Banana bunchy top virus (bunchy top of banana)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Wood Packaging
- Vectors and Intermediate Hosts
- Impact Summary
- Economic Impact
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Banana bunchy top virus
Preferred Common Name
- bunchy top of banana
Other Scientific Names
- banana bunchy top nanovirus
International Common Names
- English: cabbage top of banana; curly top of banana
- Spanish: cogollo racimoso del banano
- French: maladie du bunchy top du bananier; sommet touffu du bananier
- BBTV00 (Banana bunchy top virus)
Taxonomic TreeTop of page
- Domain: Virus
- Unknown: "ssDNA viruses"
- Unknown: "DNA viruses"
- Family: Nanoviridae
- Genus: Babuvirus
- Species: Banana bunchy top virus
Notes on Taxonomy and NomenclatureTop of page
Banana bunchy top virus (BBTV) was originally included in the luteovirus group, but is now recognised as a species of the Babuvirus genus, one of two genera included in the Nanoviridae family (King et al., 2011).
DescriptionTop of page
Evidence for a Viral Agent
A virus, BBTV, is the causal agent of bunchy top disease of banana. Although unequivocal evidence by reproduction of the disease through inoculation of purified virions or cloned genomic components is lacking, definitive association of BBTV with bunchy top disease was demonstrated by insect vector-mediated transmission of BBTV from an infected banana to a healthy banana plant. The virions are intimately associated with the disease (Harding et al., 1991; Thomas and Dietzgen, 1991) and have been detected in all symptomatic plants tested (Dietzgen and Thomas, 1991; Thomas, 1991; Thomas and Dietzgen, 1991; Karan et al., 1994; Kumar et al., 2011). Dale et al. (1986) and an published study (ML Iskra-Caruana, Montpellier, France) isolated dsRNA, suggestive of luteovirus infection, from Cavendish cultivars and from bunchy top affected plant samples. However, neither these, nor any subsequent studies, have identified or established a role for any virus other than BBTV in banana bunchy top disease aetiology.
Particle and Genome Properties
The virions of BBTV are icosahedra, ca 18-20 nm in diameter, have a coat protein of ca 20,000 Mr, a sedimentation coefficient of ca 46S and a buoyant density of 1.29-1.30 g/cm³ in caesium sulphate (Wu and Su, 1990c; Dietzgen and Thomas, 1991; Harding et al., 1991; Thomas and Dietzgen, 1991). Purified preparations have an A260/280 of 1.33 (Thomas and Dietzgen, 1991). The virus possesses a multi-component genome, consisting of at least six circular, single-stranded DNA (ssDNA) components each ca. 1000-1100 nucleotides long, previously referred to as DNA-1 to -6 (Wu et al., 1994; Yeh et al., 1994; Burns et al., 1995; Xie and Hu, 1995). However, they were renamed as DNA-R, -U3, -S, -M, -C and -N. The DNA-R component encodes two open reading frames and other components each encode one protein (Burns et al., 1995; Dale et al., 1986; Beetham et al., 1997). Two areas of the non-coding regions are highly conserved between the six components (Burns et al., 1995). The first is a stem-loop common region of up to 69 nucleotides. It contains a nonanucleotide loop sequence conserved amongst ssDNA plant viruses and which may be involved in rolling circle replication and initiation of viral strand DNA synthesis. The second, 5' to the stem-loop common region, is a major common region varying in size between components from 65 to 92 nucleotides and which may have a promoter function. The initiation factor for endogenous DNA primers is also located within the major common region (Hafner et al., 1997a). DNA-R (component 1) encodes a putative replication initiation protein and contains a second functional open reading frame internal to this, referred as U5, the function of which is unknown; whilst DNA-S (component 3) codes for the coat protein (Harding et al., 1993; Dale et al., 1986; Hafner et al., 1997b, Wanitchakorn et al., 1997). DNA-U3 (component 2) codes a protein of unknown function, DNA-M (component 4) codes for movement protein, DNA-C (component 5) has been shown to produce a gene product containing an LXCXE motif and to have retinoblastoma protein (Rb)-binding activity, known to perform cell-cycle-link protein, and DNA-N (component 6) codes for a nuclear shuttle protein. The gene product may be produced very early in the infection cycle and be responsible for switching the first infected cells to S-phase in preparation for virus replication. Recent research indicates that component 1 is the minimal replicative unit of BBTV and encodes the 'master' viral Rep (Horser et al., 2001a). Additional Rep encoding circular ssDNA components were reported in a few BBTV isolates from East Asia and the South Pacific region (Horser et al., 2001b). They were named BBTV-S1 and BBTV-S2, of 1109 and 1095 nts, and encoded a protein similar to the DNA-R segment but the genomic organization differed from that of DNA-R. The –S1 and –S2 components lack internal ORF U5, and the stem loop sequence was not similar to the six genomic components. These sequences were not considered as an integral part of the BBTV genome but the precise function of these additional DNAs was not known.
Strains of BBTV
Most isolates of BBTV are associated with typical severe disease symptoms. However, mild and symptomless isolates have been reported from Taiwan (Su et al., 1993; Djailo et al., 2016). BBTV has been confirmed in specimens of mild and symptomless infections from Taiwan by both ELISA and PCR (HJ Su, JL Dale and JE Thomas, Brisbane, personal communication, 1996) and the isolates can be transmitted by Pentalonia nigronervosa (HJ Su, Taipei, personal communication, 1996). Genomic differences, which correlate with these biological variants, have not yet been determined.
Two broad groups of isolates have been identified on the basis of nucleotide sequence differences between some, possibly all, of the six recognized genome components (Karan et al., 1994; Hu et al., 2007; Kumar et al., 2015; Qazi, 2016). The 'South Pacific' group (also referred as Pacific Indian Ocean (PIO) group) comprises isolates from Australia, Bangladesh, India, Myanmar, Pakistan, Sri Lanka, Fiji, Western Samoa, Tonga, Hawaii (USA) and all the isolates identified, as of 2017, in Africa (Angola, Benin, Burundi, Cameroon, CAR, Congo, DRC, Egypt, Equatorial Guinea, Gabon, Malawi, Nigeria, Rwanda, South Africa and Zambia), whilst the 'Asian' group (also referred as Southeast Asian (SEA) group) comprises isolates from China, Indonesia, Japan, the Philippines, Taiwan, Thailand and Vietnam. These differences are present throughout the genomes of components 1 and 6, but are most striking in the untranslated major common region. No biological differences have been associated with these sequence differences.
Magee (1948) noted that certain plants of 'Veimama', a cultivar originally from Fiji and growing then in New South Wales, showed a 'partial recovery' from bunchy top symptoms and produced bunches. After an initial flush of typical severe symptoms in three or four leaves, subsequent leaves showed few, if any, dark-green flecks. Suckers derived from these partially recovered plants also displayed a flush of typical symptoms followed by partial recovery. The origin of the infection, whether from Australia or Fiji, was uncertain. This partial recovery was noted for some infected plants of 'Veimama' only, and in Fiji was noted for one sucker only on a single infected stool from among hundreds of infected stools of 'Veimama' observed. Magee was not able to transmit the virus from partially recovered plants and was only able to super-infect them, with difficulty, with high inoculum pressure. This may be an example of a mild strain of BBTV, possibly a non-aphid transmitted one, propagated vegetatively, reaching only a low titre and conferring a degree of cross-protection. Alternatively, 'Veimama' may not be uniform and individual plants with a degree of resistance may exist. The complete explanation for this phenomenon is unclear. Evidence from recent studies suggests the occurrence of Musa cultivars with variable response to BBTV infection, ranging from extreme to moderate susceptibility and recovery associated with reduced virus titre (Ngatat et al., 2017; PL Kumar, IITA, Nigeria, personal communication, 2017). It is likely that previous observations of mild symptoms and lack of aphid-transmission may be related to virus-host interaction rather than to mild strains.
The inability to transmit bunchy top from abacá to banana (Ocfemia and Buhay, 1934) was originally considered evidence that two distinct strains of the virus existed. However, recent studies have identified a new virus, Abaca bunchy top virus (ABTV) which also belongs to the genus Babuvirus, as the cause of bunchy top-like symptoms in abacá (Sharman et al., 2008). The possibility of co-infection or single infection of BBTV and ABTV in abacá cannot be ruled out in endemic regions.
DistributionTop of page
BBTV has been confirmed in Africa, Asia, Australia and South Pacific islands. Confirmed findings of BBTV symptomatic plants and/or BBTV have been reported from the following countries.
Asia: Bangladesh, China, India, Iran, Japan, Indonesia, Myanmar, Pakistan, the Philippines, Taiwan, Thailand, Vietnam
Australia and South Pacific: Australia, Fiji, Western Samoa, Tuvalu, Tonga, and Wallis and Futuna; Hawaii (USA)
Africa: Angola, Benin, Burundi, Cameroon, CAR, Congo, DRC, Egypt, Equatorial Guinea, Gabon, Malawi, Nigeria, Rwanda, South Africa and Zambia.
Reports of BBTV in Cambodia (Stover, 1972), French Polynesia (CMI, 1977), Laos (Stover, 1972), Hong Kong (Buddenhagen, 1968; CMI, 1977), Papua New Guinea (Magee, 1954; CMI, 1977), Sabah (Magee, 1927; CMI, 1977) and the United Arab Republic (Buddenhagen, 1968) remain unconfirmed (Dale, 1987; Thomas and Iskra-Caruana, 1999). Sulyo and Muharam (1985) reported BBTV to be present in Irian Jaya, Indonesia, but symptoms have not been seen in recent surveys (Shivas et al. ,1996; R Davis, Mareeba, personal communication, 2000). Although there have been reports of bunchy top disease in Peninsular Malaysia (CMI, 1977), a survey conducted by MARDI and INIBAP in 1993 failed to locate any plants with typical or atypical symptoms (DR Jones, Montpellier, personal communication, 1993). A report of bunchy top in South Africa in the early 1990s (Su et al., 1993) was found to be erroneous (Pietersen et al., 1996), but there us now a confirmed report of BBTV in South Africa (Jooste et al., 2016). BBTV symptomatic plants were also recorded in Eritrea (Saverio 1964) but the presence of the virus was not confirmed and the current status is unknown. A report of BBTV in northern Mozambique in 2007 (Gondwe et al., 2007) is unconfirmed; however, the presence of the virus was confirmed in southern Mozambique in 2016 in surveys conducted by the Direccao Nacional De Agriculture E Silvicultura Departamento De Sanidade Vegetal of Mozambique. In Australia, BBTV is restricted to northern New South Wales and southern Queensland. Quarantine measures are in force to prevent its introduction to northern Queensland and other states (Thomas and Iskra-Caruana, 1999). Similar to the situation in Australia, the presence of BBTV is restricted to certain regions of Nigeria, Benin, Cameroon, India, and a number of other countries where the virus has been reported (Kumar et al., 2015).
It is virtually impossible to state for many countries whether the virus is native or exotic. There is little doubt that BBTV is now native in many countries, but there is also some evidence that it was inadvertently disseminated to many of them in infected vegetative propagules with further spread within and between regions assisted by aphid vector and the movement of vegetative propagules by humans (Almeida et al., 2009; Kumar et al., 2011, 2015; Stainton et al., 2015).
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Bangladesh||Present||CABI/EPPO, 2013; EPPO, 2014|
|Cambodia||Absent, unreliable record||EPPO, 2014|
|China||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Fujian||Present||Invasive||Zhou and Xie, 1992; Zhou and Zheng, 2001; CABI/EPPO, 2013; EPPO, 2014|
|-Guangdong||Present||Invasive||Zhou and Xie, 1992; He et al., 2001; CABI/EPPO, 2013; EPPO, 2014|
|-Guangxi||Present||Invasive||Zhou and Xie, 1992; CABI/EPPO, 2013; EPPO, 2014|
|-Hainan||Present||Feng et al., 2010; CABI/EPPO, 2013|
|-Hong Kong||Absent, unreliable record||EPPO, 2014|
|-Yunnan||Present||Invasive||Zhou and Xie, 1992; CABI/EPPO, 2013; EPPO, 2014|
|India||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Andhra Pradesh||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Assam||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Karnataka||Present||Invasive||Sharma, 1988; CABI/EPPO, 2013; EPPO, 2014|
|-Kerala||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Maharashtra||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Odisha||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Tamil Nadu||Present||Invasive||Govindaswamy et al., 1977; Thiribhuvanamala and Doraiswamy, 2001; CABI/EPPO, 2013; EPPO, 2014|
|-Uttar Pradesh||Present||Invasive||Khurana, 1971; CABI/EPPO, 2013; EPPO, 2014|
|-West Bengal||Present||CABI/EPPO, 2013|
|Indonesia||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Irian Jaya||Absent, formerly present||EPPO, 2014|
|-Java||Present||Invasive||Sulyo and Muharam, 1985; CABI/EPPO, 2013; EPPO, 2014|
|-Kalimantan||Present||Invasive||Sulyo and Muharam, 1985; CABI/EPPO, 2013; EPPO, 2014|
|-Nusa Tenggara||Present||CABI/EPPO, 2013; EPPO, 2014|
|Iran||Restricted distribution||Bananej et al., 2007; CABI/EPPO, 2013|
|Japan||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Bonin Island||Present||Invasive||Gadd, 1926|
|-Ryukyu Archipelago||Restricted distribution||Invasive||Kawano and Su, 1993; CABI/EPPO, 2013; EPPO, 2014|
|Korea, Republic of||Absent, reported but not confirmed||CABI/EPPO, 2013; EPPO, 2014|
|Laos||Absent, unreliable record||EPPO, 2014|
|Malaysia||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Peninsular Malaysia||Absent, formerly present||CABI/EPPO, 2013; EPPO, 2014|
|-Sabah||Absent, unreliable record||EPPO, 2014|
|-Sarawak||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|Myanmar||Present||CABI/EPPO, 2013; EPPO, 2014|
|Nepal||Absent, invalid record||IPPC, 2005; CABI/EPPO, 2013|
|Pakistan||Restricted distribution||Introduced||Invasive||Khalid et al., 1993; CABI/EPPO, 2013; EPPO, 2014|
|Philippines||Restricted distribution||Invasive||Castillo and Martinez, 1961; CABI/EPPO, 2013; EPPO, 2014|
|Sri Lanka||Present||Invasive||Bryce, 1921; CABI/EPPO, 2013; EPPO, 2014|
|Taiwan||Present||Invasive||Sun, 1961; CABI/EPPO, 2013; EPPO, 2014|
|Thailand||Present||CABI/EPPO, 2013; EPPO, 2014|
|Vietnam||Present||Invasive||Vakili, 1969; CABI/EPPO, 2013; EPPO, 2014|
|Angola||Restricted distribution||Kumar et al., 2009; CABI/EPPO, 2013; EPPO, 2014|
|Benin||Restricted distribution||Lokossou et al., 2012; CABI/EPPO, 2013; EPPO, 2014|
|Burundi||Present||Invasive||Thomas et al., 1994; CABI/EPPO, 2013; EPPO, 2014|
|Cameroon||Restricted distribution||Oben et al., 2009; IPPC, 2010; CABI/EPPO, 2013; EPPO, 2014|
|Central African Republic||Present||Invasive||Thomas et al., 1994; Diekmann and Putter, 1996; CABI/EPPO, 2013; EPPO, 2014|
|Congo||Present||Invasive||Thomas et al., 1994; CABI/EPPO, 2013; EPPO, 2014|
|Congo Democratic Republic||Widespread||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|Egypt||Restricted distribution||Invasive||Magee, 1927; CABI/EPPO, 2013; EPPO, 2014|
|Equatorial Guinea||Present||CABI/EPPO, 2013; EPPO, 2014|
|Eritrea||Present||CABI/EPPO, 2013; EPPO, 2014|
|Gabon||Restricted distribution||Invasive||Fouré and Manser, 1982; CABI/EPPO, 2013; EPPO, 2014|
|Malawi||Widespread||Invasive||Kenyon et al., 1997; CABI/EPPO, 2013; EPPO, 2014|
|Mozambique||Restricted distribution||Gondwe et al., 2007; CABI/EPPO, 2013; EPPO, 2014; IPPC, 2017|
|Nigeria||Restricted distribution||Adegbola et al., 2013; CABI/EPPO, 2013; EPPO, 2014|
|Rwanda||Present||Invasive||Thomas et al., 1994; CABI/EPPO, 2013; EPPO, 2014|
|South Africa||Restricted distribution||2015||CABI/EPPO, 2013; EPPO, 2014; Jooste et al., 2016|
|Zambia||Restricted distribution||Gondwe et al., 2007; CABI/EPPO, 2013; EPPO, 2014|
|USA||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-Hawaii||Present||Invasive||Dietzgen and Thomas, 1991; Hu et al., 1993; CABI/EPPO, 2013; EPPO, 2014|
|Brazil||Absent, intercepted only||Introduced||Not invasive||Oliveira et al., 2002|
|American Samoa||Present||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|Australia||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|-New South Wales||Restricted distribution||Invasive||Magee, 1927; CABI/EPPO, 2013; EPPO, 2014|
|-Queensland||Restricted distribution||Invasive||CABI/EPPO, 2013; EPPO, 2014|
|Fiji||Present||Invasive||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|French Polynesia||Absent, invalid record||EPPO, 2014|
|Guam||Present||Invasive||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Kiribati||Absent, invalid record||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Micronesia, Federated states of||Absent, unreliable record||EPPO, 2014|
|New Caledonia||Restricted distribution||Introduced||Invasive||Kagy et al., 2001; Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Northern Mariana Islands||Absent, unreliable record||CABI/EPPO, 2013; EPPO, 2014|
|Palau||Absent, invalid record||CABI/EPPO, 2013; EPPO, 2014|
|Papua New Guinea||Absent, unreliable record||EPPO, 2014|
|Samoa||Present||Invasive||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Tonga||Present||Invasive||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Tuvalu||Present||Invasive||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Wallis and Futuna Islands||Present||Invasive||Pearson and Grisoni, 2002; CABI/EPPO, 2013; EPPO, 2014|
Risk of IntroductionTop of page
Great care should be taken to prevent the dissemination of BBTV to areas where it does not occur. The Americas are free of the disease, but the aphid vector, Pentalonia nigronervosa, is present and the disease would be expected to cause very serious problems if it appeared in smallholdings in the Caribbean and Central or South America. No movement should occur other than by tissue culture plantlets certified as free of BBTV because BBTV transmission has been demonstrated in micropropagated cultures (Drew et al., 1989).
Infected tissue culture plantlets were indistinguishable from uninfected control plantlets in culture (Drew et al., 1992). When plantlets were deflasked after 12 months in culture (as proliferating tissue) and allowed to grow, all plants developed severe symptoms within 1 month and all had died by 4 months. After 16 months in culture, 75% of plantlets showed symptoms, although it took up to 6 months for all plants to develop symptoms. The other 25% grew normally and appeared healthy (Drew et al., 1992). They were later tested for BBTV with negative results.
Helliot et al. (2001) achieved 97-100% eradication of BBTV using meristems from in vivo or in vitro cultured plants. Proliferating tissue cultures initiated from meristems from BBTV-infected plants were also shown to produce virus-free plants (Helliot et al., 2001; DR Jones, Montpellier, France, unpublished, 1995) but it would be advisable to test all germplasm from BBTV-affected areas before meristems are taken to initiate cultures. BBTV has been eliminated from Lakatan (AAA) by heat-treating shoot-tip cultures for extended periods (Ramos and Zamora, 1990). Subsequently, it was reported that the uneven distribution and low concentration of BBTV after exposure of proliferating tissue cultures to heat leads to BBTV-free primordial cells, which in turn develop into healthy plants (Wu and Su, 1991).
Hosts/Species AffectedTop of page
In the Musaceae, BBTV is known to infect a range of Musa species, cultivars in the Eumusa (derived mainly from M. acuminata and M. acuminata x M. balbisiana) and Australimusa (derived mainly from M. maclayi, M. lolodensis and M. peekelii) series of edible banana and Ensete ventricosum (enset). Susceptible Musa species include M. balbisiana (Magee, 1948; Espino et al., 1993), M. acuminata ssp. banksii, M. textilis (abacá) (Magee, 1927), M. velutina (Thomas and Dietzgen, 1991), M. uranoscopos, M. jackeyi, M. ornata and M. acuminata ssp. zebrina (ADW Geering and JE Thomas, Brisbane, personal communication, 1998).
To date, there are no confirmed reports of immunity to BBTV in any Musa species or cultivar. However, differences in susceptibility between cultivars subject to either experimental or field infection have frequently been noted (Magee, 1948; Muharam, 1984; Espino et al., 1993; Ngatat et al., 2017).
Espino et al. (1993) evaluated a total of 57 banana cultivars for their reaction to bunchy top, both by experimental inoculation and field observations. All cultivars in the AA and AAA genomic groups were highly susceptible. However, low levels of infection (as assessed by symptom expression) or total absence of symptoms following aphid inoculation was noted in some cultivars containing the B genome. These included 'Radja' (AAB, syn. 'Pisang Raja' - 12.5% of inoculated plants with symptoms), 'Bungaoisan' (AAB, Plantain subgroup - 0%), 'Pelipia' (ABB, syn. Pelipita' - 10%), 'Pundol' (ABB - 0%), 'Katali' (ABB, syn. 'Pisang Awak' - 0%), 'Abuhon' (ABB - 0%) and 'Turangkog' (ABB - 0%).
These cultivars were not back-indexed by aphid transmission to a susceptible banana cultivar or tested biochemically (for example, by ELISA), so the presence of symptomless infection cannot be ruled out. Also, greater numbers of aphids than the 15 used here may have resulted in infection. Cultivars 'Abuhon' and 'Bungaoisan' are susceptible to BBTV by experimental aphid inoculation (ADW Geering and JE Thomas, Brisbane, personal communication, 1998). Nevertheless, it appears that real differences exist in cultivar reaction to bunchy top and the time taken before symptoms are expressed.
Evaluation of 16 Musa genotypes in Cameroon comprising plantain landraces, Cavendish bananas and synthetic hybrids revealed a high level of tolerance to BBTV in Gros Michel (AAA, Cavendish sub-group) and Fougamou (ABB cooking banana) (Ngatat et al., 2017). In another study of 40 Musa genotypes in Burundi, 8 genotypes (Musa balbisiana type Tani (BB), Kayinja (ABB), FHIA-03 (AABB), Prata (AAB), Gisandugu (ABB), Pisang Awak (ABB), Saba (ABB) and Highgate (AAA, Gros Michel subgroup)) were found to be asymptomatic, although Pisang Awak, Saba and Highgate tested positive to virus indicating tolerance to BBTV in some genotpyes (Niyongere et al., 2011).
Cultivars within the Cavendish subgroup form the basis of the international banana export trade and are generally highly susceptible to bunchy top. However, it appears that not all cultivars with an AAA genome are similarly susceptible. 'Gros Michel' exhibits resistance to the disease under both experimental inoculation and field conditions and Magee (1948) considered that the introduction of this cultivar to Fiji in the early 1900s contributed to partial rehabilitation of the bunchy top-devastated industry. Compared to 'Williams' (AAA, Cavendish subgroup), the concentration of virions of BBTV in infected plants of 'Gros Michel' and the proportion of plants infected by aphid inoculation is lower. Symptoms are also slower to develop and are less severe (Ngatat et al., 2017; ADW Geering and JE Thomas, Brisbane, Australia, unpublished, 1997). These factors may contribute to a reduced rate of aphid transmission and field spread in plantations of 'Gros Michel' (Ngatat et al., 2017).
There is no evidence for hosts outside the Musaceae, though reports have been conflicting. Su et al. (1993) obtained positive ELISA reactions from BBTV-inoculated Canna indica and Hedychium coronarium, and recovery of the virus to banana, though not reported here, was demonstrated (HJ Su, Taipei, personal communication, 1996). Ram and Summanwar (1984) reported Colocasia esculenta as a host of BBTV. However, Hu et al. (1996) were unable to demonstrate C. esculenta or Alpinia purpurata as experimental (E) or natural (N) hosts of BBTV in Hawaii. Geering and Thomas (1996) also found no evidence for the following species as hosts of BBTV in Australia: Strelitzia sp. (N), C. indica (E, N), C. x generalis (N), C. x orchiodes (N), H. coronarium (E), Helocania psittacorum (E), Alpinia coerulea (E, N), A. arundinelliana (E), A. zerumbet (E), Alocasia brisbaensis (E, N) or C. esculenta (E, N). Magee (1927) was unable to infect Strelitzia sp., Ravenala sp., Canna sp. (including C. edulis), Solanum tuberosum and Zea mays. Since the advent of improved and reliable diagnostics for BBTV, searches for alternative hosts outside the Musaceae, including those earlier suspects, have turned out to be negative.
Primary hosts are banana cultivars derived from M. acuminata and M. acuminata x M. balbisiana, and Musa textilis (abacá).
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page Flowering stage, Fruiting stage, Vegetative growing stage
SymptomsTop of page
The typical symptoms of bunchy top of banana are very distinctive and readily distinguished from those caused by other viruses of banana. Plants can become infected at any stage of growth and there are some initial differences between the symptoms produced in aphid-infected plants and those grown from infected planting material.
In aphid-inoculated plants, symptoms usually appear in the second leaf to emerge after inoculation and consist of a few dark-green streaks or dots on the minor veins on the lower portion of the lamina. The streaks form 'hooks' as they enter the midrib and are best seen from the underside of the leaf in transmitted light. The 'dot-dash' symptoms can sometimes also be seen on the petiole. The following leaf may display whitish streaks along the secondary veins when it is still rolled. These streaks become dark green as the leaf unfurls. Successive leaves become smaller, both in length and in width of the lamina, and often have chlorotic, upturned margins. The leaves become dry and brittle and stand more erect than normal giving the plant a rosetted and 'bunchy top' appearance.
Suckers from an infected stool can show severe symptoms in the first leaf to emerge. The leaves are rosetted and small with very chlorotic margins that tend to turn necrotic. Dark-green streaks are usually evident in the leaves.
Infected plants rarely produce a fruit bunch after infection and do not fruit in subsequent years. Plants infected late in the growing cycle may fruit once, but the bunch stalk and the fruit will be small and distorted. On plants infected very late, the only symptoms present may be a few dark green streaks on the tips of the flower bracts (Thomas et al., 1994).
Mild strains of BBTV, which induce only limited vein clearing and dark-green flecks, and symptomless strains have been reported in Cavendish plants from Taiwan (Su et al., 1993). Mild disease symptoms are expressed in some banana cultivars and Musa species. The dark-green leaf and petiole streaks, so diagnostic and characteristic of infection of cultivars in the Cavendish subgroup, can be rare or absent (Magee, 1953). Some plants of 'Veimama' (AAA, Cavendish subgroup), after initial severe symptoms, have been observed to recover and to display few if any symptoms.
List of Symptoms/SignsTop of page
|Fruit / abnormal shape|
|Inflorescence / lesions; flecking; streaks (not Poaceae)|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Whole plant / distortion; rosetting|
|Whole plant / dwarfing|
Biology and EcologyTop of page
BBTV is transmitted by an aphid vector (Pentalonia nigronervosa) and is disseminated in vegetative planting material, but is not transmitted by mechanical inoculation (Magee, 1927).
Distribution and Movement within the Plant
Magee (1927) showed that banana bunchy top was systemic. Following aphid inoculation, symptoms generally do not appear until a further two or more leaves have been produced (Magee, 1927). This period can vary between 19 days in summer to 125 days in winter (Allen, 1978a). The virus can only be acquired by aphids from the first symptom leaf or those formed subsequently (Magee, 1940). Suckers produced on an infected stool generally develop severe symptoms before reaching maturity (Magee, 1927). The emergence of virus-free suckers from an infected stool due to incomplete virus systemicity in the corm has been reported (Djailo et al., 2016) but was found to be temporary with the virus later invaded apparently healthy parts of the corm and stool.
Magee (1939) also concluded that the virus was restricted to the phloem tissue. Microscopic examination revealed hypertrophy and hyperplasia of the phloem tissue and a reduction in the development of the fibrous sclerenchyma sheaths surrounding the vascular bundles. The cells surrounding the phloem contained abnormally large numbers of chloroplasts giving rise to the macroscopic dark-green streak symptom.
Subsequent investigation using RNA probes and PCR (Hafner et al., 1995) has demonstrated that BBTV replicates for a short period at the site of aphid inoculation, then moves down the pseudostem to the basal meristem, then finally to the corm, roots and newly formed leaves. Trace levels of virus were eventually detected by PCR in leaves formed prior to inoculation, but replication was not demonstrated. This latter observation is consistent with the inability to transmit the virus by aphids from such leaves (Magee, 1940) and with the sequential development of single, new leaves from the basal meristem.
BBTV has been detected by ELISA and/or PCR in most parts of the plant, including leaf lamina and midrib, pseudostem, corm, meristematic tissues, roots, fruit stalk and fruit rind (Thomas, 1991; Wu and Su, 1992; Hafner et al., 1995; Hooks et al., 2009b; Peng et al., 2012).
BBTV is efficiently disseminated in conventional planting material including corms, bits and suckers. All suckers from an infected stool will eventually become infected (Djailo et al., 2016). Magee (1927) demonstrated 100% transmission of bunchy top through new 'eyes' (meristematic growing points) even in a plant that had only been expressing symptoms for 2-3 weeks.
BBTV is also transmitted in micropropagated banana plants (Drew et al., 1989; Ramos and Zamora, 1990; Wu and Su, 1991) though not always at rates of 100%. From time to time, apparently virus-free meristems producing apparently virus-free plants can arise from an infected clone (Thomas et al., 1995; Djailo et al., 2016).
In Pakistan in the early 1990s, much of the available planting material of 'Basrai' (AAA, Cavendish subgroup) was infected with BBTV. Plantations established from infected suckers and corms were completely unproductive.
Epidemiology of Banana Bunchy Top
The epidemiology of banana bunchy top in Australia, as well as in sub-Saharan Africa, is simplified by the presence of a single susceptible host and a single vector species (P. nigronervosa). Dissemination over long distances is by infected planting material and it is by this means that new plantings in isolated areas usually become infected. Spread over short distances from these infection foci is by the banana aphid (Kumar et al., 2011).
In studies of outbreaks of bunchy top in commercial banana plantations, Allen (1978b, 1987) showed that the average distance of secondary spread of the disease by aphids was only 15.5-17.2 m. Nearly two-thirds of new infections were within 20 m of the nearest source of infection and 99% were within 86 m. Allen and Barnier (1977) showed that if a new plantation was located adjacent to a diseased plantation, the chance of spread of bunchy top into the new plantation within the first 12 months was 88%. This chance was reduced to 27% if the plantations were separated by 50-1000 m, and to less than 5% if they were 1000 m apart. On average, the interval between infection of a plant and movement of aphids from this plant to initiate new infections elsewhere (the disease latent period) was equivalent to the time taken for 3.7 new leaves to emerge. The rate of leaf emergence varied seasonally with a maximum in summer (Allen, 1987). On the basis of these studies, a computer program has been developed which simulates epidemics of bunchy top (RN Allen, Brisbane, 1994, personal communication). This program, which is commercially available, allows epidemiological factors to be varied and their effect on the progess of the epidemic and disease control to be monitored.
In the Philippines, Opina and Milloren (1996) also demonstrated that most new infections were adjacent to or in close proximity to primary sources of infection. In Malawi, the spread of BBTV within the country was attributed to human movement of planting material and cultural practices (Kumar et al., 2011). Inadvertent multiplication and distribution of infected planting material by government and non-governmental programmes and the movement of infected suckers by migrant workers and refugees are thought to be the major factor for the spread of BBTV in sub-Saharan Africa (Kumar et al., 2011; Mukwa et al., 2014).
Means of Movement and DispersalTop of page
In Australia, the banana aphid (Pentalonia nigronervosa) was considered to have a role in the etiology of banana bunchy top (Darnell-Smith, 1924) and in 1925 was conclusively demonstrated to be the vector (Magee, 1927). Banana aphids have a worldwide distribution with a host range that includes Musa textilis and other species in the Musaceae. Species in several closely related plant families including the Araceae (Alocasia sp., Caladium spp., Dieffenbachia spp., Xanthosoma sp.), Cannaceae (Canna spp.), Heliconiaceae (Heliconia spp.), Strelitzeaceae (Strelitzia spp.) and Zingiberaceae (Alpinia spp., Costus sp., Hedychium spp.) are also colonized (Wardlaw, 1961; RN Allen, Brisbane, Australia, personal communication, 1996). However, a degree of host preference is displayed and some difficulty can be experienced transferring them between host species. Recently, mitochondrial COI sequence based analysis identified lineages on most of the non-Musa hosts as Pentalonia caladii (Foottit et al., 2010), a recently proposed species, and P. nigronervosa was dominant on Musa. A recent population genetics study of Pentalonia aphids using mitochondrial COI or microsatellite markers found that P. nigronervosa and P. caladii include distinct genotypes, demonstrating the occurrence of intraspecific genetic variation in populations in Hawaii, India and also in Nigeria (Galambao, 2011; Savory and Ramakrishnan 2015; PL Kumar, IITA, Nigeria, unpublished data). Aphids were found more frequently near the base of plants, followed by the newest unfurled leaf at the top of the plant. Aphids were least likely to be located on leaves in between the top and bottom of the plant (Robson et al., 2006). Aphid numbers decrease during periods of drought (Wardlaw, 1961).
Transmission of BBTV is of the persistent, circulative, non-propagative type (Anhalt and Almeida, 2008). The transmission parameters reported from Hawaii (Hu et al., 1996) and Australia (Magee, 1927), respectively, are: minimum acquisition access period 4 h/17 h; minimum inoculation access period 15 min/30 min-2 h; retention of infectivity after removal from virus source 13 days/20 days; a latent period of 20-28 h for virus transmission was detected. Similar parameters have also been reported by Thiribhuvanamala et al. (2001) from India and Ngatat et al. (2017) from Cameroon. No evidence was found for transmission of BBTV to the parthenogenetic offspring (Magee, 1940; Hu et al., 1996) or for multiplication of BBTV in the aphid vector (Hafner et al., 1995; Watanabe et al., 2013).
Transmission efficiency for individual aphids has been reported as ranging from 46 to 67% (Magee, 1927; Wu and Su., 1990a; Hu et al., 1996) and the virus is more efficiently acquired by nymphs than by adults (Magee, 1940).
Colonies of P. nigrHooks et al., onervosa from Australia (where bunchy top occurs) and from Reunion Island (where bunchy top does not occur) both transmitted each of six isolates of BBTV with similar efficiency (ML Iskra-Caruana, Montpellier, personal communication, 1994).
Banana plants treated with systemic herbicide can serve as source for virus acquisition for up to 6 weeks after treatment (Hooks et al., 2009a).
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||Yes||Pest or symptoms usually invisible|
|Flowers/Inflorescences/Cones/Calyx||Yes||Pest or symptoms usually invisible|
|Fruits (inc. pods)||Yes||Pest or symptoms usually invisible|
|Leaves||Yes||Pest or symptoms usually visible to the naked eye|
|Roots||Yes||Pest or symptoms usually invisible|
|Seedlings/Micropropagated plants||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground)/Shoots/Trunks/Branches||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|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|
Vectors and Intermediate HostsTop of page
Impact SummaryTop of page
|Fisheries / aquaculture||None|
Economic ImpactTop of page
BBTV is the most serious virus disease of bananas and plantains. Devastating epidemics occurred in Fiji at the turn of the century and in Australia in the 1920s. The economic effect in northern New South Wales was dramatic. Between 1922 and 1926, about 90% of the area under bananas had gone out of production, despite a rapid expansion of the industry to compensate for abandoned farms. In the Currumbin district in southern Queensland, the number of plantations fell from 100 to 4 between 1922 and 1925, and production plummeted by over 95% (Dale, 1987). In recent years, bunchy top disease has been decimating the banana industry in Pakistan. In the early 1990s, statistics revealed that the area under banana cultivation in Sindh province fell by 55% in 1 year (Jones, 1994). BBTV is a major constraint to production in many areas where it occurs. In sub-Saharan Africa, BBTV was the main contributor to a reduction in banana bunch production by up to 70-90% in disease affected areas (Kumar et al., 2015). Precise estimates of losses due to BBTV are not known. However, Cook et al. (2012) estimated that implementation of BBTV exclusion measures prevented Aus$15.9-27.0 million in annual losses for the banana industry in Australia. This study suggests significant economic benefit in controlling BBTV.
DiagnosisTop of page
Prior to 1990, the only assays available for banana bunchy top were visual assessment of symptoms and aphid transmission to a sensitive banana cultivar. Subsequently, both serological and nucleic acid-based assays have become available.
Polyclonal and monoclonal antibodies are now routinely used in ELISA to detect BBTV in field and tissue culture plants and can detect the virus in single viruliferous aphids (Wu and Su, 1990b; Dietzgen and Thomas, 1991; Thomas and Dietzgen, 1991; Thomas et al., 1995). Triple antibody sandwich-ELISA was found to be the optimum assay format for routine virus indexing (Geering and Thomas, 1996). Double antibody sandwich (DAS)-ELISA has also been used to successfully detect BBTV (Prakash et al., 2010). All isolates tested from Africa, Australia, Asia and the Pacific region are serologically related (Thomas, 1991).
A variety of nucleic acid-based assays have been applied to the detection of BBTV in plant tissue and viruliferous aphids, including DNA and RNA probes, labelled either non-radioactively or with 32P (Hafner et al., 1995; Xie and Hu, 1995). PCR has proved to be about one thousand times more sensitive than ELISA or dot blots with DNA probes (Xie and Hu, 1995; Zhou and Zheng, 2001; Manickam et al., 2002). Substances in banana sap inhibitory to PCR can be circumvented by simple extraction procedures (Thomson and Dietzgen, 1995) or by immunocapture PCR (Anceau, 1996; M Sharman, JE Thomas and RG Dietzgen, Brisbane, Australia, personal communication, 1997).
More recently, isothermal assays such as Loop-mediated Isothermal Amplification (LAMP) (Peng et al., 2012) and Recombinase Polymerase Amplification (RPA) (Kapoor et al., 2017) assays have been developed for BBTV detection.
Detection and InspectionTop of page The presence of 'dot-dash' symptoms on leaves almost certainly indicates that a plant is infected with BBTV. The rosetted appearance of leaves which are progressively shorter, narrower and more upright is noticeable at a distance. Yellowing of the leaf margins is also indicative, though this can be caused by other problems.
Prevention and ControlTop of page
BBTV has not been eradicated from any country where it occurs, but it is believed to have been eliminated from certain banana-growing districts in Australia. Here, the disease is kept in check by strict State Government legislation which controls the source and movement of planting material, controls the issue of planting permits and requires the destruction of feral plants and all plants with symptoms. Banana inspectors are also employed to police these regulations and locate diseased and feral plants. An ambitious programme of eradication is on-going which is based on replacing plantations where the disease regularly occurs, with BBTV-tested, tissue-cultured, planting material (Thomas et al., 1994). Another initiative to control the spread of BBTV in Africa, named ALLIANCE for BBTV control in Africa, aims to contain the spread of BBTV from disease-affected areas to new regions through quarantine regulations and the recovery of banana production by eradication of infected stools and replanting with health planting material (Kumar et al., 2016; www.bbtvalliance.org).
When little work had been undertaken on testing germplasm for resistance, it was thought that all cultivars were susceptible, although some may take longer to develop symptoms and others may escape infection because of aphid preferences or host morphological factors. However, work in Australia suggested that Musa coccinea, a wild species, and the cultivar Kluai Teparot (ABBB/ABB) may have physiological resistance (J Thomas, QDPI, Indooroopilly, Queensland, Australia, personal communication, 1995). Several studies have since been undertaken to evaluate Musa genotypes for BBTV resistance and found genotypes with tolerance (no symptoms and near normal performance of virus infected plants (e.g. Gros Michel), delayed expression of symptoms (e.g. Dwarf Apple, also known as Santa Catarina) and difficult to infect (e.g. Fugamou) (Espino et al., 1993; Hooks et al., 2009b; Niyongere et al. 2011; Ngatat et al., 2017).
Banana bunchy top disease can be effectively controlled by the eradication of diseased plants and the use of virus-tested planting material. Before destruction, diseased plants should first be sprayed with power kerosene or insecticide to kill all viruliferous aphids. The whole stool, including corm and all associated suckers, must then be destroyed by uprooting and chopping into small pieces or by herbicide treatment, as the virus will ultimately spread to all parts of the mat. Control must be practised across the whole production area to avoid the rapid re-infection of virus-tested planting material (Thomas et al., 1994; Kumar et al., 2016).
Aphicides have been used in some countries to control populations of Pentalonia nigronervosa, the aphid vector of bunchy top, and a decrease in disease incidence has been reported. In Tonga, Aphidius colemani, a parasitic wasp, has been released in an attempt at biological control of the aphid vector, but its effects on disease incidence have been disappointing.
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15/10/17 Review by:
Lava Kumar, International Institute of Tropical Agriculture (IITA), Ibadan, Nigeria.
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