Introduction

Viral diseases that banana suffers from

Diseases caused by bacteria, fungi, and viruses are the primary factors limiting crop production quality and creating a barrier to international germplasm trading (Kumar et al. 2015). Various bacterial and fungal pathogens include particularly the Xanthomonas campestrispv. Musacearum (Xcm) that cause banana xanthomonas wilt (BXW) disease; Ralstonia solanacearum, causing the disease known as moko and bugtok and blood disease, Pseudocercospora eumusae, P. fijiens, P. musae, causing leaf spot disease, black Sigatoka and yellow Sigatoka, respectively, as well as Fusarium oxysporum f. sp. cubense causing fusarium wilt or the Panama disease (Ploetz 2015; Tripathi et al. 2016). On the other hand, over 20 virus species from various families have been identified as infecting bananas globally (Kumar et al. 2015). The economically significant banana viruses are banana bunchy top virus (BBTV) (Babuvirus genus in the Nanoviridae family); several species of banana streak virus (BSV) (Badnavirus genus in the Caulimoviridae family); banana bract mosaic virus (BBrMV) (Potyvirus genus in the Potyviridae family); cucumber mosaic virus (CMV) (Cucumovirus genus in the Bromoviridae family) (Tchatchambe et al. 2020; Tripathi et al. 2021). BSV, BBrMV, and CMV have been found in all banana-producing countries, whereas BBTV is found only in a few (Tripathi et al. 2021).

Banana bunchy top disease: Discoveryand its geographical distribution

One of the most common virus diseases linked to banana cultivation is banana bunchy top disease (BBTD), which spreads quickly over a short period of time (Chakraborty et al. 2023). BBTD is most likely to have originated in the genus Musa; first reported during a widespread outbreak in Cavendish banana (AAA) in Fiji (in the year 1879) (Magee 1927), is the most overwhelming virus disease of banana and plantain (Dale 1987). However, the virus was isolated in the late 1980s. BBTD is currently present in over 36 countries across Africa, Asia, Oceania, and the South Pacific, including 17 African countries, and banana-producing neighbouring countries are at substantial risk of infection (Kumar et al. 2011; Adegbola et al. 2013; Jooste et al. 2016). It is common in Southeast Asia and the South Pacific, being reported in parts of India and Africa, as well as Sri Lanka, in parts of China, Indonesia, Malaysia, Vietnam, Philippines, Taiwan, Japan, Iran, Nepal and Pakistan, Bangladesh, Myanmar, and Thailand. In the last decade, BBTV has spread to at least six African countries, including Benin, Cameroon, Mozambique, Nigeria, South Africa, and Zambia (Tripathi et al. 2021). An outbreak of BBTV occurred in Togo in 2018, but early detection and eradication stopped the disease from disseminating (IITA News 2019); and is hypothesized that the disease is spreading continuously in banana-producing areas, resulting in lower crop yield (Ngatat et al. 2017; Tripathi et al. 2021). Recently, its emergence has been reported for the first time in Bengkulu, Indonesia (Sutrawati and Ginting, 2020); in sub-Saharan Africa, Tanzania and East Africa (Kolombia et al. 2021; Shimwela et al. 2022).

BBTV: Vector and transmission

BBTV infection causes BBTD and is possibly the most damaging viral infection in bananas, with a significant economic impact on banana productivity (Tripathi et al. 2021). The movement of infected plant material causes long-distance spread of the phloem-limited BBTV virus, transmitted from plant to plant by the aphid (Drew et al. 1989; Thomas et al. 1995).

Importantly, BBTV spread via an aphid, Pentalonia nigronervosa Coquerel, and also by the infected planting materials (Tripathi et al. 2021), via vegetative propagules, i.e., corms/suckers and tissue-cultured plants (Drew et al. 1989); but not mechanically (Dietzgen 1991; Hu et al. 1996). Banana aphids are well-known BBTV vectors that transmit BBTV in a persistent, circulative, and non-propagative manner (Anhalt and Almeida 2008). Thepersistent-transmission implies that the virus stays inside the vector throughout its lifetime, with a relatively long acquisition period (a few hours to many days) during a meal on an infected plant. After being consumed by the vector, the viruses enter the gut and go beneath the intestinal wall. The viruses may spread from the hemolymph to the salivary glands and infect new plants (circulative transmission). During the transfer, no additional viral replication occurs (i.e., non-propagative transmitted) (Raccah and Fereres 2009; Gray et al. 2014; Murhububa et al. 2021).

According to Robson et al. (2006), aphids are typically located close to the base of banana plants, followed by the topmost newly-unfurled leaf. Aphids transmit BBTV after 4 hours (minimum period) of acquisition access and 15 minutes of inoculation access (Hu et al. 1996), with adult aphids transmitting BBTV more efficiently than third instar nymphs. In general, BBTV acquisition and inoculation efficiency peak after 18 hours of plant access (Anhalt and Almeida 2008). It has a high population growth rate at 25°C compared to 20 or 30°C. However, the banana aphid could not spread BBTV below 16°C, so BBTD is absent in high-altitude tropical locations below that temperature. Also, BBTV transmission is proportional to the number of virulent aphids feeding on healthy hosts and inversely proportional to host age (Wu and Su 1990a). In terms of the P. caladii aphid (another closely related species), there is insufficient research on the transmission of BBTV via P. caladii in fields. However, laboratory testing on transmission studies revealed that P. caladii is capable to acquire BBTV from the infected plants and transmit it to the uninfected banana plants (Foottit et al. 2010; Watanabe et al. 2013).

BBTV: Etiology and diversity

The BBTV genome has been revealed, and its genetic variability has extensively studied as molecular techniques have advanced over the last two decades (Magee 1927). BBTV is an isometric virus with a diameter of 18-20 nm with a genome composed of at least six circular, single-stranded (ss) DNA components, each with a size of approximately 1 Kb. In contrast, the molecular interactions of viral proteins with host metabolites and proteins have received little attention (Qazi 2016). The protein functions and viral interactions of BBTV are comparable to those of the Geminiviridae ssDNA plant virus family.

Different BBTV isolates have been divided into two distinct lineages based on the phylogenetic relationships among the DNA-R component sequences: (i) the Pacific-Indian Oceans (PIO) group, which consists of isolates from Tonga, Hawaii, Australia, Africa, South Asia, and Myanmar (ii) the South-East Asian (SEA) group (Asian group), which includes isolates from China, Indonesia, Japan, Taiwan, the Philippines, and Vietnam (Karan et al. 1994; Stainton et al. 2012; Yu et al. 2012; Banerjee et al. 2014). Around the world, various BBTV isolates with >85% homology have been identified (Banerjee et al. 2014). In India, the genetic diversity of BBTV isolates is minor (Vishnoi et al. 2009; Selvarajan et al. 2010a), though the north-eastern region has a relatively higher diversities (Banerjee et al. 2014), including an identification of a new Babuvirus—Cardamom bushy dwarf virus (CBDV)—in cardamom (Mandal et al. 2013).

About BBTV Family and Genus

Plant viruses are classified as DNA or RNA viruses in Baltimore's viral taxonomy (Baltimore 1971). Based on the genomic organization, the International Committee on Virus Taxonomy (ICTV) divided ssDNA plant viruses into two families: Geminiviridae and Nanoviridae (Randles et al. 2000; Vetten et al. 2012; Zerbini et al. 2017). Geminiviridae is a large plant virus family capable of infecting diverse ranges of plant hosts from various genera and families. Plant viruses in this family have extremely small virions with 6-8 multipartite DNA genomes, each about 1.0 kb in length, and a few satellite molecules, each with a specific function (Vetten et al. 2012; Briddon et al. 2018; Malathi and Dasgupta 2019). The Nanoviridae family has been divided into two genera, Nanovirus and Babuvirus; based on genome organization and transmission vectors, while coconut foliar decay virus (CFDV) is an unclassified species (Mandal, 2010). Nanoviruses have multipartite 8-10 circular ssDNA that is 1 kb in size (Sano et al. 1998; Gronenborn 2004). Babuvirus members have six components, each approximately 1.0-1.1 kb in size (Halbert and Baker 2015). The ssDNA rolling circle replication process, which is used by viruses to replicate themselves, takes place in the nuclei of infected cells (Rosario et al. 2012; Jeske 2018). Members of the Nanoviridae family have a wide range of host plants, causing symptoms such as leaf rolling, mosaicism, necrosis, dwarfism, stunted growth, and ultimately plant death (Mandal 2010; Grigoras et al. 2014; Hull 2014; Gaafar et al. 2017, 2018). Furthermore, virus transmission by aphids is a feature of the Nanoviridae family (Sano et al. 1998). Infection with Nanoviridae is a new emerging threat in the agricultural sector as aphids transmit Nanovirus and Babuvirus genus members (Lal et al. 2020). The number of reports of Nanoviridae members from various parts of the world has increased. The aphid vectors P. nigronervosa and Micromyzus kalimpongensis spread Babuvirus (Almeida et al. 2009; Bressan and Watanabe 2011; Ghosh 2016; Halbert and Baker 2015; Qazi 2016). BBTV is a circular single-stranded plant DNA virus and is a typical member of the genus Babuvirus of the Nanoviridae family (Burns et al. 1995; Sharman et al. 2008; Qazi 2016). The most commonly infected species by BBTV are M. acuminata, M. coccinea, M. balbisiana, M. ornata, M. jackeyi, M. textilis, and M. velutina. Babuvirus members are among the most common viruses in the Nanoviridae family, and BBTV has been reported almost everywhere in the world (Sun 1961; Burns et al. 1995; Beetham et al. 1997; Amin et al. 2008; Almeida et al. 2009; Blomme et al. 2013). They have been found to infect the monocot species of the Musaceae and Zingiberaceae families but may infect any other plant families (Burns et al. 1995; Mandal et al.2004; Amin et al. 2008). In the hosts, babuvirus members (ABTV, BBTV and CBDV) cause dark green streaks, streak mosaicism, and a bushy appearance (Lal et al. 2020).  

BBTV genome

BBTV is an ssDNA virus with a multipartite genome composed of six circular components or virions, which include DNA-R, -U3, -S, -M, -C, and -N (earlier named DNA 1-6), each of which is approximately 1.1 kb in size and approximately 18-20 nm diameter (Harding et al. 1993; Burns et al. 1995). All six components have at least one open reading frame (ORF) for a major gene in the virion sense, polyadenylation signals linked to each gene, a major common region (CR-M), a stem-loop common area (CR-SL), a potential TATA box 30 of the stem-loop (Burns et al.1995). Rep protein, encoded by DNA-R, initiates viral DNA replication, DNA-S encodes the coat protein (CP), DNA-M encodes the movement protein (MP),DNA-C stands for cell cycle link protein (Clink), DNA-N stands for nuclear shuttle protein (NSP) and DNA-U3 stands for unknown function (Burns et al. 1995; Wanitchakorn et al. 1997, 2000).

Localization of BBTV in plants and replication of their genome

BBTV replicates in a way similar to the other nanoviruses and geminiviruses (Harding et al. 1993; Wu et al. 1994; Sano et al. 1998; Timchenko et al. 1999). Like the other nanoviruses in BBTV, one of the Rep protein genes is a master Rep (M-Rep) capable of activating genomic component replication (Timchenko et al. 2000). One of the earliest events is the synthesis of viral double-stranded (ds) DNA using host DNA polymerases and endogenous primers attached to genomic DNA (Hafner et al. 1997b). The host RNA polymerase produces mRNAs from these dsDNA forms that encode the M-Rep and other viral proteins needed for viral replication. M-Rep binds to similar sequence signals on all genomic DNAs and initiates viral DNA replication.

In vitro studies have revealed that the BBTV Rep proteins can nick and connect within the conserved sequence TAT/GTATT-AC (Herrera-Valencia et al. 2007; Hafner et al. 1997a). BBTV replicates in phloem; BBTV NSP has expressed alone, and it is transported to the nucleus, however when combined with MP, it is transported to the cell periphery (Wanitchakorn et al. 2000). BBTV may use a system similar to geminiviruses in which NSP binds to viral DNA for intercellular transport. The MP transports the NSP-DNA complexes to the cell periphery. Due to differences in the copy number and transcript levels of various genomic components, multipartite DNA viruses exhibit extremely flexible gene expression. As a result, they are better able to adjust to shifting circumstances and keep themselves in top physical condition (Bashir et al. 2022).

BBTV infection in host plant and symptoms

Majority of the banana cultivars are highly susceptible to BBTV (Ngatat et al. 2017), has been found in species such as M. acuminata, M. balbisiana, M. coccinea, M. jackeyi, M. ornata, M. textilis, and M. velutina (Magee1927, 1948; Thomas and Dietzgen 1991; Thomas et al. 2000; Furuya et al. 2003). Depending on the time of infection, variations in symptoms appear in the banana cultivars (Nelson 2004; Qazi 2016). BBTV infection at an early age makes the susceptible cultivars severely stunted, and when they do bear fruit, the fruit is likely to be twisted and deformed. Additionally, the symptoms in the field may vary depending on the time and the infection severity (Thomas et al. 2000). Early symptoms include distinctive dark green veins streaks of varying length on the leaves, forming a dot-dash pattern known as the Morse code pattern. Infected plants produce leaves that are shorter, narrower, brittle in texture, bunch up at the top, and have wavy leaf lamina and yellow leaf margins (Thomas et al. 1994; Nelson 2004; Tripathi et al. 2021). Infected plants' phloem and associated parenchyma become disorganized, with excessive, irregular divisions and many cells becoming chlorophyllous, giving rise to the dark green dots and streaks in the leaves, midribs, and petioles (Magee 1940). Characteristic symptoms of advanced infection include dwarfing, upright, and bunchy leaves at the top, with wavy and chlorotic margins that eventually turn necrotic (Magee 1940).

Because of their inconspicuous nature, the incubation period from virus inoculation to symptom expression ranges from 19 to 125 days, depending on the stage of infection, cultivar, and weather (Allen 1978; Hooks et al. 2008). Symptoms appear faster at high temperatures than at low temperatures, both in the field and controlled environment cabinets (Sun 1961; Dale et al. 1987). Although the leaf appears normal to untrained eyes, symptoms are visible upon closer inspection (Thomas et al. 1994). The presence of dark green streaks on the lower midrib and thereafter on the secondary veins is the first observable symptom. Streaks are composed of dot-dash patterns, or "Morse code," that become more evident on the leaf blade. Holding the leaf up to the light makes it easier to see the dark-green hook-like vein extensions that extend down along the midrib towards the petiole. These extensions are best visible from the underside of the leaf. 'Primary' and 'secondary' terms are used to distinguish between aphid-caused infections and those spread from the mother plant to suckers (Thomas et al. 1994). The symptoms of BBTD become more severe when the disease is transferred from an infected mother plant. Infected plants typically have stunted growth, twisted and distorted bunches, and infrequent fruit production. When the infected plant flowers, the bracts veins of the inflorescence display sporadic streaks that resemble the symptoms of the "Morse code" on petioles and leaves (mottled inflorescence). Male flower buds' bracts sporadically develop into leafy structures with dark green dots and streaks (Thomas et al. 1994). Infected plants' fruit production declines by 70% to 100% in the first season, and are unable to recover from infections (Ngatat et al. 2017).

Diagnosis of BBTV

To identify the viral particles, a number of techniques are used based on the characteristics of the virus, such as biological activities, physical features of the virus particle, the makeup of viral proteins, and the viral nucleic acid (Hull 2009). The electron microscopy (EM) technique is generally dependable and relies on the physical properties of the virus particle to deliver accurate information (Hull 2009). However, this method's basic need for virus identification requires knowledge of the virus particle's size, shape, and surface characteristics. Today, a negative-staining technique is available to look for viral particles in crude extracts or un-purified preparations (Hull 2009). In the rapid epidermal strip method, a strip of leaf epidermis is cut and wiped over a negative stain on the EM grid. Negative stains such as ammonium molybdate, sodium phosphotungstate, or uranyl acetate may be used, depending on the resistance the viruses have to a particular stain. However, this method has limitations, such as the inability to distinguish between virus particles and normal cell components. Large, enveloped viruses, plant reoviruses, and rod-shaped viruses in thin sections frequently deviate from the typical internal cell structures, making them easily detectable (Hull 2009). Depending on the properties of viral proteins, several other techniques have been developed to identify and quantify interactions between antibodies (abs) and antigens (ags). The most widely used methods for identifying Ab-virus interaction are the enzyme-linked immune-absorbent assay (ELISA), immunosorbent electron microscopy (ISEM), and dot blots using either polyclonal Abs or monoclonal Abs. A method for identifying viruses based on their protein composition is sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) is frequently used to separate proteins according to size and net electric charge at the pH (Hull 2009). The position and number of the proteins can be determined using a nonspecific technique like staining or a specific approach like an immunoassay, such as western blotting (Hull 2009).

Another detection method takes into account, the characteristics of the viral nucleic acid (Hull 2009). It is essential to classify an unknown virus into a family or group based on its viral nucleic acid, such as whether it is double- or single-stranded, made up of one or more segments, or DNA or RNA. As a result of the ability to make DNA copies (complementary DNA or cDNA) of the entire or specific regions of a plant virus' RNA genome, numerous new possibilities are emerging. With the exception of dsRNA, these characteristics are of limited use for typical diagnosis, detection, or assay. Number of copies of DNA, and nucleotide sequences can be determined, but with a few exceptions, such as the process being far too time-consuming to be used as a diagnostic tool. Therefore, the four primary methods of using nucleic acids for virus diagnosis are the type and molecular size of the associated nucleic acids, the pattern of viral DNA or cDNA cleavage, the hybridization of nucleic acids, and the polymerase chain reaction (PCR) (Hull 2009).

ELISA, a commercially available technique relying on monoclonal and polyclonal abs, is the first detection method used for BBTV (Thomas and Dietzgen 1991; Wu and Su 1990b). Diverse ELISA techniques (triple antibody sandwich ELISA, plate-trapped antigen ELISA, double antibody sandwich ELISA) have been developed for the accurate identification of the virus in field-grown plants, aphids, and tissue culture plants (Wu and Su 1990b; Thomas and Dietzgen 1991; Geering and Thomas 1996; Selvarajan et al. 2010b). The viruses could be found in the inoculated plants after 12–25 days in any part of the infected plant, depending on the genotype and stage of infection. However, samples from the mid-rib region of the youngest leaf provide the most sensitive detection. For the sensitive detection of BBTV, methods that employ nucleic acid spot hybridization (NASH) with DNA probes have been used (Harding et al. 1991; Xie and Hu 1995; Selvarajan and Balasubramanian 2008). However, PCR-based techniques have become the primary method for viral identification in plants and vectors due to their increased sensitivity and adaptability (Xie and Hu 1995; Hu et al. 1996; Thiribhuvanamala et al. 2005; Galal 2007). DNA primers have been designed for the amplification of BBTV, components 1-6, and virus-associated satellite DNAs (Qazi et al. 2016). Additionally, various primers are available to differentiate isolates from the PIO and SEA (Burns et al.,1995; Sharman et al. 2000; Mansoor et al. 2005; Stainton et al. 2012). A protocol technique could be performed for virus isolation from tissues without homogenization, to achieve rapid virus detection using PCR (Thomson and Dietzgen 1995). For the quantitative detection of viral DNA segments in plant and aphid tissues, real-time PCR techniques with TaqMan probes are also used (Bressan and Watanabe 2011; Chen and Hu 2013). Rolling circle amplification (RCA) and loop-mediated isothermal amplification (LAMP) are two techniques for DNA amplification that have been developed (Peng et al. 2012). The product of LAMP can be identified visually by observing turbidity or changes in color or by traditional agarose gel electrophoresis (Peng et al. 2012). Recombinase polymerase amplification is another isothermal technique being looked at for the detection of BBTV. For quick and sensitive detection outside the lab at temperatures between 37°C and 42°C, this technology is rapidly evolving as a DNA amplification technique (Piepenburg et al. 2006).

Conclusion

Production of bananas is restricted by a variety of biotic and abiotic stresses. The pressure from diseases and pests on bananas is unlikely to lessen in the near future. Therefore, a thorough plan and policy must be created to address this issue before it has a disastrous impact on the global economy and food security.

Conflict of Interest

Authors declares no conflict of interest.

References

Adegbola RO, Ayodeji O, Awosusi OO, Atiri G I, Kumar PL (2013) First report of banana bunchy top virus in banana and plantain (Musa spp.) in Nigeria. Plant Disease, 97(2):290-290.

Allen RN (1978) Epidemiological factors influencing the success of rouging for the control of bunchy top disease of bananas in New South Wales [Virus-like pathogen transmitted by the banana aphid (Pentalonia nigronervosa)]. Australian Journal of Agricultural Research, 29:535-544.

Almeida RPP, Bennett, GM, Anhalt, MD, Tsai, C W, O’Grady, P (2009) Spread of an introduced vector‐borne banana virus in Hawaii. Molecular Ecology, 18(1):136-146.

Amin I, Qazi J, Mansoor S, Ilyas M, Briddon RW (2008) Molecular characterisation of banana bunchy top virus (BBTV) from Pakistan. Virus genes, 36(1):191-198.

Anhalt MD, Almeida RPP (2008) Effect of temperature, vector life stage, and plant access period on transmission of banana bunchy top virus to banana. Phytopathology, 98(6):743-748.

Baltimore D (1971) Expression of animal virus genomes. Bacteriological Reviews, 35(3):235-241.

Banerjee A, Roy S, Behere GT, Roy SS, Dutta SK, Ngachan, SV (2014) Identification and characterization of a distinct banana bunchy top virus isolate of Pacific-Indian Oceans group from North-East India. Virus Research, 183: 41-49.

Bashir S, Farrakh S, Yasmin T, MuhammadA, Bashir T, Manghwar H, Mora-Poblete F, Iqbal S, Baazeem A, Hyder, MZ (2022) Quantitation of multipartite banana bunchy top virus genomic components and their transcripts in infected tissues of banana (Musa acuminata). Agronomy, 12(12):2990

Beetham PR, Hafner GJ, Harding RM, Dale JL (1997) Two mRNAs are transcribed from banana bunchy top virus DNA-1.Journal of General Virology: 78(1):229-236.

Blomme G, Ploetz R, Jones D, De Langhe E, Price N, Gold C,Geering A, Viljoen A,KaramuraD, Pillay M, Tinzaara W, Teycheney PY, Lepoint P, Karamura E,Buddenhagen I(2013) A historical overview of the appearance and spread of Musa pests and pathogens on the African continent: Highlighting the importance of clean Musa planting materials and quarantine measures. Annals of Applied Biology, 162(1):4-26.

Bressan A, Watanabe S (2011)Immunofluorescence localisation of banana bunchy top virus (family Nanoviridae) within the aphid vector, Pentalonia nigronervosa, suggests a virus tropism distinct from aphid-transmitted luteoviruses. Virus Research, 155(2):520-525.

Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olivé E, Moriones E, Lett JM, Zerbini FM,Varsani A (2018) Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus-and nanovirus-associated alphasatellites. Archives of Virology, 163(9):2587-2600.

Burns TM, Harding RM, Dale JL (1995) The genome organization of banana bunchy top virus: analysis of six ssDNA components. Journal of General Virology, 76(6):1471-1482.

Chakraborty S, Dutta S, Barman M, Samanta S, Sarkar KP, Poorvasandhya R, Tarafdar J (2023) Detection and in silico characterization of banana bunchy top virus in West Bengal, India: relevance to global genetic diversity and population structure. VirusDisease. doi:10.1007/s13337-023-00815-0

Chen Y,Hu X (2013) High-throughput detection of banana bunchy top virus in banana plants and aphids using real-time TaqMan® PCR. Journal of Virological Methods, 193(1):177-183.

Dale JL (1987) Banana bunchy top:An economically important tropical plant virus disease. Advances in Virus Research, 33:301-325.        

Dale JL, Phillips DA, Parry JN (1986) Double-stranded RNA in banana plants with bunchy top disease. Journal of General Virology, 67(2):371-375.

Dietzgen RG, Thomas JE (1991) Properties of virus-like particles associated with banana bunchy top disease in Hawaii, Indonesia and Tonga. Australasian Plant Pathology, 20(4):161-165.

Drew RA, Moisander JA, Smith MK (1989) The transmission of banana bunchy-top virus in micropropagated bananas. Plant Cell Tissue and Organ Culture, 16:187-193.

Foottit RG, Maw HEL, Pike KS, Miller RH (2010) The identity of Pentalonia nigronervosa Coquerel and P. caladii van der Goot (Hemiptera: Aphididae) based on molecular and morphometric analysis. Zootaxa, 2358(1):25-38.

Furuya N, Susamto S, Keiko NT (2004) Virus detection from local banana cultivars and the first molecular characterization of banana bunchy top virus in Indonesia. Journal of Agricultural Science, 49:75-81.

Gaafar Y, Cordsen Nielsen G,Ziebell H (2018) Molecular characterisation of the first occurrence of pea necrotic yellow dwarf virus in Denmark. New Disease Reports, 37:16.

Gaafar Y, Timchenko T, Ziebell H (2017) First report of pea necrotic yellow dwarf virus in the Netherlands. New Disease Reports, 35(23): 2044-20588.

Galal AM (2007) Use of polymerase chain reaction for detecting banana bunchy top nanovirus. Biotechnology, 6(1): 53-56.

Geering ADW, Thomas JE(1997) Search for alternative hosts of banana bunchy top virus in Australia. Australasian Plant Pathology, 26(4): 250-254.

Ghosh A, Das A, Vijayanandraj S, Mandal B (2016). Cardamom bushy dwarf virus infection in large cardamom alters plant selection preference, life stages, and fecundity of aphid vector, Micromyzuskalimpongensis (Hemiptera: Aphididae). Environmental Entomology, 45(1): 178-184.

Gray S, Cilia M, Ghanim M (2014) Circulative, “non propagative” virus transmission: an orchestra of virus-, insect-, and plant-derived instruments. Advances in Virus Research, 89: 141-199.

Grigoras I, del Cueto Ginzo AI, Martin DP, Varsani A, Romero J, Mammadov AC, Huseynova IM, Aliyev JA, Kheyr-Pour A, Huss H, HeikoZiebell H, Timchenko T, Vetten HJ Gronenborn B (2014) Genome diversity and evidence of recombination and reassortment in nanoviruses from Europe. Journal of General Virology, 95(5):1178-1191.

Gronenborn B (2004) Nanoviruses: Genome organisation and protein function. Veterinary Microbiology, 98(2):103-109.

Hafner GJ, Harding RM, Dale JL (1997a). A DNA primer associated with banana bunchy top virus. Journal of General Virology, 78(2):479-486.

Hafner GJ, Stafford MR, Wolter LC, Harding RM,Dale, JL (1997b) Nicking and joining activity of banana bunchy top virus replication protein in vitro. Journal of General Virology, 78(7):1795-1799.

Halbert SE, Baker CA (2015) Banana bunchy top virus and its vector Pentalonia nigronervosa (Hemiptera: Aphididae). Florida Department of Agriculture and Consumer Services, Division of Plant Industry Pathology Circular: 417(8).

Harding RM, Burns TM, Dale JL (1991) Virus-like particles associated with banana bunchy top disease contain small single-stranded DNA. Journal of General Virology, 72(2):225-230.

Harding RM, Burns TM, Hafner G, Dietzgen RG, Dale JL(1993) Nucleotide sequence of one component of the banana bunchy top virus genome contains a putative replicase gene. Journal of General Virology, 74(3):323-328.

Herrera-Valencia, VA, Dugdale, B, Harding, RM, Dale, JL (2007)Mapping the 5′ ends of banana bunchy top virus gene transcripts. Archives of Virology, 152(3): 615-620.

Hooks CRR, Wright MG, Kabasawa DS, Manandhar R, Almeida RPP (2008) Effect of banana bunchy top virus infection on morphology and growth characteristics of banana. Annals of Applied Biology, 153(1):1-9.

Hu JS, Wang M, Sether D, Xie W, Leonhardt KW (1996) Use of polymerase chain reaction (PCR) to study transmission of banana bunchy top virus by the banana aphid (Pentalonia nigronervosa). Annals of Applied Biology, 128(1):55-64.

Hull R (2009)Comparative plant virology. Elsevier Academic Press, London, p 245.

Hull R(2014) Plant virology. Academic press, San Diego, p 145.

IITA News (2018) Building regional capacity to contain banana bunchy top disease (BBTD) spread in West Africa. https://www.iita.org/wp-content/uploads/2019/01/Bulletin_2469. Accessed 18 January 2019

Jeske H (2018) Barcoding of plant viruses with circular single-stranded DNA based on rolling circle amplification. Viruses, 10(9):469.

JoosteAEC, Wessels N, Van der Merwe M (2016) First report of banana bunchy top virus in banana (Musa spp.) from South Africa. Plant Disease, 100(6):1251.

Karan M, Harding RM, Dale JL (1994) Evidence for two groups of banana bunchy top virus isolates. Journal of General Virology, 75(12): 3541-3546.

Kolombia YA, Oviasuyi T, Dzola AK, Ale Gonh-Goh A, Atsu T, Oresanya A, Ogunsanya P, Alabi T, Kumar PL (2021) First report of banana bunchy top virus in banana (Musa spp.) and its eradication in Togo. Plant Disease, 105(10):3312.

Kumar PL, Hanna R, Alabi OJ, Soko MM, Oben TT, Vangu GHP, Naidu RA (2011) Banana bunchy top virus in sub-Saharan Africa: Investigations on virus distribution and diversity. Virus Research, 159(2):171-182.

Kumar PL, Selvarajan R, Iskra-Caruana ML, Chabannes M, Hanna R (2015) Biology, etiology, and control of virus diseases of banana and plantain. Advances in Virus Research, 91:229-269.

Lal A, Vo TTB, Sanjaya IGNPW, Ho PT, Kim JK, Kil EJ, Lee S (2020) Nanovirus disease complexes: An emerging threat in the modern era. Frontiers in Plant Science, 11, 558403. doi: https://doi.org/10.3389/fpls.2020.558403

Magee CJ (1927) Investigation on the bunchy top disease of bananas. Bulletin of the Council for Scientific and Industrial Research in Australia, 30: 64.

Magee CJ(1948) Transmission of bunchy top to banana varieties. Journal of the Australian Institute of Agricultural Science, 14:18-24.

Magee CJP (1940) Transmission studies on the banana bunchy top virus. Journal ofthe Australian Institute of Agricultural Science, 6:109-110.

Malathi VG, Dasgupta I (2019) Insights into the world of ssDNA viruses. Virus Disease, 30(1):1-2.

Mandal B (2010) Advances in small isometric multicomponent ssDNA viruses infecting plants. Indian Journal of Virology, 21(1):18-30.

Mandal B, Mandal S, Pun KB, Varma ACPV (2004) First report of the association of a nanovirus with foorkey disease of large cardamom in India. Plant Disease, 88(4):428-428.

Mandal B, Shilpi S, Barman AR, Mandal S, Varma A (2013) Nine novel DNA components associated with the foorkey disease of large cardamom: evidence of a distinct babuvirus species in Nanoviridae. Virus Research, 178(2): 297-305.

Mansoor S, Qazi J, Amin I, Khatri A, Khan IA, Raza S, Zafar Y,Briddon RW (2005) A PCR-based method, with internal control, for the detection of banana bunchy top virus in banana. Molecular Biotechnology, 30(2):167-169.

Murhububa SI, Tougeron K, Bragard C, Fauconnier ML, BasengereBE, WalangululuMasamba, J, Hance, T (2021) Banana tree infected with banana bunchy top virus attracts Pentalonia nigronervosa aphids through increased volatile organic compounds emission. Journal of Chemical Ecology, 47(8):755-767.

Nelson SC (2004) Banana bunchy top: Detailed signs and symptoms. Knowledge Creation Diffusion Utilization, 1-22.

Ngatat S, Hanna R, Kumar PL, GraySM, Cilia M, Ghogomu RT, Fontem DA (2017)Relative susceptibility of Musa genotypes to banana bunchy top disease in Cameroon and implication for disease management. Crop Protection, 101:116-122.

Peng J, Fan Z, Huang J (2012) Rapid detection of banana streak virus by loop‐mediated isothermal amplification assay in South China. Journal of Phytopathology, 160(5):248-250.

Piepenburg O, Williams CH, Stemple DL, Armes NA (2006) DNA detection using recombination proteins. PLoS Biology, 4:Article e204.

Ploetz RC, Kepler AK, Daniells J, Nelson SC (2007) Banana and plantain-an overview with emphasis on Pacific Island cultivars. In:Elevitch CR (ed) Species profiles for Pacific Island agroforestry. Ver. 1. Permanent Agriculture Resources (PAR), Hawaii, pp 1-27.

Qazi J (2016) Banana bunchy top virus and the bunchy top disease. Journal of General Plant Pathology, 82(1): 2-11.

Raccah A, Fereres A (2009) Plant virus transmission by insects. In:Maldener I, Muro-Paster AM (eds). Encyclopedia of life sciences (ELS). John Wiley & Sons, pp1-9.

Randles JW, Chu PWG, Dale JL, Harding R, Hu J, Katul L, Vetten HJ (2000) Nanoviridae. In: van Regenmortel MH, Fauquet CM, Bishop DH, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR,WicknerRB (eds), Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego.

Raut SP, Ranade S (2004) Diseases of banana and their management. In Naqvi, SAMH (Ed), Diseases of fruits and vegetables Diagnosis and management. Volume II: Diagnosis and Management. Springer, pp. 37-52.

Robson JD, Wright MJ, Almeida RPP (2006) Within-plant spatial distribution and binomial sampling of Pentalonia nigronervosa (Hemiptera: Aphididae) on banana. Journal of Economic Entomology, 99(6):2185-2190.

Rosario K, Duffy S, Breitbart M (2012) A field guide to eukaryotic circular single-stranded DNA viruses:Insights gained from metagenomics. Archives of Virology, 157(10):1851-1871.

Sano Y, Wada M, Hashimoto Y, Matsumoto T, Kojima M (1998) Sequences of ten circular ssDNA components associated with the milk vetch dwarf virus genome. Journal of General Virology, 79(12):3111-3118.

Selvarajan R, Balasubramanian V (2008) Banana viruses. In: Rao GP, Mytra A, Ling K(eds), Characterization, diagnosis and management of plant viruses. Studium Press LLC, pp. 109-124

Selvarajan R, Sheeba M, Balasubramanian V, Rajmohan R, Dhevi NL, Sasireka T (2010a) Molecular characterization of geographically different banana bunchy top virus isolates in India. Indian Journal of Virology, 21(2):110-116. 

Selvarajan R, Balasubramanian V, Dayakar S, Sathiamoorthy S, Ahlawat YS (2010b) Evaluation of immunological and molecular techniques for the detection of different isolates of banana bunchy top virus in India. Indian Phytopathology, 63:333-336. 

Sharman M, Thomas JE, Dietzgen RG (2000) Development of a multiplex immunocapture PCR with colourimetric detection for viruses of banana. Journal of Virological Methods, 89(1-2): 75-88.

Sharman M, Thomas JE, Skabo S, Holton T A (2008) Abacá bunchy top virus, a new member of the genus Babuvirus (family Nanoviridae). Archives of Virology, 153(1):135-147.

Shimwela MM, Mahuku G, Mbanzibwa DR, Mkamilo, G, Mark D, Mosha HI, Pallangyyo B, Fihavango M, Oresanya A, Ogunsanya P, Kumar, PL (2022) First report of banana bunchy top virus in banana and plantain (Musa spp.) in Tanzania. Plant Disease, 106(4):1312.

Singh HP, Uma S, Selvarajan R, Karihaloo JL (2011) Micropropagation for production of quality banana planting material in Asia-Pacific. Asia-Pacific Consortium on Agricultural Biotechnology (APCoAB). New Delhi, India, 92.

Stainton D, KrabergerS, Walters M, Wiltshire EJ, Rosario K, Lolohea S, Katoa I, Faitua TH, Aholelei W, Taufa L, Thomas JE, Collings DA, Martin DP, Varsani A (2012). Evidence of inter-component recombination, intra-component recombination and reassortment in banana bunchy top virus. Journal of General Virology, 93(5): 1103-1119.

Sun SK (1961). Studies on the bunchy-top disease of banana. Special Publication College of Agriculture, National Taiwan University, 10:82-109.

Sutrawati M, Ginting S (2020) First report of banana bunchy top disease on banana in Bengkulu. Plant Disease, 3(2):82-87.

Tchatchambe NBJ, Ibanda N, Adheka G, Onautshu O, Swennen R, Dhed’a D (2020) Production of banana bunchy top virus (BBTV)-free plantain plants by in vitro culture. African Journal of Agricultural Research, 15(3):361-366.

Thiribhuvanamala G, Sabitha D, Ganapathy T (2005) Detection of banana bunchy top virus in the aphid vector using double antibody sandwich (DAS) ELISA. Indian Journal of Virology, 16:12-14.

Thomas JE, Dietzgen RG (1991) Purification, characterization and serological detection of virus-like particles associated with banana bunchy top disease in Australia. Journal of General Virology, 72(2):217-224.

ThomasJE, Iskra-Caruana ML, Jones D R (2000) Diseases caused by viruses, bunchy top. Disease of banana, abaca and enset. CABI Publishing, Wallingford.

Thomas JE, Iskra-Caruana ML, Jones DR (1994) Banana bunchy top disease. Musa Disease Fact Sheet No. 4. INIBAP, Montpellier.

Thomson D,Dietzgen RG (1995) Detection of DNA and RNA plant viruses by PCR and RT-PCR using a rapid virus release protocol without tissue homogenization. Journal of Virological Methods, 54(2-3):85-95.

Timchenko T, De Kouchkovsky F, Katul L, David C, Vetten HJ,Gronenborn B (1999) A single rep protein initiates replication of multiple genome components of faba bean necrotic yellows virus, a single-stranded DNA virus of plants. Journal of Virology, 73(12):10173-10182.

Timchenko T, Katul L, Sano Y, de KouchkovskyF, Vetten HJ, Gronenborn B(2000) The master rep concept in Nanovirus replication: Identification of missing genome components and potential for natural genetic reassortment. Virology, 274(1):189-195.

Tripathi S, Patil BL, Verma R (2016) Viral diseases of banana and their management. In: Gaur R, Petrov N, Patil B, Stoyanova M (eds), Plant viruses: Evolution and management. Springer, pp 289–308

Tripathi L, Ntui VO, Tripathi JN (2019) Application of genetic modification and genome editing for developing climate‐smart banana. Food and Energy Security, 8(4): Article e00168.

Tripathi L, Ntui VO, Tripathi JN, Kumar PL (2021) Application of CRISPR/Cas for diagnosis and management of viral diseases of banana. Frontiers in Microbiology, 11: 609784.

Vetten HJ, Dale JL, Grigoras I, Gronenborn B, Harding R, Randles JW (2012) Family Nanoviridae in virus taxonomy: Ninth report of the international committee on taxonomy of viruses. Elsevier, p 395-404.

Vishnoi R, Raj SK, Prasad V (2009) Molecular characterization of an Indian isolateof banana bunchy top virus based on six genomic DNA components. Virus Genes, 38 (2):334-344.

Wanitchakorn R, Hafner GJ, Harding RM, DaleJL (2000) Functional analysis of proteins encoded by banana bunchy top virus DNA-4 to-6. Journal of General Virology, 81(1):299-306.

Wanitchakorn R, Harding RM, Dale JL (1997) Banana bunchy top virus DNA-3 encodes the viral coat protein. Archives of Virology, 142(8):1673-1680.

Watanabe S, Greenwell AM,Bressan A (2013) Localization, concentration, and transmission efficiency of banana bunchy top virus in four asexual lineages of Pentalonia aphids. Viruses, 5(2):758-776.

Wu RY, Su HJ (1990a) Transmission of banana bunchy top virus by aphids to banana plantlets from tissue culture. Botanical Bulletin of Academia Sinica, 31(1):7-10.

Wu RY, Su HJ (1990b) Purification and characterization of banana bunchy top virus. Journal of Phytopathology, 128(2):153-160.

Wu RY, You LR, Soong TS (1994) Nucleotide sequences of two circular single-stranded DNAs associated with banana bunchy top virus. Phytopathology, 84(9):952-957.

Xie WS, Hu JS (1995) Molecular cloning, sequence analysis, and detection of banana bunchy top virus in Hawaii. Phytopathology, 85(3):339-347.

Yu NT, Zhang YL, Feng TC, Wang JH, Kulye M, Yang WJ, Lin ZS, Xiong Z,Liu ZX (2012) Cloning and sequence analysis of two banana bunchy top virusgenomes in Hainan. Virus Genes, 44:488-494.

Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rafael Rivera-Bustamante R, Roumagnac P, Varsani A, Consortium IR (2017) ICTV virus taxonomy profile: Geminiviridae. The Journal of General Virology, 98(2):131-133.