Tropical race 4
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 and distribution
In Taiwan, symptoms of Fusarium wilt on Cavendish cultivars were first observed in 1967.8 In 1972, the results of pathogenicity tests suggested that the isolates belonged to race 1,9 but isolates tested in 1977 were designated as race 4.8 In 1989, a previously undescribed VCG, designated VCG 01213, was identified in samples from Taiwan.10
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 Malaysia.11 Ivan Buddenhagen hypothesized that TR4 was probably already present in the soil when the plantations were set up and had been introduced to Taiwan from banana plants collected in the region.11 His theory is that TR4 evolved as an endophyte in Musa acuminata ssp. malaccensis, one of the wild ancestors of domesticated bananas.12
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By the end of the 20th century, TR4 had been found in Taiwan, Malaysia13 , Indonesia (Java, Sumatra, Sulawesi, Halmahera, Kalimantan14 on the island of Borneo, and Papua Province15 on the island of New Guinea), mainland China (Guangdong16 , Hainan17 , Guangxi18 , Fujian19 20 and Yunnan21 ), and Australia (Northern Territory22 ). In 2008, it was reported to be in the Philippines' island of Mindanao since at least 2005.23
Since then, the number of first reports has escalated, although they have not all been formally published.
Though not formally published, TR4 is in Oman.24 25 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 region, based on isolates collected in 2006.26 A 2014 survey revealed another infected area north of the original outbreak.27
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 Mozambique.28 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).29
In 2015, TR4 was reported to be in Queensland, Australia,30 31 in Lebanon where symptoms were first observed in 2013,32 and in Pakistan where symptoms were first observed in 2012.33 An analysis of isolates from Pakistan and the Phillipines showed that they were closely related.34 The incursion in Lebanon has also been shown to be associated with the one in Jordan.34
In 2017, TR4 was reported in Laos where symptoms had been observed in 201635 and Vietnam where symptoms were first observed in 2014.36
In 2018, TR4 was confirmed to be in Myanmar where symptoms were observed during a survey in 2016.34 The analysis of isolates from Laos, Vietnam and Myanmar provided evidence that the particular TR4 strain in these countries was likely introduced from China.34
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 2016.37 After taking measures to contain the incursions, the NPPO declared that the fungal strain had been eradicated from Israel.38 The declaration drew comments that TR4 had been contained rather than eradicated.39 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 area.40
In 2018, TR4 was officially reported to be in India, based on isolates collected in the state of Uttar Pradesh in 2017.41 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 201942 , by which time it had spread to the states of Uttar Pradesh, Madhya Pradesh and Gujarat.43
In August 2019, the Instituto Colombiano Agropecuario (ICA) confirmed the presence of TR4 in an area of 175 ha in Colombia's La Guajira department.5 Symptomatic plants had been spotted earlier and the area quarantined on 11 June. It is the first report of TR4 in Latin America.44
Suspected cases of Fusarium wilt in a plantation operated by a Chinese company were reported in June 2019 in the Chiang Rai province of Thailand.45 Since Chinese companies operating abroad typically set up plantatations of Cavendish bananas to supply the Chinese market, the disease would be most likely caused by TR4.
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.46
In 2020, TR4 was officially reported to be present on the island of Grande-Terre, in the French overseas department of Mayotte.47 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.48 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.49
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)50 and 'Pisang Mas'. The often cited figure that TR4 affects cultivars that account for more than 80% of the world's banana production51 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.52 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.53 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/3x54 ) 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 TR455 . 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 TR456 . 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) did57 .
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 test58 . 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 pathogen59 .
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)55 . Chinese leeks has also been used as an intercrop60 .
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 fungus61 62 (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 TR455 .
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 TR456 . 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 planting63 . The one exception was Ibwi (ITC146564 ), whose ploidy (2x/3x)65 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) did66 .
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 67 , 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 Territory68 .
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 TR469 had taken immediate action to contain the fungal strain when it first showed up in an area: Australia in 201570 and Israel in 201637 .
Regulatory framework
- 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 TR471 .
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 farm72 . 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 pathways72 .
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 zoning73
. 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®74 75 76 .
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 arrive77 .
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 Territory78 .
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 provinces79 and at least 3 countries in the Greater Mekong area34 .
In the Philippines, the full extent of the damage in Cavendish plantations is unknown. In 2014, the Mindanao Banana Farmers and Exporters Association, which represents small-scale farmers growing Cavendish cultivars for the export market, reported that about 5,900 hectares of their members’ aggregate plantation area had been infected, including 3,000 hectares that have been abandoned80 . Some growers say their farm was infected by run-off from a nearby large commercial farm81 . In 2015, some 15,500 ha (32% of the Cavendish production area in the Davao Region) were affected by TR482 .
In Africa, by the time TR4 was officially reported in 2013 to be present in an export plantation of northern Mozambique,4 the pathogen had been spreading for a while and the disease had entered the epidemic phase. From 5,656 symptomatic plants (out of a total of more than 2.5 m plants) surveyed six months after the announcement, the number of symptomatic plants was 576,760 in September 201583 . The disease reduced the production area from 1,500 ha in 2014 to 900 ha in 201629 . 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 201829 .
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 Mozambique84 , the African Consortium for TR4 (AC4TR4) was launched at a workshop held at the University of Stellenbosch in April 201485 .
Australia
Following the first confirmed case of TR4 in Queensland86 , Biosecurity Queensland, in partnership with the Australian Banana Growers' Council, set up a programme of surveillance and containment87 88 . 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 plants89 .
In 2018, after TR4 had been found in two other farms90 91 , 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 material92 ). 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 met93 .
In 2018, the Queensland Department of Agriculture and Fisheries released the review of Biosecurity Queensland's TR4 programme94 . It had commissioned the independent review to establish on what basis the programme should continue95 .
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 only71 .
The banana research network for Latin America and the Caribbean, MUSALAC, has organized training on quarantine pests, with a special emphasis on TR496 .
National authorities have been on high alert since TR4 was reported in Colombia in 2019.
Global
In December 2013, a task force on TR4 was set up within the framework of the World Banana Forum97 . In December 2014, the FAO held a consultation with a group of international experts to agree on the framework for a global programme98 . 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 various projects on TR499 .
References
See also on this website
- Banana pathogens’ new names
- TR4 confirmed on a fifth property in Queensland, Australia
- TR4 in Mayotte
- TR4 in Turkey
- TR4 in Colombia