Fusarium oxysporum f. sp. cubense
Fusarium oxysporum f. sp. cubense (Foc) is one of more than 100 formae speciales (special forms) of the Fusarium oxysporum species complex of pathogenic as well as non-pathogenic 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 related genetically.1 An analysis of more than 200 isolates collected in Indonesia has led to the identification of 11 new Fusarium species2 one of which, Fusarium odoratissimum, includes the TR4 strain spreading globally on Cavendish cultivars3 .
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).4 Each VCG has its own characteristics in terms of aggressiveness and the banana cultivars that it attacks most readily. The VCG associated with tropical race 4 (TR4) — VCG01213/16 — was ranked as the greatest threat to banana production because of its lethal impact, wide host range and persistence in the soil.5
F. oxysporum has no known sexual stage. Variation in the fungus is thought to result from mutations.
In 1876, the author of the first report on the disease, J. Bancroft, speculated that it was caused by a fungus.6 Unaware of Bancroft's work, J.E. Higgins, an horticulturist at the Hawaii Agricultural Experiment Station, also proposed in 1904 that a fungus caused the disease.7
The plant pathologist Erwin F. Smith became the first person to isolate the pathogen from banana tissues he had received from Cuba.8 He reported his results at the first meeting of the American Phytopathological Society held in Boston in 1908.9 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 1919.10
In 1935, H. W. Wollenweber and O. A. Reinking recognized that Fusarium cubense was a variant of Fusarium oxysporum and renamed it Fusarium oxysporum variety cubense.11 It became Fusarium oxysporum f. sp. cubense in 1940, when W. C. Snyder and E. W. Hansen created special forms (formae speciales) to classify plant-pathogenic strains of Fusarium oxysporum.12
No sexual stage has been observed. Inside the plant, the fungus produces three types of asexual spores: microconidia, macroconidia and chlamydospores.
Chlamydospores are round, thick-walled resting propagules that are produced by the dying banana plant. Infection is initiated when they germinate in response to exudates from the roots and hyphae (long and branching filamentous structures collectively known as mycelium) penetrate the lateral roots.
Chlamydospores have a reputation for surviving for 30 years or more in soil, but it is more likely that the persistence observed in fields in which susceptible banana plants had not been grown for decades is the result of Foc living as endophytes and multiplying in alternative hosts, such as weeds13 14 . It has also been sugested that former fields of 'Gros Michel' that have been converted to Cavendish are still infective for susceptible cultivars because the Foc strains live as endophytes in the Cavendish cultivars15 .
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.
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 autoclaving16 .
It's still not clear how the fungus kills the plant. One hypothesis is fungus releases toxins into the plant, killing its cells. Another is that the fungus tricks the plant into killing its cells by triggering the natural process of programmed cell death that eliminates unwanted, damaged or used cells. The decaying plant tissues would then be used by the fungus as a food source17 .
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 plant18 .
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 exist19 . 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 2 strains prey on Bluggoe and closely related cooking cultivars.
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 Africa21 , as well as in some tropical growing areas such as Jamaica and Guadeloupe. Circumstantial evidence suggested that the limited damage was due to predisposing factors: low temperatures in the subtropics and edaphic factors in the tropics22 . 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 01213/16 VCG (see Vegetative compatibility below) associated with TR4 was first identified in isolates from Taiwan at the end of the 1980s15 . 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 VCG of the isolate (VCG0124) is associated with race 1 strains23 .
TR4 also attacks cultivars susceptible to races 1 and 2, and additional cultivars such as Barangan (Lakatan subgroup, AAA genome group)24 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.
For details on where TR4 has been found, go to the Musapedia page on TR4.
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)4 . 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 last number represents the order in which the VCGs were identified (0120, 0121, 0122 etc.). The race 1 isolate used to designate the first VCG0120 came from Australia4 . Some 24 VCGs have since been characterized worlwide.
The region with the greatest diversity of VCGs is Asia. A series of surveys documented 11 VCGs in the five banana-producing regions of mainland China25 , 3 VCGs and 4 isolates of unknown VCG in Indonesia's Lampung province26 , and 5 VCGs and 7 isolates of unknown VCG in Indonesia's West Sumatera province27 . A survey of 9 Asian countries reported 12 VCGs28 .
Tropical race 4 isolates belong to the VCG01213/16 complex, although other VCGs are also known to cause Fusarium wilt on Cavendish cultivars: the so-called STR4 strains that attack Cavendish bananas in the subtropics (0120, 0121, 0129 and 01211 in Australia; 0120 in South Africa and the Canary Islands and 0122 in the Philippines)15 . In India, VCG0124 isolates have also been extracted from Cavendish bananas exhibiting Fusarium wilt symptoms23 . In Latin America, VCG0124 isolates are classified as race 1 because they infect Gros Michel but not Cavendish bananas.
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