Banana bunchy top virus

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 A 260/280 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 (c omponent 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.