Fusarium oxysporum f.sp. cubense (Panama disease of banana)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Means of Movement and Dispersal
- Plant Trade
- Wood Packaging
- Impact Summary
- Environmental Impact
- Impact: Biodiversity
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Fusarium oxysporum f.sp. cubense (E.F. Sm.) W.C. Snyder & H.N. Hansen
Preferred Common Name
- Panama disease of banana
Other Scientific Names
- Fusarium cubense E.F. Sm.
- Fusarium cubense var. inodoratum E.W. Brandes
- Fusarium var. cubense (E.F. Sm.) Wollenw.
International Common Names
- English: banana wilt; Fusarium wilt of banana; vascular wilt of banana and abaca
- Spanish: mal de Panamá
- French: fusariose du bananier; maladie de Panama
Local Common Names
- Germany: Panama-Krankheit: Banane; Welke: Banane
- Indonesia/Java: Javanese vascular wilt
- FUSACB (Fusarium oxysporum f. sp. cubense)
Summary of InvasivenessTop of page
F. oxysporum f.sp. cubense (Foc) is considered invasive because it can be distributed from location to location and from country to country with traditional planting material. Also, once established it can spread within plantations in runoff water and in soil on the tyres/wheels of farm machinery, feet of farm animals and shoes of farm workers. Once farm soil is contaminated, susceptible cultivars can only be grown with great difficulty and with much crop loss. Tropical race 4 (TR4) isolates of the pathogen threaten the production of Cavendish cultivars, which produce the bulk of export bananas (see Biology and Ecology).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Ascomycota
- Subphylum: Pezizomycotina
- Class: Sordariomycetes
- Subclass: Hypocreomycetidae
- Order: Hypocreales
- Family: Nectriaceae
- Genus: Fusarium
- Species: Fusarium oxysporum f.sp. cubense
Notes on Taxonomy and NomenclatureTop of page
Fusarium oxysporum f.sp. cubense cannot be distinguished reliably in culture from other formae speciales (special forms). The forma specialis designated cubense was applied only on the evidence of pathogenicity tests and its ability to cause wilt symptoms under field conditions appears to be confined to hosts in the Musaceae: species of Musa and of Heliconia.
For further information on F. oxysporum f.sp. cubense tropical race 4 (TR4), see separate datasheet.
DescriptionTop of page
Fusarium wilt of bananas is caused by F. oxysporum f.sp. cubense, a common soil inhabitant. Other formae speciales attack a wide variety of other crops, including cotton, flax, tomatoes, cabbages, peas, sweet potatoes, watermelons and oil palms.
The formae speciales of Fusarium oxysporum each produce three types of asexual spores. The macroconidia (22-36 x 4-5 µm; see Wardlaw, 1961 for measurements) are produced most frequently on branched conidiophores in sporodochia on the surface of infected plant parts or in artificial culture. Macroconidia may also be produced singly in the aerial mycelium, especially in culture. The macroconidia are thin-walled with a definite foot cell and a pointed apical cell. Oval or kidney-shaped microconidia (5-7 x 2.5-3 µm) occur on short microconidiophores in the aerial mycelium and are produced in false heads. Both macroconidia and microconidia may also be formed in the xylem vessel elements of infected host plants, but the microconidia are usually more common. The fungus may be spread by macroconidia, microconidia and mycelium within the plant as well as outside the plant. Illustrations of the conidia have been published (Nelson et al., 1983).
Chlamydospores (9 x 7 µm) are thick-walled asexual spores that are usually produced singly in macroconidia or are intercalary or terminal in the hyphae. The contents are highly refractive. Chlamydospores form in dead host-plant tissue in the final stages of wilt development and also in culture. These spores can survive for an extended time in plant debris in soil.
Mutation in culture is a major problem for those working with vascular wilt isolates of F. oxysporum. The sporodochial type often mutates to a 'mycelial' type or to a 'pionnotal' type. The former has abundant aerial mycelium, but few macroconidia, whereas the latter produces little or no aerial mycelium, but abundant macroconidia. These cultures may lose virulence and the ability to produce toxins. Mutants occur more frequently if the fungus is grown on a medium that is rich in carbohydrates.
DistributionTop of page
F. oxysporum f.sp. cubense is believed to have evolved with wild and cultivated banana in South-East Asia because it is in this region that most genetic diversity of the pathogen occurs (Pegg et al., 1993, Bentley et al., 1995). Of all the locations in South-East Asia, the area encompassing Java, Sumatra, peninsular Malaysia and possibly Borneo would seem the most likely centre of origin and has been indicated as such in the above list. There is also some evidence for an independent origin in Malawi, Africa (see Biology and Ecology), but more research is needed to verify this theory.
F. oxysporum f.sp. cubense is probably present in most areas where bananas are grown in Asia, Africa and the Americas. Exceptions seem to be parts of the South Pacific and Melanesia, some countries bordering the Mediterranean and Somalia. A record for Israel in CABI/EPPO (1999) is based on specimens from 1952 which cannot be verified. In the absence of published reports and with information from the Israeli Plant Protection and Inspection Services, this record is now considered unreliable.
The latest locations to have recorded the pathogen are the islands of New Guinea (Shivas et al., 1996; Shivas and Philemon, 1996; Davis et al., 2000) and Yap in the Federated States of Micronesia (Smith et al., 2002). The progression of the disease across Wallace's line into Melanesia is significant (Ploetz and Pegg, 1997). It is likely that the disease has only very recently been introduced to these areas through the movement of infected planting material from South-East Asia. The replacement of traditional banana cultivars susceptible to black leaf streak by South-East Asian cultivars resistant to the disease has been noted in the Federated States of Micronesia (Watson, 1993). Introduced germplasm could have carried the Fusarium wilt pathogen to Yap. Circumstantial evidence indicates that migrants bringing planting material from Java may have introduced the pathogen to the island of New Guinea (Ploetz and Pegg, 2000).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 25 Feb 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Congo, Democratic Republic of the||Present||Introduced||Invasive|
|Congo, Republic of the||Present||Introduced||Invasive|
|-Gujarat||Present||Original citation: EPPO (2018b)|
|-Madhya Pradesh||Present||Original citation: EPPO (2018b)|
|-Uttar Pradesh||Present||Original citation: EPPO (2018b)|
|Israel||Present, Transient under eradication|
|Laos||Present||TR4 (VCG 01213/16); Original citation: Chittarath et al. (2017)|
|Lebanon||Present, Few occurrences|
|Sri Lanka||Present, Widespread||Introduced||Invasive|
|British Virgin Islands||Present||Introduced||Invasive|
|Saint Vincent and the Grenadines||Present||Introduced||Invasive|
|Trinidad and Tobago||Present||Introduced||Invasive|
|U.S. Virgin Islands||Present||Introduced||Invasive|
|United States||Present, Localized||Introduced|
|-New South Wales||Present, Localized||Introduced||Invasive|
|-Northern Territory||Present, Few occurrences||Introduced||Invasive|
|Federated States of Micronesia||Present|
|Northern Mariana Islands||Present||Introduced||Invasive|
|Papua New Guinea||Present||Introduced||Invasive|
|-Ceara||Present||Original citation: EPPO (2018b)|
|-Goias||Present||Original citation: EPPO (2018b)|
|-Rio Grande do Norte||Present||Original citation: EPPO (2018b)|
|-Rio Grande do Sul||Present||Introduced||Invasive|
History of Introduction and SpreadTop of page
Evidence suggests that F. oxysporum f.sp. cubense co-evolved with banana in South-East Asia (Pegg et al., 1993; Bentley et al., 1995). Therefore, the pathogen could have been carried to new areas in Asia in prehistoric times with the first waves of transported rhizome planting material. Such spread would have been inevitable because symptoms on planting material, even if apparent, may not have been associated by early farmers with the later decline and death of plants (Jones, 2002). It is likely that the disease was afflicting susceptible banana cultivars in many locations around the world by the time it was first described on the highly susceptible cultivar 'Silk' (AAB genome) in Australia in the 19th century (Bancroft, 1876). Therefore, details of the initial spread of the disease, which seems to have occurred before plant pathology became an exact science, are not known.
It was only after the commercial production of the cultivar 'Gros Michel' (AAA genome) started in the Latin American/Caribbean region late in the 19th century that the disease became important. Here it acquired the name Panama disease after the country where it first caused extensive damage. Although the pathogen was almost certainly disseminated with planting material of 'Gros Michel', it is highly likely that it already existed in many locations in small plantings of cultivars such as 'Silk', which were introduced to the Americas in colonial times. During the middle of the 20th century the disease disseminated Gros Michel and had a devastating impact on the banana industry in the region. Fortunately, a commercially acceptable cultivar resistant to populations of F. oxysporum f.sp. cubense present in the Americas was found in the form of 'Valery', a cultivar in the Cavendish subgroup (AAA genome). 'Valery' replaced 'Gros Michel' in the 1960s to be the main cultivar for the trade. Since 'Valery', other Cavendish cultivars, such as 'Robusta', 'Williams' and 'Grand Nain' have also gained prominence (Stover, 1962, 1990; Jones, 2002; Ploetz, 2006).
In the 1980s Fusarium wilt was observed on Cavenish bananas in Taiwan, leading to the designation of F. oxysporum f.sp. cubense race 4, a pathotype also capable of attacking cultivars susceptible to races 1 and 2. Until 1990, race 4 was only found to cause major losses in subtropical areas, namely in Australia, the Canary Islands and Taiwan (Su et al., 1986; Pegg et al., 1996). Given the subsequent emergence of a new pathogen variant (see below), this race is now referred to as ‘subtropical race 4’.
Perhaps the greatest threat to export banana production comes from Cavendish cultivar-attacking populations of the Fusarium wilt pathogen designated F. oxysporum f.sp. cubense 'tropical race 4'. This variant was first reported on Cavendish bananas in the early 1990s in peninsular Malaysia and nearby Sumatra in Indonesia (Ploetz and Pegg, 2000; Ploetz, 2005). It has since caused severe damage to the cultivar in Malaysia, Indonesia, South China, the Philippines and the Northern Territory of Australia (Ploetz, 2006; Molina et al., 2008; Buddenhagen, 2009). To date, populations of this variant have not been reported beyond the South-East Asian/Australasian region. If it were to establish and spread in the Latin American/Caribbean region then Cavendish cultivation could become uneconomical, just as the production of 'Gros Michel' became uneconomical in the 1950s. However, depending on how quickly an outbreak is recognised, a scenario of total destruction of the export crop should be avoidable as an outbreak on a commercial plantation of Cavendish in the Latin American/Caribbean region would almost certainly be quarantined. Furthermore, the industry would by necessity replant exclusively with plants derived from tissue-cultured to prevent onward dissemination of the pathogen with traditional planting material. If practical, the practice of annual cropping - which is gaining popularity in Taiwan and the Philippines - would also be expected to reduce the impact of the disease (Jones, 2002) and perhaps also levels of pathogen inoculum in soils.
Risk of IntroductionTop of page
The pathogen is commonly spread locally, nationally and internationally in infected rhizomes or suckers and attached soil. However, infected plant material may not exhibit symptoms. The fungus can also be spread in soil attached to farm machinery, implements and vehicles.
Although Fusarium wilt is found in most banana-growing regions, it has not been confirmed as present in many South Pacific countries. Banana material should only be introduced to this region as tissue cultures which would be free of the disease.
At least one pathotype of F. oxysporum f.sp. cubense, which is capable of attacking Cavendish cultivars (AAA genome) in the tropics, exists in South-East Asia, but is not found in the Latin American/Caribbean region where most Cavendish bananas for export are produced. Plantains (AAB genome), which are an important food resource in Africa and the Americas, have succumbed to subtropical race 4 in Australia. Care must be taken to ensure that strains that are now of limited distribution, but which have the capability of causing severe damage in other parts of the world, are not inadvertently moved to other countries. Movement of Musa germplasm by tissue culture is seen as essential to prevent dissemination of the more potent pathotypes (Jones and Diekmann, 2000).
Hosts/Species AffectedTop of page
F. oxysporum f.sp. cubense is one of around 100 formae speciales (special forms) of F. oxysporum which cause vascular wilts of flowering plants (Gerlach and Nirenberg, 1982). Hosts of the various formae speciales are usually restricted to a limited and related set of taxa. As currently defined, F. oxysporum f.sp. cubense affects the following species in the order Zingiberales: in the family Musaceae, Musa acuminata, M. balbisiana, M. schizocarpa and M. textilis; and in the family Heliconeaceae, Heliconia caribaea, H. chartacea, H. crassa, H. collinsiana, H. latispatha, H. mariae, H. rostrata and H. vellerigera (Stover, 1962; Waite, 1963). Additional hosts include hybrids between M. acuminata and M. balbisiana, and M. acuminata and M. schizocarpa.
F. oxysporum f.sp. cubense may survive as a parasite of non-host weed species. Three species of grass (Paspalum fasciculatum, Panicum purpurascens [Brachiaria mutica] and Ixophorus unisetus) and Commelina diffusa have been implicated (Waite and Dunlap, 1953).
Host Plants and Other Plants AffectedTop of page
|Chloris barbata (purpletop chloris)||Poaceae||Unknown|
|Cyanthillium cinereum (little ironweed)||Asteraceae||Unknown|
|Euphorbia heterophylla (wild poinsettia)||Euphorbiaceae||Unknown|
|Heliconia caribaea||Heliconiaceae||Wild host|
|Heliconia chartacea||Heliconiaceae||Wild host|
|Heliconia collinsiana||Heliconiaceae||Wild host|
|Heliconia crassa||Heliconiaceae||Wild host|
|Heliconia latispatha||Heliconiaceae||Wild host|
|Heliconia mariae||Heliconiaceae||Wild host|
|Heliconia rostrata||Heliconiaceae||Wild host|
|Heliconia vellerigera||Heliconiaceae||Wild host|
|Musa acuminata (wild banana)||Musaceae||Wild host|
|Musa acuminata var. sumatrana||Unknown|
|Musa balbisiana||Musaceae||Wild host|
|Musa banksii (wild banana)||Musaceae||Unknown|
|Musa schizocarpa||Musaceae||Wild host|
|Musa textilis (manila hemp)||Musaceae||Main|
|Musa x paradisiaca (plantain)||Musaceae||Unknown|
|Tridax procumbens (coat buttons)||Asteraceae||Unknown|
Growth StagesTop of page
SymptomsTop of page
The various symptoms of Fusarium wilt on banana are described and well illustrated by Ploetz and Pegg (1999).
The first external symptoms of Fusarium wilt on bananas is a faint off-green to pale-yellow streak or patch at the base of the petiole of one of the two oldest leaves. The disease can then progress in different ways. The older leaves can yellow, beginning with patches at the leaf margin. Yellowing progresses from the older to the younger leaves until only the recently unfurled or partially unfurled centre leaf remains erect and green. This process may take from 1 to 3 weeks in cultivar 'Gros Michel'. Often the yellow leaves remain erect for 1-2 weeks or some may collapse at the petiole and hang down the pseudostem. In contrast to this 'yellow syndrome', leaves may remain completely green except for a petiole streak or patch but collapse as a result of buckling of the petiole. The leaves fall, the oldest first, until they hang about the plant like a skirt. Eventually, all leaves on infected plants fall down and dry up. The youngest are the last to fall and often stand unusually erect.
Splitting of the base of the pseudostem is another symptom as is necrosis of the emerging heart leaf. Other symptoms include irregular, pale margins on new leaves and the wrinkling and distortion of the lamina. Internodes may also shorten (Stover, 1962, 1972; Jones, 1994; Moore et al., 1995).
The characteristic internal symptom of Fusarium wilt is vascular discoloration. This varies from one or two strands in the oldest and outermost pseudostem leaf sheaths in the early stages of disease to heavy discoloration throughout the pseudostem and fruit stalk in the later disease stages. Discoloration varies from pale yellow in the early stages to dark red or almost black in later stages. The discoloration is most pronounced in the rhizome in the area of dense vascularization where the stele joins the cortex. When symptoms first appear, a small or large portion of the rhizome may be infected. Eventually, almost the entire differentiated vascular system is invaded. The infection may or may not pass into young budding suckers or mature 'daughter' suckers. Where it does, discoloration of vascular strands may be visible in the excised sucker. Usually, suckers less than 1.5 m tall and ca. 4 months old do not show external symptoms. Where wilt is epidemic and spreading rapidly, suckers are usually infected and seldom grow to produce fruit. Above- and below-ground parts of affected plants eventually rot and die.
Fusarium wilt was reported to occur on banana cultivars of the 'Mutika-Lujugira' (AAA genome) subgroup in East Africa above 1400 m. Internal symptoms were much less extensive than those described above and external symptoms more subtle, comprising thin pseudostems and small fingers. Nevertheless, symptomatic plants were recognized by smallholders and were rogued. These mild symptoms were initially believed to be indicative of an attack on a plant whose defences have been weakened as a result of cooler conditions or other predisposing factors at altitude (Ploetz et al., 1994). Given the importance of this banana group, also referred to locally as ‘East African highland bananas’, to local trade and as a staple food, further investigation was merited. This revealed that the disorder also affected non-indigenous banana types, including Cavendish and Bluggoe (which were not affected by Fusarium wilt) and was related to abnormal soil nutrient levels and farm management practice. Discoloration similar to that caused by F. oxysporum f.sp. cubense was observed in vascular tissues of affected plants. Fusarium pallidoroseum (syn. Fusarium semitectum) was consistently isolated from such tissues but found to be non-pathogenic. F. oxysporum was not recovered (Kangire and Rutherford, 2001; Rutherford, 2006).
It is not known whether the East African Highland bananas or plantain bananas cultivated in tropical Africa are susceptible to F. oxysporum f.sp. cubense tropical race 4.
Abacá (Musa textilis)
The external symptoms of Fusarium wilt on abacá are less conspicuous than on bananas. Leaf yellowing is not as pronounced; leaves dry up and are broken by the wind. Leaves bunch and are stunted, but off-colour streaks at the base of petioles, collapse of petioles and longitudinal splitting of the pseudostem are not characteristic symptoms in abaca (Stover, 1972).
List of Symptoms/SignsTop of page
|Fruit / reduced size|
|Growing point / dead heart|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / abnormal leaf fall|
|Leaves / necrotic areas|
|Leaves / wilting|
|Leaves / yellowed or dead|
|Roots / rot of wood|
|Roots / soft rot of cortex|
|Stems / discoloration of bark|
|Stems / distortion|
|Stems / internal discoloration|
|Stems / stunting or rosetting|
Biology and EcologyTop of page
Fusarium wilt is a lethal fungal disease of banana. The causal pathogen attacks the banana's vascular system. As diseased plants die, the fungus grows out of the xylem into surrounding tissues. Many chlamydospores are formed which are returned to the soil as the plant decays. Chlamydospores are stimulated to germinate and infect nearby banana roots. Following germination, mycelium is produced from which conidia form in 6-8 hours and chlamydospores in 2-3 days. Small secondary or tertiary roots are invaded. No banana cultivars are immune and the fungus is able to establish itself in the vascular system of the root. In susceptible plants, the fungus is not blocked by the host defence mechanisms and the infection becomes systemic through the vascular system of the corm, pseudostem and fruit stalk. In resistant cultivars, the fungus becomes blocked by vascular occluding responses of the host and cannot advance into the corm.
F. oxysporum f.sp. cubense can survive for up to 30 years as chlamydospores in infested plant debris or in the roots of alternative hosts (Stover, 1962).
Physiology and phenology
Pathogenic races in F. oxysporum f.sp. cubense are designated based on banana species and clones attacked. Previously, four races were recognized (Waite and Stover, 1960; Stover and Buddenhagen, 1986; Su et al., 1986; Stover and Simmonds, 1987; Stover, 1990; Ploetz and Pegg, 2000).
Race 1 attacks: Musa textilis (abacá), 'Gros Michel' (AAA genome), 'Maqueño' (AAB genome), 'Silk' (AAB genome), 'Pome' (AAB genome), Pisang Awak (ABB genome), 'I.C.2' (AAAA genome- bred hybrid).
Race 2 attacks: 'Bluggoe' (ABB genome), bred AAAA hybrids.
Race 3 attacks: Heliconia spp.
Race 4 attacks: Cultivars in the Cavendish subgroup (AAA genome), such as 'Dwarf Cavendish', 'Grand Nain' and 'Williams'. Plantains and all cultivars that are susceptible to races 1 and 2.
Isolates found to attack cultivars in the Cavendish subgroup (AAA genome) in the subtropics only belong to F. oxysporum f.sp. cubense subtropical race 4. The susceptibility of Cavendish cultivars to subtropical race 4 has been attributed to abiotic stress conditions (cold winter temperatures) which weaken the plant’s resistance (Moore et al., 1993; Ploetz and Pegg, 2000).
Isolates that can attack Cavendish cultivars in tropical conditions belong to tropical race 4. This variant is also capable of attacking Cavendish in subtropical conditions (Buddenhaggen, 2009).
Seedlings of Musa balbisiana (BB genome) and 'Gros Michel' (AAA genome) have been reported to be slightly susceptible to race 3. However, as this race does not cause Fusarium wilt on banana it is no longer considered part of the F. oxysporum f.sp. cubense race structure (Ploetz, 2005; Fourie et al., 2011).
Given that host resistance is potentially the most effective means of Fusarium wilt management (see Prevention and Control), variability within F. oxysporum f.sp. cubense and the response of banana genotypes to pathogen variants must be defined. Field testing of isolates is, however, problematic as it is influenced by environmental factors, method of inoculation and other variables. It is also time consuming, expensive and the required set of differentials may not be available. The 'race' system of distinguishing different pathotypes of F. oxysporum f.sp. cubense has proved limiting as exceptions are known, which indicate that more races may exist. As described below, advances in methodology for assessing diversity have shown that the currently defined race structure does not adequately reflect the extent of genetic and phenotypic variability in F. oxysporum f.sp. cubense and needs to be redefined by testing a range of representative isolates on a variety of diverse banana genotypes (Ploetz and Pegg, 2000; Dita et al., 2010; Fourie et al., 2011).
In recent years, F. oxysporum f.sp. cubense isolates have been characterised on the basis of vegetative compatibility group (VCG), ability to produce volatile aldehydes and genetic variability as revealed by application of various molecular analytical techniques (see Biology and Ecology-Genetics).
As a phenotypic characteristic, vegetative compatibility may be subject to selection pressure and does not provide a measure of genetic relatedness. It does, however, provide a good means for assessing diversity within populations and identifying genetically isolated groups in F. oxysporum f.sp. cubense (Glass and Kuldau, 1992; Leslie, 1993; Visser et al., 2010; Fourie et al., 2011). The distribution and relationship between vegetative compatibility groups has provided important information on the dissemination and evolution of the pathogen. Twenty-four VCG have been recognized in F. oxysporum f.sp. cubense, which is a large number for a forma specialis of F. oxysporum and may be a result of the diverse banana host and the presumed old age of the pathosystem. Isolates in some VCG are cross compatible with those in other VCG, resulting in VCG complexes such as VCG 0120-01215, VCG 0124-0125-0128-01220 and VCG 01213-01216. The worldwide distribution of isolates observed for VCG 0120-01215 and VCG 0124-0125-0128-01220 is probably due to their frequent dispersal in banana rhizomes moved to new production areas. In contrast, VCG 0122, 01211, 01212, 01214, 01217 have only been found in Philippines, Australia, Tanzania, Malawi and Malaysia respectively. F. oxysporum f.sp. cubense subtropical race 4 isolates belong to VCG 0120, 0121, 0122, 0129 and 01211 and F. oxysporum f.sp. cubense tropical race 4 isolates to VCG 01213-01216. The majority of VCG are present in Asia, indicating that this is the main centre of origin (Correll et al., 1987; Ploetz and Corrrell, 1988; Moore et al., 1993; Bentley et al., 1995; Ploetz and Pegg, 1997; Ploetz and Pegg, 2000; Buddenhagen, 2009; Fourie et al., 2009; Visser et al., 2010; Fourie et al., 2011).
The use of VCG as a means of determining pathotypes in F. oxysporum f.sp. cubense is limited, as isolates of differing race may occur in one VCG and each race can comprise isolates of more than one VCG. The occurrence of race 1 and race 2 isolates in VCG 0124, for example, prevents the use of VCG to assign pathotypes in Australia (Gerlach et al., 2000).
Molecular approaches have been widely used in recent years to analyse genetic variability within and between populations in F. oxysporum f.sp. cubense. They include analysis of microsatellites, simple sequence repeats (SSR), restriction fragment length polymorphisms (RFLP), amplified fragment length polymorphisms (AFLP), random amplified polymorphic DNA (RAPD) and DNA sequencing. These have helped to overcome the limitations of other, non-molecular methods and provided clarification as to the genetic structure and diversity of F. oxysporum f.sp. cubense and how this relates to phenotypic characteristics, including pathogenic races and VCG. Multi-gene phylogenetic analyses have provided a better understanding of the evolution of the fungus, while DNA sequencing has facilitated the development of population specific diagnostic tools (see Diagnosis) (Boehm et al., 1994; Bentley et al., 1995, 1998; Pegg et al., 1995; Koenig et al., 1997; O’Donnell et al., 1998; Ploetz and Pegg, 2000; Groenewald et al., 2006; Lin et al., 2009; Fourie et al., 2009, 2011; Dita et al., 2010).
Multi-gene phylogenetic studies have shown that at least eight distinct phylogenetic lineages exist in F. oxysporum f.sp. cubense, with most lineages consisting of isolates in closely related VCG, even where these are distributed across a broad geographic area. These relationships were supported by RAPD, RFLP and AFLP analyses and suggest a clonal reproductive strategy for the pathogen. As such, diversity in F. oxysporum f.sp. cubense may arise through mutation and/or parasexual recombination. However, analysis of RFLP haplotypes (Koenig et al., 1997) suggests that recombination may have occurred between two lineages (Taylor et al., 1999), while the recently reported occurrence of both mating type (MAT) idiomorph alleles (i.e. MAT-1 isolates and MAT-2 isolates) in some lineages suggests that these may have a sexual origin (Fourie et al. 2009, 2011). Some subtropical race 4 isolates were more closely related to isolates in other formae speciales of F. oxysporum than to those in F. oxysporum f.sp. cubense.
One lineage, comprising isolates from Malawi in VCG 0124, was distinct genetically from other F. oxysporum f.sp. cubense lineages. This may have arisen independently outside the main centre of origin of the pathogen and on a host other than banana (Koenig et al., 1997; Ploetz and Pegg, 2000; Fourie et al., 2011).
The research to date suggests that the ability of F. oxysporum f.sp. cubense to cause Fusarium wilt disease on some or all of the race differential cultivars has evolved convergently, as members of some races occur in different lineages. Various factors – including co-evolution with the host plant and horizontal gene transfer – may have shaped the pathogen’s evolution (Fourie et al., 2011).
Although attempts have been made to correlate genetic diversity in F. oxysporum f.sp. cubense with pathogenicity and the pathogenic races highlighted above, a relationship has not been established.
Soils that suppress the disease have been found in several locations (Stover, 1962; Alvarez et al., 1981; Chuang, 1988). In general, these disease-suppressive soils are recognized by the length of time high levels of production can be sustained in the presence of the pathogen. This may be associated with chemical and physical factors, such as a clay fraction of the montmorillanoid type (Ploetz and Pegg, 2000).
Plants grown from tissue-culture have been shown to be more susceptible to Fusarium wilt than conventional planting material (Smith et al., 1998).
The pathogen is able to colonise and persist in the roots of alternative hosts, including close relatives of banana, and three non-host species of grasses and a non-host weed (Commelinia diffusa), even though these plants remain symptomless under field conditions (Waite and Dunlop, 1953; Ploetz and Pegg, 2000).
Experiments have shown that there is a synergistic interaction between the nematode Meloidogyne incognita and F. oxysporum f.sp. cubense (Jonathan and Rajendran, 1998).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
Means of Movement and DispersalTop of page
Spores can be carried in surface run-off water, spreading the disease rapidly and decimating a plantation within months if conditions are favourable.
F. oxysporum f.sp. cubense is commonly spread locally, nationally and internationally in infected rhizomes or suckers and attached soil. As infected plant material may not exhibit symptoms, a visual examination of suckers or rhizome pieces may not be an effective method of determining its presence. The fungus can also be spread in soil adhering to farm machinery, implements and vehicles. Spores can contaminate irrigation reservoirs and be rapidly spread around plantations in irrigation water.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bulbs/Tubers/Corms/Rhizomes||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Roots||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
Wood PackagingTop of page
|Wood Packaging not known to carry the pest in trade/transport|
|Loose wood packing material|
|Processed or treated wood|
|Solid wood packing material with bark|
|Solid wood packing material without bark|
Impact SummaryTop of page
|Fisheries / aquaculture||None|
ImpactTop of page
Fusarium wilt was responsible for the decimation of the export trades in Central and South America and the Caribbean that were based on the cultivar 'Gros Michel' (AAA genome) which is susceptible to race 1 of the fungus. It has been estimated that about 40,000 ha became unproductive over a period of 50 years (Stover, 1972). The industry was saved by changing to cultivars in the Cavendish subgroup (AAA genome), which were resistant to race 1. However, Cavendish cultivars in plantations in subtropical Australia, the Canary Islands, South Africa and Taiwan were subsequently affected by F. oxysporum f.sp. cubense subtropical race 4. More recently, Cavendish cultivars planted on a large scale in South-East Asia are succumbing to F. oxysporum f.sp. cubense 'tropical race 4' (Ploetz and Pegg, 2000). Since its appearance, tropical race 4 has caused severe damage to Cavendish cultivars in Malaysia, Indonesia, South China, the Philippines and the Northern Territory of Australia (Ploetz, 2006; Molina et al., 2008; Buddenhagen, 2009). Garcia-Bastidas et al. (2014) have recently reported tropical race 4 in Cavendish bananas in Jordan, with 80% of the Jordan Valley production area affected by Fusarium wilt, and 20-80% of the plants affected in different farms.
Cultivars that are favoured by smallholders are also affected by Fusarium wilt. 'Silk' (AAB genome) is a very popular dessert banana in Brazil, India, Indonesia, Malaysia, the Philippines and elsewhere, but it is extremely susceptible to the disease and is almost impossible to grow in some areas. Cultivars in the Pome (AAB genome) and Bluggoe (ABB genome) subgroups, and 'Pisang Awak' (ABB genome) are also attacked and losses are significant. Fusarium wilt is a major factor limiting the production of many cultivars.
Because conventional banana planting material can carry F. oxysporum f.sp. cubense and other pathogens, the local and international movement of banana suckers and corm pieces is viewed as undesirable. This has led to the development of alternative strategies, such as micropropagation techniques for producing clean planting material.
Environmental ImpactTop of page
The seriousness of Fusarium wilt in commercial plantations of 'Gros Michel' (AAA genome) in the Latin American/Caribbean region led to the abandonment of cultivation on vast tracts of land. To compensate, new land in the coastal tropics had to be cleared for cultivation. This cycle continued as the disease gradually spread throughout new plantings. Large areas of natural vegetation were eventually destroyed so that production could be maintained. However, the introduction of Cavendish cultivars, which are resistant to races of the pathogen present in the Latin America/Caribbean region, into commercial production in the 1960s meant that cultivation could be maintained almost indefinitely on the same land.
Impact: BiodiversityTop of page
The presence of Fusarium wilt in cultivated land has led to some small growers abandoning the cultivation of some susceptible cultivars. 'Silk' (AAB genome), which is a popular cultivar in many countries, is extremely susceptible to the disease. Because of high losses of plants, cultivation of 'Silk' has been reduced. It is possible that some plants that are difficult to grow because of Fusarium wilt may disappear from cultivation. However, a scarcity of supply can lead to higher prices for favoured fruit, which may compensate growers for losses due to disease and allow some vulnerable cultivars to survive in cultivation.
DiagnosisTop of page
Diagnostic methods to identify F. oxysporum f.sp. cubense have been discussed elsewhere (see Symptoms, Similarities to Other Species/Conditions and Detection and Inspection). However, different races (pathotypes) of the fungus have been recognized (see Biology and Ecology-Physiology and phenology) and, more recently, emphasis has been placed on the identification of vegetative compatibility groups of the pathogen.
Races of F. oxysporum f.sp. cubense have been identified on the basis of host range. As a general rule, race 1 attacks cultivars in the 'Gros Michel' (AAA genome) and 'Pome' (AAB genome) subgroups and the 'Silk' (AAB genome) and 'Pisang Awak' (ABB genome) clones of banana; race 2 attacks 'Bluggoe' (ABB genome) and close relatives; race 3 attacks Heliconia spp. but not banana; race 4 attacks cultivars in the Cavendish subgroup (AAA genome) and hosts of races 1 and 2. The three races attacking bananas can be distinguished by pathogenicity tests using the cultivars 'Gros Michel', 'Bluggoe' and 'Dwarf Cavendish'. 'Gros Michel' is susceptible to races 1 and 4, 'Bluggoe' is susceptible to races 2 and 4 and 'Dwarf Cavendish' is only susceptible to race 4. However, it is not always possible to characterize populations of the fungus using pathogenicity tests because of interactions between plant and environment and because the current set of host differentials may not adequately assess the virulence, which exists among populations in the designated races.
A more thorough and reliable diagnosis can be made by vegetative compatibility group (VCG) analysis, which groups genetically identical or very similar isolates. It can also be used to assess the diversity of strains of F. oxysporum f.sp. cubense in a given region. Although strong correlation between VCG and pathogenicity has been observed in some regions, the occurrence of several races of the fungus within one VCG and more than one VCG in a particular race limits the potential for using VCG for pathotype determination. Currently, 24 VCGs have been described, and a pattern of distribution throughout the world is emerging (Pegg et al., 1994; Ploetz and Pegg, 2000; Fourie et al., 2011).
F. oxysporum f.sp. cubense can also be characterized by production of volatile odours produced when the fungus grows on rice cultures. In Australia, all race 4 isolates produced distinctive volatile aldehydes whereas race 1, race 2 and non-pathogenic isolates of F. oxysporum did not (Moore et al., 1991).
A variety of genetic markers have been used to assess diversity in F. oxysporum f.sp. cubense, such as arbitrarily primed PCR (e.g. RAPD type techniques) to generate DNA fingerprints (see Biology and Ecology-Genetics). Using DNA fingerprints, it is possible to determine the genetic relationships between different VCGs as well as isolates within each VCG (Bentley et al., 1995). Other molecular techniques have also been used (Boehm et al., 1994; Koenig et al., 1997). Information derived through application of such methods has also enabled the development of molecular markers to detect pathogen variants. Recently, Lin et al. (2009) used RAPD-PCR to develop a diagnostic for detection of race 4 isolates in Taiwan. Of significance, use of this technique indicated the presence of subtropical race 4 in Brazil, Costa Rica, Honduras and the USA, where it has not been officially reported. Dita et al. (2010) used polymorphisms observed in the intergenic spacer region (IGS) to develop a rapid and reliable PCR-based diagnostic tool to detect isolates of F. oxysporum f.sp. cubense, tropical race 4 (VCG 01213). Li et al. (2011) diagnosed isolates of race 4 using a PCR diagnosis specific to that race. Isolates were also subjected to amplified fragment length polymorphism (AFLP) analysis. Diagnostic tools such as these may be of major benefit for early detection and monitoring spread of the pathogen.
Detection and InspectionTop of page
Pronounced yellowing symptoms of Fusarium wilt are easy to observe in the field. However,very early symptoms are more difficult for the untrained eye to detect. Proof of Fusarium wilt is vascular discoloration in the lower pseudostem or in the rhizome. In countries with Moko disease (Ralstonia solanacearum race 2), which also causes vascular discoloration, it is possible to confuse the two diseases. However, Fusarium wilt does not cause wilting and blackening of young suckers nor a dry rot in fruit as does Moko. In addition, the first symptoms of Moko on rapidly growing plants are the chlorosis, yellowing and collapse of the three youngest leaves, not the older leaves as with Fusarium wilt. Also, the vascular discoloration is concentrated near the centre of the pseudostem with Moko and is not found peripherally, which is common with Fusarium wilt.
Similarities to Other Species/ConditionsTop of page
Symptoms of Fusarium wilt of bananas can be mistaken for Moko disease caused by Ralstonia solanacearum race 2 and vice versa. The two can be distinguished if the plant has fruit. Fusarium wilt does not affect fruit, but Moko causes an internal dry rot symptom clearly visible if the fruit is cut (see also Detection and Inspection).
Symptoms similar to those caused by Fusarium wilt - such as leaf yellowing - may be caused by other biotic and abiotic factors, including water stress. Care should be taken to avoid attributing such yellowing to Fusarium wilt, by examining the plant for other external and internal symptoms, such as vascular dicolouration. Where possible, the presence of Fusarium oxysporum should be confirmed by isolation from plant tissues onto a suitable growth medium.
Many species of Fusarium look similar in culture to the untrained eye. However, F. oxysporum is readily identified and distinguished from other common species of Fusarium in banana tissue, such as F. pallidoroseum, F. moniliforme [Gibberella fujikuroi] and F. solani. Chlamydospores are lacking in F. moniliforme but present in F. oxysporum after 7-10 days in culture. Microconidia are usually absent in F. pallidoroseum, but present in F. oxysporum. The shape of the macroconidia of F. oxysporum is distinct from that of F. solani. By following well-illustrated keys such as those given by Nelson et al. (1983), F. oxysporum is readily identified (Stover, 1972). However, to determine whether the isolate is the pathogenic F. oxysporum f.sp. cubense and not a soil saprophyte or root inhabitant, it is necessary to carry out a pathogenicity test or use a molecular approach such as DNA analysis. Strains of F. oxysporum can also be classified on the basis of vegetative compatibility, genetic markers and other methods as described elsewhere in this datasheet.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
There is no satisfactory method to control Fusarium wilt. Chemical control, flood fallowing, crop rotation and the use of organic amendments have not been effective in managing the disease (Ploetz and Pegg, 1999). As a soilborne pathogen producing chlamydospores, the fungus may persist in soil in the absence of the host for many years (Stover, 1962, 1990). Replacement of affected plants with susceptible varieties in infested soil, while it may provide temporary respite and yield benefit, would not be effective in controlling the disease.
Several factors influence the development of Fusarium wilt. The banana cultivar is of primary importance; drainage, environmental conditions and soil type also influence host-pathogen interactions. Suppressive soils, in which microbial populations suppress the pathogen population, were first described in the 1930s in Central America. Such soils have also been recorded in the Canary Islands, Australia and South Africa.
The only effective means of control is by host resistance. Natural sources of resistance exist in wild species and cultivars and in synthetic diploids developed by breeding programmes. Major, conventional breeding programmes are located in Honduras - Fundación Hondureño de Investigación Agricola (FHIA), Brazil - Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), Nigeria - International Institute of Tropical Agriculture (IITA), Guadeloupe - Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD) and Cameroon - Centre Régional Bananiers et Plantains (CRBP). These programmes have concentrated on using resistance in 'Pisang Jari Buaya' (AA genome), 'Pisang Lilin' (AA genome) and Musa acuminata subsp. burmannicoides (accession Calcutta 4). Although it has not been possible to breed a 'Cavendish' replacement for Cavendish cultivars by conventional techniques because of fertility constraints, useful hybrids can be bred to replace AAB dessert and ABB cooking banana types. Biotechnology, mutation breeding and somaclonal variation techniques are also being used to produce resistant genotypes. The Taiwan Banana Research Institute (TBRI) have developed clones of Pei-Chiao (AAA, Cavendish subgroup) by somaclonal variation which are much more resistant to Fusarium wilt than the parent plants. These are now being adopted by the local banana industry (Jones, 2000). Efforts are also continuing to develop and evaluate genetically modified bananas with resistance to Fusarium wilt, including Cavendish cultivars resistant to F. oxysporum f.sp. cubense tropical race 4.
Quarantine and exclusion procedures are effective in controlling the disease by restricting the movement of corms, suckers and soil that could be carrying F. oxysporum f.sp. cubense from infested to clean areas.
The use of micropropagated planting material should be encouraged (Jones and Diekmann, 2000), as this, if managed correctly, should be free from contamination by the pathogen. Plants derived from tissue culture and planted in soil where bananas have not been previously grown should remain free of Fusarium wilt for a considerable period.
F. oxysporum f.sp. cubense tropical race 4 is the newest major threat to banana production and trade. Should the pathogen emerge or spread to the major banana producing areas of Latin America, the Caribbean or West Africa, extensive damage and yield loss is possible. Indeed, given the susceptibility of Cavendish cultivars, plantain cultivars and many other cooking and dessert bananas, it has been estimated that 80% of global production is under threat from tropical race 4 (Ploetz, 2005). If not contained, it has the potential to have a devastating impact not only on the export industry but also on the livelihood and food security of millions of people throughout the world. In the absence of resistant cultivars disease monitoring, and the identification and monitoring of the pathogen is critical.
ReferencesTop of page
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