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
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ABSTRACT
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Article history:
Received
08 April 2023
Received in revised form
21 May 2023
Accepted
Keywords:
Banana bunchy top;
BBTV;
Disease;
Vector;
Virus detection;
Viruses
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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.
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Introduction
DOI: 10.52228/NBW-JAAB.2023-5-1-3
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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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