkey. According to the first report in Plant Disease, symptoms of Fusarium wilt were first observed in March 2018 during a survey of banana greenhouses along the Mediterranean coast.47

In 2020, TR4 was officially reported to be present on the island of Grande-Terre, in the French overseas department of Mayotte.48 The fungus was found in 'Baraboufaka' (Bluggoe) and 'Kissoukari' (Silk) plants sampled from two adajacent plots in Poroani, a village in the southwestern part of the island. The symptoms were first observed in Semptember 2019.

TR4 is also present at the Eden Project's indoor rainforest biome in Cornwall, England.49 .It was first observed in the banana exhibit in 2009, after which the soil and plants were changed. It reappeared in 2015. The fungus was isolated from a symptomatic plant and its DNA sequenced.50

Host range

In addition to Cavendish cultivars, TR4 affects cultivars susceptible to races 1 and 2 as well as hitherto unaffected cultivars such as, 'Barangan' (Lakatan subgroup, AAA genome group)51 and 'Pisang Mas'. The often cited figure that TR4 affects cultivars that account for more than 80% of the world's banana production52 assumed that Plantains were also susceptible. At the time, however, the only Plantain-like material that had been evaluated against TR4 were hybrids produced by breeders.53 The reaction of the Plantains domesticated in Africa, along with another group of locally domesticated bananas, the East African highland bananas (EAHB), was not known. The first field screening of these two subgroups was conducted in 2011-2012 in the Philippines using accessions from the ITC genebank. Most of the accessions tested were slightly to moderately susceptible.54 Except for the 'Obubit Ntanga' Plantain accession that was still symptom-free after 10 months (a relatively short time given the perennial nature of most banana production), the disease incidence was below 5%, with the exception of 'Ibwi', for which the disease incidence was 29%. However, the ploidy of the ITC accession called Ibwi (2x/3x55 ) suggests that the material tested might not be the EAHB cultivar  'Ibwi'.

The FHIA improvement programme has produced hybrids that are resistant to races 1 and 4, while the Taiwan Banana Research Institute (TBRI) has released Giant Cavendish tissue-culture variants (GCTCV) that are partially resistant to TR456 . In field trials conducted in China, FHIA-01, FHIA-02, FHIA-18, FHIA-25, Pisang Jari Buaya, Rose (AA), and to a lesser extent GCTCV-119 and FHIA-03, have shown resistance to TR457 . In a field trial conducted in the Philippines, only 1% of the GCTCV-219 plants exhibited symptoms of Fusarium wilt in the second crop cycle, whereas none of plants of the Cardava cultivar (Saba subgroup) did58 .

Symptoms and diagnosis

The symptoms of a TR4 infection are the same as those caused by any other Foc strains (see symptoms of Fusarium wilt).

However, the wide host range of TR4 makes it difficult to diagnose TR4 on non-Cavendish bananas that are susceptible to other strains. For example, a Gros Michel infected with TR4 would not raise alarm because the assumption would be that it is infected with a race 1 strain.

The quickest way to confirm a TR4 infection is by analysing tissue samples using a TR4-specific PCR test59 . Fungal isolates can also be analysed to determine their vegetative compatibility group (VCG). The VCG associated with TR4 is 01213.

Modes of transmission

TR4 can be spread through infected planting material, infested soil and water. For more information, see the section on the modes of transmission of Fusarium wilt.

Disease management

Like all the other Foc strains, TR4 cannot be controlled using fungicides and cannot be eradicated from soil using fumigants. As a result, the spread of TR4 has led to an increase in research on biological control and the role of the soil microbial community in suppressing the pathogen60 .

Crop rotation with a non-banana crop that has anti-fungal activity has been used to reduce losses. In China, farmers have been growning bananas in the presence of TR4 by rotating them with Chinese leek (Allium tuberosum)56 . Chinese leeks has also been used as an intercrop61 .

The solution best adapted to the continued production of bananas in infested soils is replacing susceptible cultivars with resistant ones. However, given TR4's wide host range, virulence and persistence in the soil6 , experts stress the importance of preventing the spread of the fungus62 63 (see Preventing the spread of TR4).

Resistant cultivars

The FHIA improvement programme has produced hybrids that are resistant to races 1 and 4, while the Taiwan Banana Research Institute (TBRI) has released Giant Cavendish tissue-culture variants (GCTCV) that have been selected for their increased resistance to TR456 .

In field trials conducted in China, FHIA-01, FHIA-02, FHIA-18, FHIA-25, Pisang Jari Buaya, Rose (AA), and to a lesser extent GCTCV-119 and FHIA-03, have shown resistance to TR457 . Preliminary results from a field trial conducted in the Philippines in 2011-2012 suggest that EAHB and Plantain might be relatively resistant to TR4. The incidence of Fusarium wilt on the screened ITC accessions was generally low 75 weeks after planting64 . The one exception was Ibwi (ITC146565 ), whose ploidy (2x/3x)66 suggests that the accession might not be representative of the Ibwi cultivar. It is possible that the wrong accession was introduced to the ITC. In a separate field trial conducted in the Philippines, only 1% of the GCTCV-219 plants exhibited symptoms of Fusarium wilt in the second crop cycle, whereas none of plants of the Cardava cultivar (Saba subgroup) did67 .

Two genetic engineering strategies, one involving the introduction of a resistance gene isolated from a wild relative of the banana and the other of an anti-apoptosis gene derived from a nematode 68 , are being tested in Australia. Two of the evaluated lines were still free of the disease after three years of a field trial conducted in the Northern Territory69 .

Preventing the spread of TR4

Even though the threat posed by TR4 has been widely recognized, few TR4-free countries have taken the steps to prevent the entry of the fungal strain or to contain it when it was first detected. By 2018, only two of the 16 countries that are known to have TR470 had taken immediate action to contain the fungal strain when it first showed up in an area: Australia in 201571 and Israel in 201638 .

Regulatory framework

At the country level, several steps need to be taken, such as:
  • Designate TR4 as a quarantine pest;
  • Set up a monitoring system to promptly detect incursions;
  • Enact regulations that allow the national plant protection organisation to intervene on farms, including:
    • Conduct inspections;
    • Collect samples;
    • Enforce the destruction of plants.

Contingency plans are typically developed by the authorities responsible for planning and responding to incursions of pests and diseases. They cover the technical and regulatory aspects of confirming suspected cases of and stopping the pest or pathogen from getting established.

Generic contingency plans can also be developed. OIRSA, a regional plant protection organization, whose membership includes Belize, Costa Rica, the Dominican Republic, El Salvador, Guatemala, Honduras, Mexico, Nicaragua and Panama, developed one against TR472 .

Containment

At the farm level, containment (keeping the pathogen in) and exclusion (keeping the pathogen out) are two sides of the same coin. Except for the actions specific to isolating an infested area, the biosecurity measures aimed at preventing the fungus from escaping an infested farm are essentially the same as the ones growers can take to protect their farm73 . But whereas exclusion is the responsibility of the producer, containment can be legislated.

Exclusion

TR4 is mostly spread by infected planting material and contaminated soil and water. In Australia, the biosecurity measures banana growers have been encouraged to implement were designed to halt the movement of the pathogen along these pathways73 .

Click on photo for resources on how to protect a banana farm produced by Queensland Biosecurity (Photo by J. Daniells)
Click on photo for resources on how to protect a banana farm produced by Queensland Biosecurity (Photo by J. Daniells)

The primary line of defence is the exclusion of all non-essential visitors, vehicles and plant material from outside. This is part of a strategy to manage people and vehicle access that is called differential access zoning74 . For banana farms, three key zones are proposed:
1. The exclusion zone for vehicles that don’t need to enter the farm;
2. The separation zone for essential vehicles that are low risk (i.e. not associated with field production) and which are usually subjected to cleaning/disinfection procedures;
3. The farming zone, where farming activities take place, is physically separated from the other zones to manage the risk of cross-contamination.

Some of the actual practices put in place include physical barriers, facilities for footwear change at zone boundaries, and vehicle wash-down facilities that use disinfectants such as Farmcleanse®, Sporekill® or Domestos®75 76 77 .

These practices also provide a barrier to the entry of other pests, diseases and weeds. Managing the movement of water and soil can also have a beneficial impact on the environment.

Putting in place measures that reduce soil erosion, such as ground covers and grassed inter-rows,  would also lessen the severity of Fusarium wilt should it arrive78 .

Impact

The severity of the damage depends on interactions between the strain, its host and environmental conditions.

TR4 has devastated commercial plantations of Cavendish bananas in Taiwan, Indonesia, Malaysia and Australia’s Northern Territory79 .

In mainland China, the strategy of establishing Cavendish plantations in TR4-free areas to stay ahead of the disease has led to the spread of the fungus to all the main banana-growing provinces80 and at least 3 countries in the Greater Mekong area35 .

In the Philippines, the extent of the damage in Cavendish plantations has not been documented. The Mindanao Banana Farmers and Exporters Association, which represents small-scale farmers growing Cavendish cultivars for the export market, has reported that about 5,900 hectares of their members’ aggregate plantation area had been infected, including 3,000 hectares that have been abandoned81 . Some growers say their farm was infected by run-off from a nearby large commercial farm82 .

In the few instances in which losses to TR4 have been estimated, they amounted to 121 million USD in Indonesia, 253.3 million USD in Taiwan  and 14.1 million USD Malaysia83 .

In Africa, where TR4 was reported for the first time in 2013 in an export plantation of northern Mozambique, the number of symptomatic plants had risen to more than 570,000 (out of a total of more than 2.5 m plants) by September 201584 . The disease reduced the production area from 1,500 ha in 2014 to 900 ha in 201630 . That same year, Formosana was planted on 200 ha. In 2018, only these 200 hectares were still in production and the number of workers had been reduced from 2,500 in 2014 to 750 in 201830 .

For more information, see the section on the impact of Fusarium wilt.

Efforts to address the threat of TR4

Africa

Following the announcement that TR4 had been detected in Mozambique85 , the African Consortium for TR4 (AC4TR4) was launched at a workshop held at the University of Stellenbosch in April 201486 .

Asia

The Banana Asia-Pacific Network (BAPNET) is coordinating a number of TR4-related projects and activities in various Asian countries87 .

Australia

Following the first confirmed case of TR4 in Queensland88 , Biosecurity Queensland, in partnership with the Australian Banana Growers' Council, set up a programme of surveillance and containment89 90 . The farm was bought by the Australian Banana Growers Association in late 2016 with the objective of shutting down the farm and destroying all the banana plants91 .

In 2018, after TR4 had been found in two other farms92 93 , a system of certification was put in place for TR4-infested farms that meet the requirements for interstate and intrastate quarantine purposes (Inspection of bananas for freedom of soil and plant material94 ). The system allows accredited businesses to certify their fruit consignments without putting the wider industry at risk. Accredited farms will be visited by biosecurity officers to audit the fruit inspection process and ensure that biosecurity requirements are being met95 .

In 2018, the Queensland Department of Agriculture and Fisheries released the review of Biosecurity Queensland's TR4 programme96 . It had commissioned the independent review to establish on what basis the programme should continue97 .

Latin America and the Carribean

OIRSA, a regional organzation for plant and animal health, has 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 available in Spanish only98 .

The banana research network for Latin America and the Caribbean, MUSALAC, has been organizing training on quarantine pests, with a special emphasis on TR499 .

In 2014, the Caribbean Agricultural Research and Development Institute (CARDI) organized a seminar and a training workshop to raise awareness of the potential threat of TR4 as a key step to prevent its introduction to the Caribbean100 .

Global

In December 2013, a task force on TR4 was set up within the framework of the World Banana Forum101 . In December 2014, the FAO held a consultation with a group of international experts to agree on the framework for a global programme102 . The plan would work on three main fronts: preventing future outbreaks, managing existing cases, and strengthening international collaboration and coordination among institutions, researchers, governments and producers.

The Wageningen university & research centre in the Netherlands is leading three projects on TR4: INREF, KNAW-SPIN and PromoBanana103 .

References

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6 Ploetz, R.C. 2009. Assessing threats posed by destructive banana pathogens. Proceedings of the International ISHS-ProMusa Symposium on Recent Advances in Banana Crop Protection for Sustainable Production and Improved Livelihoods held in White River, South Africa, 10-14 September 2007. Jones, D.R. and Van den Bergh, I. (eds). Acta Horticulturae 828:245-252.
8 Heartbleed and the banana, published 18 April 2014 in the Under the peel blog of the ProMusa community.
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10 Under the peel blog post on the origin of TR4, published 18 December 2014
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13 R.C. Ploetz. 2018. Fusarium Wilt "in" Handbook of diseases of banana, abaca and enset. D.R. Jones (ed.). CABI, UK.
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26 Distribution of TR4 on the Banana Fusarium wilt in Africa website
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32 The 22 days that changed the Australian banana industry InfoMus@ News and analysis posted on 16 March 2015.
36 Chittarath, K., Mostert, D., Crew, K.S., Viljoen, A., Kong, G., Molina, A.B. 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.
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40 Comments on the declaration that TR4 had been eradicated from Israel on Mediawatch, Facebook and Twitter
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54 Risk assessment of Eastern African Highland Bananas and Plantains against TR4, a poster presented at the 2012 International Banana Symposium in Taiwan.
55 Ploidy of Ibwi in MGIS
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65 ITC1465 in MGIS
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69 Dale, J. et al. 2017. Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4. Nature Communications 8(1):1496.
70 In order of first reports: Taiwan, Malaysia, Indonesia, China, Australia, Philippines, Oman, Jordan, Mozambique, Lebanon, Pakistan, India, Israel, Laos, Vietnam and Myanmar.
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73 TR4 Grower Kit: resources to help banana growers protect their farm against an incursion of TR4.
74 The benefits of exclusion in TR4 as a driver of agroecological approaches in banana production.
75 Nel, B., Steinberg, C., Labuschagne, N. and Viljoen, A. 2007. Evaluation of fungicides and sterilants for potential application in the management of Fusarium wilt of banana. Crop Protection 26(4):697-705.
76 Meldrum, R.A., Daly, A.M., Tran-Nguyen, L.T.T. and Aitken, E.A.B. 2013. The effect of surface sterilants on spore germination of Fusarium oxysporum f. sp. cubense tropical race 4. Crop Protection 54:194-198.
77 Research findings of disinfectant trials for TR4 conducted by Australia's Department of Fisheries and Fisheries
78 TR4 as a driver of agroecological approaches in banana production, published by Jeff Daniells in InfoMus@'s Under the peel blog on 25 Octobre 2016.
79 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 held in White River, South Africa, 10-14 September 2007. Jones, D.R. and Van den Bergh, I. (eds.). Acta Horticulturae 828:109-116. ISHS, Leuven, Belgium.
80 Farquhar, I. 2012. Bananas in China. Report on a visit to three banana producing provinces of China by Dr. Iain Farquhar on behalf of Banana Link and the Steering Committee of the World Banana Forum. 35 pp.
84 Containing TR4 by Altus Viljoen, a presentation given at the 2015 Congress of the Australian Banana Idustry.
85 The year of TR4 published on 19 December 2013 in the ProMusa blog.
86 AC4TR4 on the website on Fusarium wilt in Africa
87 Website of the BAPNET network
89 Biosecurity Queensland's response to TR4
90 TR4 response on the website of the Australian Banana Grower's Council
91 Unprecedented banana farm buy-out in InfoMus@'s Mediawatch, 24 October 2016
92 [http://www.promusa.org/blogpost510-Second-TR4-incursion-in-Australia-s-Tully-Valley|Second incursion of TR4 in Queensland, Australia, published 26 July 2017 in Mediawatch
93 [http://www.promusa.org/blogpost533-Third-case-of-TR4-in-Queensland-Australia|Third case of TR4 in Queensland, Australia, published 8 February 2018 in Mediawatch
94 Inspection of bananas for freedom of soil and plant material Version 1 (30 July 2018) developed by Biosecurity Queensland in partnership with Biosecurity Solutions Australia
95 Bananas: TR4 affected farms benefit from new agreement, published 13 September 2018 in the North Queensland Register
98 Dita, M., Echegoy&eacute;n Ramos, P.E. and P&eacute;rez Vicente, L.F. 2013. Plan de contingencia ante un brote de la raza 4 tropical de Fusarium oxysporum f. sp. cubense En un pa&iacute;s de la regi&oacute;n del OIRSA. OIRSA, San Salvador, El Salvador. 155p.
99 TR4's transcontinental leap published in InfoMus@'s News and analysis section on 21 November 2013.
102 FAO and partners call for a global response to deadly banana disease published 23 December 2014. Retrieved 14 January 2015.
103 Research projects led by Wageningen University scientists

See also on this website

News and blogs on TR4:
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

Tropical race 4 grower kit, series of documents produced by Biosecurity Queensland to help Australian banana growers protect their farms
Contingency plan (in Spanish) on TR4 for OIRSA countries
Diagnostic manual and links to presentations given at a 2014 FAO-CARDI regional workshop on the prevention and diagnostic of Fusarium wilt
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
Research projects on Fusarium wilt that are managed by Wageningen University & Research Centre: fusariumwilt.org
Response to TR4 on the website of the Australian Banana Growers' Council
Response to TR4 on the website of Biosecurity Queensland
Banana Production at the Crossroads, video of a scientific session on the impact of TR4 at the American Phytopathological Society's 2015 Annual Meeting in Pasadena, California, USA.