Fusarium oxysporum f. sp. cubense
Fusarium oxysporum f. sp. cubense (Foc) is one of more than 100 formae speciales (special forms) of the soil-borne Fusarium oxysporum species complex of 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 necessarily related genetically1. F. oxysporum has no known sexual stage. Variation in the fungus is thought to result from mutations.
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)2. Each VCG has its own characteristics in terms of aggressiveness and the banana cultivars that it attacks most readily.
In 1876, the author of the first report of the disease, J. Bancroft, speculated that it was caused by a fungus3. Unaware of Bancroft's work, a horticulturist at the Hawaii Agricultural Experiment Station also proposed in 1904 that a fungus caused the disease4. The plant pathologist Erwin F. Smith became the first person to isolate the pathogen from banana tissues he had received from Cuba5. He reported his results at the first meeting of the American Phytopathological Society held in Boston in 19086. 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 19197. Fusarium cubense was recognized as a variant of Fusarium oxysporum and renamed Fusarium oxysporum f. sp. cubense in 19358.
Three types of asexual spores have been identified: microconidia, macroconidia and chlamydospores, with the latter acting as primary inocula.
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.
Chlamydospores are round, thick-walled resting propagules that can withstand extreme environmental conditions. They can persist in soil for indefinite periods of time (more than 30 years).
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 autoclaving9.
No sexual stage has been observed.
Mode of action
Scientists used to think that the fungus injected toxins into the plant, killing its cells. Instead, evidence suggests that the fungus tricks the plant into killing its cells by triggering the natural process of programmed cell death, which eliminates unwanted, damaged or used cells. The decaying plant tissues are then used by the fungus as a food source10.
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 plant11.
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 exist12. 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 Africa, as well as in some tropical growing areas such as Taiwan15, Jamaica and Guadeloupe. Circumstantial evidence suggested that, with the exception of Taiwan, the limited damage was due to predisposing factors: low temperatures in the subtropics and edaphic factors in the tropics16. 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 isolates in Taiwan were later shown to be associated with TR417. 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 isolate was not associated with either STR4 or TR418.
STR4 has been reported in the subtropical regions of Australia (southeast Queensland and northeast New South Wales), South Africa and Canary Islands19.
In addition to Taiwan, TR4 has been reported in peninsular Malaysia20 and Sarawak, Indonesia (Papua province21, Kalimantan22, Halmahera, Java, Sulawesi and Sumatra), mainland China (Guangdong23, Guangxi, Hunan, Hainan24), the Philippines25 and Australia (Northern Territory in 19972627 and Queensland in 201528). In 2013, it was reported to be in Jordan, where it had been present since 2006 according to the disease report29, and Mozambique30, where it might have arrived 2-3 years earlier31. In 2015, it was reported to be in Lebanon and Pakistan32. There are also reports that it is in Oman33.
TR4 is said to also attack cultivars susceptible to races 1 and 2, and additional cultivars such as Barangan (Lakatan subgroup, AAA genome group)22 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.
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). 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 following digit(s) represents the order in which the VCGs were identified (e.g. 0120, 0121, 0122 etc.). Some 24 VCGs have been characterized worlwide. Tropical race 4 isolates belong to the VCG 01213/16 complex, although other VCGs are also known to cause Fusarium wilt on Cavendish cultivars. For example, the results of a survey published in 2013 documented 11 VCGs in the five banana-producing regions of mainland China34.
Isolates within a VCG can belong to more than one race. For example, in Central America Cavendish cultivars are not affected by the VCG0120 strain to which Gros Michel is susceptible. On the other hand, in South Africa and the Canary Islands, VCG0120, which is usually the only strain present, causes Fusarium wilt in Cavendish plants35. In India, VCG 0124 isolates have also been extracted from Cavendish bananas exhibiting Fusarium wilt symptoms18. In Latin America, VCG 0124 isolates are classified as race 1 because they infect Gros Michel but not Cavendish bananas.