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Author(s): Smriti Adil1, Afaque Quraishi*2

Email(s): 115oct.sadil@gmail.com, 2drafaque13@gmail.com

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    1School of Studies in Biotechnology, Pt. Ravishankar Shukla University, Raipur, Chhattisgarh, India
    2School of Studies in Biotechnology, Pt. Ravishankar Shukla University, Raipur, Chhattisgarh, India
    *Corresponding Author Email- drafaque13@gmail.com

Published In:   Volume - 5,      Issue - 1,     Year - 2023


Cite this article:
Smriti Adil, Afaque Quraishi (2023) An aphid transmitted banana bunchy top disease of banana and its detection: A Review. NewBioWorld A Journal of Alumni Association of Biotechnology,5(1):10-19.

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 NewBioWorld A Journal of Alumni Association of Biotechnology (2023) 5(1):10-19            

REVIEW ARTICLE

An aphid transmitted banana bunchy top disease of banana and its detection: A Review

 

Smriti Adil1and Afaque Quraishi1*

1School of Studies in Biotechnology, Pt. Ravishankar Shukla University, Raipur, Chhattisgarh, India.

Author’s Email- 15oct.sadil@gmail.com, drafaque13@gmail.com

*Corresponding Author Email- drafaque13@gmail.com

ARTICLE INFORMATION

 

ABSTRACT

Article history:

Received

08 April 2023

Received in revised form

21 May 2023

Accepted

25 May 2023

Keywords:

Banana bunchy top;

BBTV;

Disease;

Vector;

Virus detection;

Viruses

 

One of the most significant horticultural crops in the world, the banana is an edible fruit (technically a berry) produced by a variety of large herbaceous flowering plants in the genus Musa. It is grown in about 120 different countries around the world. Particularly, virus intensification between subsequent plantings via contaminated planting material limits the banana crop yield. Banana bunchy top virus (BBTV) control is challenging because it spreads vegetatively (through suckers or in vitro plantlets) and by an aphid Pentalonia nigronervosa Coquerel, thus increasing the virus potential for dispersal within the fields. To propagate plants, exchange germplasm, breed better genotypes, and distribute them are challenging to use planting material that has been virus affected. Diagnosis of the BBTV, relies essentially only upon the symptom’s recognition of infection and, seldom, with additional affirmation by aphid transmission. At present, polymerase chain reaction (PCR) based and non-PCR techniques are available for BBTV detection. Implementation of these diagnostic tools and procedure facilitates the identification of healthy ones of the germplasm that can be used in propagation systems.

 


Graphical Abstract


Introduction

DOI: 10.52228/NBW-JAAB.2023-5-1-3

Bananas and their closely related plantains (Musa spp.) were among the first crop plants domesticated by humans (Singh et al. 2011). Bananas are herbaceous perennial monocots cultivated in the tropical and subtropical areas worldwide. It is a major staple food crop for millions and generates income through local and international trade (Singh et al. 2011). Numerous factors, including biotic and abiotic stresses (diseases and pests posing a major threat), limit banana yields globally (Tripathi et al. 2019). Almost all commercial banana cultivars are highly susceptible to certain lethal diseases (Raut and Ranade 2004).

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.

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