akhter 2019

Crop Protection 118 (2019) 57–65
Contents lists available at ScienceDirect
Crop Protection
journal homepage: www.elsevier.com/locate/cropro
Plant virus diseases and their management in Bangladesh
a,c,1
M.S. Akhter
b
c
d
, A.M. Akanda , K. Kobayashi , R.K. Jain , Bikash Mandal
T
d,∗
a
Fruit Research Station, Bangladesh Agricultural Research Institute (BARI), Rajshahi, Bangladesh
Bangabandhu Sheikh Mujibur Rahman Agricultural University (BSMRAU), Gazipur, Bangladesh
Laboratory of Plant Molecular Biology and Virology, Graduate School of Agricultural Sciences, Ehime University, Japan
d
Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute (IARI), New Delhi, India
b
c
A R T I C LE I N FO
A B S T R A C T
Keywords:
Bangladesh
Plant virus disease
Begomovirus
Cucumovirus
Potyvirus
Tospovirus
Plant virus vector
Plant virus management
Plant virus diseases are significant constraints in agricultural production in Bangladesh. The hot and humid
environmental conditions are highly favourable for the perpetuation of the viruses as well as vectors round the
year. Although, the virus diseases are recorded in many crops, vegetables and pulses are most seriously affected.
Several viruses belonging to the genera Begomovirus, Cucumovirus, Potyvirus and Tospovirus have been recorded
during the last decade. Whitefly and thrips-transmitted viruses have emerged as major constraints in the horticultural crops. Management of viral diseases largely depends on the control of insect vectors by widespread
application of insecticides. The epidemics of leaf curl, yellow vein, yellow mosaic and bud necrosis diseases were
witnessed in the recent past. However, the knowledge of identity and diversity of viruses occurring in
Bangladesh are largely lacking. This review provides the first comprehensive account of viral disease problems in
the cultivation of several important crops and their management in Bangladesh.
1. Introduction
Plant viruses have been recognised as one of the major constraints
in agricultural production Worldwide. The information on plant virus
diseases is generally well documented in the developed countries. The
impact of plant viruses on agricultural production in the developing and
underdeveloped countries are difficult to assess adequately due to lack
of research facilities and expertise. Devastating losses caused by plant
viruses have been witnessed in many countries in the South and South
East Asia (Mandal et al., 2012; Rishi, 2009; Schreinemachers et al.,
2015; Varma and Malathi, 2003).
Bangladesh situated in South East Asia adjacent to India has a typical hot-humid tropical environment with numerous rivers and water
bodies. Bangladesh is an agriculture-based country with 8.52 million
hectares of cultivable land, where a wide range of crops such as cereals,
fibers, fruits, oilseeds, pulses and vegetables are cultivated. Plant diseases caused by viruses are serious constraints in agriculture in
Bangladesh (Fakir, 1984). The tropical climate favours a high prevalence of viruses and their vectors in Bangladesh. Ever increasing
population pressure exerts intense demands on food production; as a
result, a large number of high yielding crop varieties are introduced
from other countries. Favourable environmental conditions, lack of
resistance in high yielding cultivars and lack of appropriate plant
protection measures contributed the outbreak of viral diseases in several crops (Akanda, 1991; Akanda et al., 1991a,1991b; Akhter et al.,
2012; Muqit and Akanda, 2007). The viruses under the genera Cucumovirus, Potyvirus and Tobamovirus are endemic in nature, whereas
Begomovirus and Tospovirus are emerging as significant problems. Plant
viral diseases have been reported throughout Bangladesh by several
researchers (Supplementary Tables 1, 2, 3, 4, 5). The distribution of the
reported plant viruses in Bangladesh is presented in the Fig. 1. However, a comprehensive status of viral disease problems in the different
crops in Bangladesh is not available. The present review summarises the
problems of plant virus diseases in the major crops in Bangladesh and
highlights the measures for the management of the plant virus diseases.
2. History of virus research
The earliest documentation of virus disease in pre-independent
Bangladesh was leaf mosaic of jute (Ghosh and Basak, 1951). Before the
liberation of Bangladesh (1971), rice tungro, mosaic of lentil and
chickpea were reported (Miah, 1977; Bakr, 1994; Islam et al., 1970;
Fakir et al., 1978). During the early 1980s, virus diseases in pulse such
as sterility mosaic and yellow mosaic of pigeon pea, yellow mosaic of
mungbean and pea, and leaf crinkle in mungbean were documented
(Ahmed et al., 1981; Ahmed, 1984a). A comprehensive survey of virus
∗
Corresponding author.
E-mail addresses: [email protected], leafcurl@rediffmail.com (B. Mandal).
1
Present address: Plant Pathology Division, Bangladesh Agricultural Research Institute (BARI), Joydebpur, Gazipur, Bangladesh.
https://doi.org/10.1016/j.cropro.2018.11.023
Received 4 July 2018; Received in revised form 24 November 2018; Accepted 26 November 2018
0261-2194/ © 2018 Elsevier Ltd. All rights reserved.
Crop Protection 118 (2019) 57–65
M.S. Akhter et al.
Fig. 1. Distribution of tospoviruses, begomoviruses, potyviruses and other viruses in Bangladesh.
symptomatology. A few studies have been conducted using serology
and molecular tools through international collaborations. Plant virus
detection based on serological techniques was launched during 1986-87
in collaboration with Kyushu University, Japan. In 1986, an electron
microscopy facility was established in the Institute of Postgraduate
Studies in Agriculture (now known as Bangabandhu Sheikh Mujibur
Rahman Agricultural University), Gazipur with the support of the Japan
International Cooperation Agency, which boosted the plant virus research in Bangladesh. The genomic information of viruses was generated during 1996–2007 with the collaborations of International Rice
Research Institute (IRRI), Philippines, World Vegetable Centre, Taiwan
and Greenwich University, UK. Of late, the genomic properties and
diversity of some important viruses occurring in Bangladesh have been
studied at the Advanced Centre for Plant Virology, Indian Agricultural
Research Institute, New Delhi, India, which was funded by The World
Academy of Science.
diseases based on symptomatology, mechanical inoculation, host range,
electron microscopy, ultra-structural study and serology was conducted
throughout the country during 1986–87, which was the first benchmark
survey of plant virus diseases in Bangladesh documenting the occurrence of twenty plant viruses (Akanda et al., 1991a). The variation in
the genome of rice tungro bacilliform virus was reported in 1996, and
this constituted the first genomic information of a plant virus in Bangladesh (Fan et al., 1996). A begomovirus, tomato leaf curl Bangladesh
virus (ToLCBDV) was identified in 2001, and this was the first molecular diagnosis of the plant virus infecting Solanaceous vegetables in
Bangladesh (Green et al., 2001). Subsequently, the genetic diversity of
several begomoviruses and their betasatellites were studied (Maruthi
et al., 2005a, 2005b; 2005c, 2007). Among the RNA viruses, papaya
ringspot virus pathotype-P (PRSV-P) was the first virus identified in
2004 based on its genome sequence (Jain et al., 2004). Subsequently,
the genetic diversity of PRSV-P population in Bangladesh has been
documented (Akhter et al., 2013).
4. Epidemics and crop losses
3. Institution and collaboration
The prevalence of virus diseases is known in many different crops,
but the magnitudes of yield loss have not been estimated for all.
However, some estimates of crop loss are available for a few serious
diseases (Table 1). Tospovirus of tomato has emerged as a significant
problem (Farooq and Akanda, 2007a, 2007b). During the 2010–2011
cropping seasons of tomato, epidemics of bud necrosis disease caused a
widespreadloss in tomato production in Rajshahi district, where
groundnut bud necrosis virus (GBNV) was identified to be associated
Bangladesh Agricultural Research Institute and Bangabandhu
Sheikh Mujibur Rahman Agricultural University are the two major institutions where plant virus research work has been addressed.
Although, some research work on plant viruses have also been reported
from Bangladesh Rice Research Institute, Bangladesh Agricultural
University, University of Dhaka and Jahangirnagar University.
Determination of virus diseases in Bangladesh is largely based on
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Table 1
Significant yield loss in some vegetable and pulse crops due to viral infection in
Bangladesh.
Crop
Associated virus
% Yield loss
References
Potato
Potato leafroll virus
Potato virus Y
Potato virus X
Potato virus M
Potato virus A
Tomato leaf curl virus
78
Up to
5–15
Up to
Up to
Up to
Mungbean yellow
mosaic virus?
Mungbean yellow
mosaic virus?
Bhendi yellow vein
mosaic virus
Up to 100
Hossain et al. (1989)
Hossain and Ali (1992)
Muqit and Akanda (2007)
Muqit and Akanda (2007)
Muqit and Akanda (2007)
Gupta (2000); Muqit and
Akanda (2007)
Jalaluddin and Shaikh
(1981)
Afzal et al. (1999)
Tomato
Mungbean
Black gram
Okra
95
25
30
95
20–100
Up to 94
Ali (1999); Muqit and
Akanda (2007)
?: Not confirmed.
with the disease (Akhter et al., 2012). Cultivation of tomato early in
winter, when rainfall is low results in a high population of thrips that
favours widespread occurrence of GBNV. Leaf curl of tomato is a
chronic problem resulting in up to 95% crop losses in some places and
seasons. During last decade, cultivation of papaya in Bangladesh was
seriously affected by PRSV (Fig. 2 a-c), but in the recent years, leaf curl
disease has emerged as another serious threat to papaya production. A
number of plant viruses are known to infect potato in Bangladesh, but
only potato virus Y (PVY) and potato leafroll virus (PLRV) are serious
threats to the potato production every year. The yellow mosaic disease
is a major constraint in the production of pulses. Up to 85–100% crop
losses in mungbean and black gram have been witnessed in Bangladesh
(Table 1).
5. Viral diseases of cereals
Cereals including wheat, rice, maize, barley, oats, millet, sorghum,
buckwheat are cultivated in Bangladesh. Rice is the main food crop
grown in Bangladesh, and 80% of its population is dependent on rice
farming. About 10.5 million ha of land are cultivated only for rice, and
the cropping intensity is increasing as a result of population increase.
On the other hand, wheat, maize, barley and millets were cultivated on
only 0.63 million ha (Karim et al., 2008). Although several types of
cereal crops are grown in Bangladesh, information of virus diseases is
available only on rice and maize.
Rice tungro is a serious viral disease of rice in South and Southeast
Asia including Bangladesh (Anjaneyulu et al., 1994). Tungro disease of
rice was recorded in Bangladesh during 1966 and has been reported as
the most damaging viral disease of rice in Bangladesh (Miah, 1977).
Stunting of the plant along with twisting of the leaves, reduced tillering,
delayed flowering, etc. are the distinguishing features of the disease.
The vector green leafhopper population is high in every year during
April, June–July and October–November and tungro diseases incidence
is also high in susceptible varieties (Rahman et al., 2007). In 1987, a
high incidence (85-81%) of tungro was recorded in the southern to
northwestern parts of the country. The ratoon crop of paddy acts as a
source of the virus for subsequent rice infection (Ali and Miah, 1990).
The yield loss due to tungro infection in Bangladesh was estimated to be
52.34% (Quazi et al., 2009). The restriction endonuclease map and
cross-hybridisation analysis of the genome of rice tungro bacilliform
virus (RTBV) from Bangladesh and other countries in Southeast Asia
(India, Malaysia, Indonesia, Thailand and the Philippines) showed that
the isolate from Bangladesh is related to the Indian isolate (Fan et al.,
1996). The preliminary study based on partial nucleotide sequences of
the coat protein gene of rice tungro spherical virus isolate from Bangladesh showed it to be different from those in other Southeast countries (Zhang, 1993).
Fig. 2. Significant plant virus diseases in Bangladesh. Seriously affected papaya
plantation with yellow mosaic on leaves and ringspots on fruit (a, b, c). Banana
plant infected by bunchy top disease (d). A cucumber field showing severe
damage by yellow mosaic disease (e). Extensive damage of tomato crop due to
tospovirus causing bud necrosis disease (f, g). The widespread occurrence of
yellow mosaic in mungbean (h). (For interpretation of the references to colour
in this figure legend, the reader is referred to the Web version of this article.)
Maize being a minor crop in Bangladesh, has limited information is
available for viral diseases. The survey, monitoring and identification
viral diseases of maize were undertaken during 1980 in Ishurdi, Jessore,
Jamalpur, Hathazari, Savar dairy farm and Sreepur, where mosaic,
dwarf mosaic, stripe and streak diseases were observed with 2–40%
incidence. The incidence of these diseases varied among different locations and varieties. Information on the specific identity of the virus
affecting maize and their impact on yield is not available.
6. Viral diseases of fibre crops
Bangladesh has a famous history in the production of the finest
cotton fabric, ‘Moslin’. The production and trading of Moslin gradually
declined during the British rule and the industry ultimately closed by
the early nineteenth century. Yet, the garment industries are flourishing
in Bangladesh and presently contribute 27% of GDP. The garment
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industry depends on the fibre crops as raw materials. The principal fibre
crops grown in Bangladesh are cotton (Gossypium spp.), Jute (Corchorus
capsularis and Corchorus olitorius), kenaf (Hibiscus cannabinus) meshta
(Hibiscus sabdariffa) and sunn hemp (Crotalaria juncea). Of all these
fibre crops, jute ranks number one. In the fiscal year 2012–13, earnings
from the jute sector was US$ 1.01 billion. The studies on viral diseases
of fibre crops have been conducted only in jute.
A yellow mosaic disease of jute (C. capsularis) is known in
Bangladesh since 1917 (Finlow, 1917). The mosaic disease of jute occurs widely in the major jute growing countries, Bangladesh, Burma
and India (Ghosh and Basak, 1951). The disease is characterised by
crinkled, leathery leaves with yellow mosaic symptoms and stunting of
plants. The effect of jute mosaic disease on jute production was investigated, and it has been considered to be one of the most important
biotic factors causing a reduction in yield and quality of jute fibre and
stick (Das et al., 2001). The disease is readily transmitted by whitefly
(Bemicia tabaci) (Ahmed, 1978; Dastogeer et al., 2012; Ghosh et al.,
2008). Management of mosaic disease through vector control and cultural practices was carried out, which suggested early removal of
symptomatic plants, application of one insecticidal spray and one extra
booster dose of nitrogen at about 30 and 45 days post- emergence of
plants were beneficial in reducing the disease in Mymensingh region
(Hoque et al., 2003). Corchorus golden mosaic virus (CoGMV), a bipartite begomovirus species was identified based on the complete
genome sequence of DNA-A and eB in jute mosaic in Bangladesh. Sequence analysis of several isolates of CoGMV from Bangladesh revealed
the existence of greater genetic diversity compared to that in India and
Vietnam (Hasan and Sano, 2014).
culture propagated plantlets. The presence of viruses in the propagative
materials poses a risk of circulation of viruses or strains in the new
areas. Virus diagnostic services and use of virus-free planting material is
very important for preventing possible virus outbreak in commercial
banana cultivation in Bangladesh.
Papaya (Carica papaya) is an important fruit crop in Bangladesh due
to its high nutritional value and diverse use as fruit and vegetable. It is
grown in the backyard garden as well as in large-scale farms. Foliar
mosaic and fruit ringspot disease (Fig. 2a–c) caused by papaya ring spot
virus (PRSV) is the major threat to papaya production in Bangladesh.
The occurrence of PRSV in Bangladesh was first confirmed based on the
serological test (Akanda, 1991; Akanda et al.,1991b, 1991d). In 2004,
PRSV was further identified in papaya based on electron-microscopy
and genome sequence analysis (Jain et al., 2004). PRSV is prevalent all
over Bangladesh with an estimated yield loss of 72–100% depending on
the time of infection and symptom severity (Akanda et al., 1991d). Of
the various symptoms induced by PRSV, leaf distortion was observed to
cause the most severe damage in the growth and yield of papaya under
field conditions (Akhter and Akanda, 2008). The genetic diversity of
PRSV population from the different papaya growing regions in Bangladesh based on the sequence of coat protein was estimated up to 14%
(Akhter et al., 2013). Leaf curl disease of papaya is emerging as a serious problem in the northern region of Bangladesh. The samples collected from Chapai Nawabganj showed the presence of tomato leaf curl
New Delhi virus (ToLCNDV) (Maruthi et al., 2007).
9. Viral diseases of pulses
7. Viral diseases of oilseeds
Several pulse crops are cultivated in Bangladesh. Lentil (Lens culinaris), chickpea (Cicer arietinum), grass pea (Lathyrus sativus), faba bean
(Vicia faba) are grown in the winter season, and black gram (Vigna
mungo) and mungbean (Vigna radiata) are grown in the summer season.
There are several biotic and abiotic stresses, which limit the pulse
cultivation in Bangladesh. Mosaic, yellow mosaic, mottling, stunting
and sterility mosaic diseases are frequently observed in the different
pulse crops, but their causal agents have not been clearly established
(Fakir, 1983). Different plant viruses have been tentatively identified
from pulse crops based on symptoms and serology (Supplementary
Table 1).
Mungbean, one of the most important pulses in Bangladesh, is seriously affected by the yellow mosaic disease (Fig. 2 h) with an estimated yield loss of 67–100% (Jalaluddin and Shaikh, 1981). Black
gram cultivation is also equally affected by the yellow mosaic disease.
The severe outbreak of this disease resulted in a shift in the cropping
pattern. The disease appears at any stage of crop growth; however, the
yield loss is severe when plants are affected at an early stage. The total
loss was recorded when the infection occurred at 1-2 week-old crop,
whereas 63% and 20–30% of loss were observed when infection took
place at 3 and 4-7 week-old crop, respectively. Symptoms of the disease
appear on leaves as minute yellow specks that expand and cover the
entire leaf area resulting in mosaic disease. Pods are reduced in size and
bear small and shrivelled seeds. A total of eight mungbean varieties,
BINA Moog-5, BARI Mung-3, BARI Mung-4, BARI Mung-5, BARI Mung6, BU Mung-1, BU Mung-2 and BU Mung-4, were evaluated at field
conditions for yield performance, incidence and severity of yellow
mosaic disease (Ali et al., 2010). The highest disease incidence (64%)
and disease severity score (8.73) was found in BARI Mung-4, and the
lowest incidence (33.01%) and disease severity score (3.36) was observed in BARI Mung 6. The yellow mosaic disease is spread through
whitefly (Bemisia tabaci). Mungbean yellow mosaic disease is known to
occur in India, and the causal virus has been identified as two begomovirus species, mungbean yellow mosaic India virus and mungbean
yellow mosaic virus (Mandal et al., 1997). However, the causal virus of
yellow mosaic disease in Bangladesh has so far not been confirmed.
The major oilseed crops grown in Bangladesh are mustard, sesame,
groundnut and linseed, while niger, soybean, sunflower, safflower and
castor are grown as minor oil crops (Biswas and Das, 2011). The major
contribution of oil comes from mustard (65%) followed by sesame
(10.71%) and groundnut. The viral disease is not a major constraint in
the production of oilseeds in Bangladesh. A mosaic disease is known in
mustard, but the associated causal virus has not yet been characterised
(Muqit and Akanda, 2007). In groundnut, mosaic, green blotch and
stunting were recorded (Khatun, 2004). Several viruses, tobacco rattle
virus (TRV), alfalfa mosaic virus (AMV), pea seed-borne mosaic virus
(PSbMV) and peanut mottle virus (PeMoV) were detected by ELISA in
groundnut samples from different places (Akanda et al., 1991a). In
soybean, mosaic, yellow mosaic, mottling, chlorosis and leaf curl were
recorded (Hossain et al., 2005). The ELISA based detection indicated
the presence of AMV, PSbMV, PeMoV and blackeye cowpea mosaic
virus (BICMV) in soybean (Akanda et al., 1991a). An unidentified virus
that causes mosaic disease in sunflower and sesame was also reported
(Hossain et al., 2005).
8. Viral diseases of fruits
A wide variety of fruit crops, citrus, jackfruit, mango, pineapple,
papaya, guava, banana, melon, watermelon, litchi, ber and hog plum
are cultivated with the annual production of 3.2 million tons from 0.6
million hectares of land. Viral diseases are a severe constraint in banana, papaya, melon and watermelon.
Banana (Musa sp.), one of the most important fruit crops in
Bangladesh, is widely grown in small, mixed gardens up to a large
commercial monoculture farming. Banana is known to be affected by
three viruses, banana bunchy top virus, banana streak virus and banana
bract mosaic virus (Sattar and Hoque, 2004), but all these viruses are
not characterised at the molecular level. Among the banana viruses,
banana bunchy top virus (BBTV) is frequently observed (Fig. 2d). In the
developing countries, the international movement of banana germplasm has increased in recent years particularly in the form of tissue
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10. Viral diseases of spices
11. Viral diseases of vegetables
Twenty-five different spices crops were grown in Bangladesh.
Among them, chilli, onion, garlic, turmeric and ginger were the most
common and have contributed as cash crops of resources poor farmers
in Bangladesh. The production of spice crops in terms of yield (ton/ha)
is very low as compared to other spices producing countries of the
world, this is because of the lack of disease-resistant varieties, especially for the viral diseases. The viral diseases are the major constraints
in spices production in Bangladesh, but for most of the diseases, the
causal agents and their vectors have not been properly documented.
Viral diseases are significant constraints wherever chilli pepper is
grown as it causes poor fruit yield and quality. Compared to the other
chilli growing countries, Bangladesh experiences a low yield in chilli
production, which is potentially due to viral disease complex prevailing
in the crop. Several viruses were reported infecting pepper worldwide,
while only CMV, PVY, TMV, chilli venal mottle virus (ChiVMV) and
chilli leaf curl virus (ChiLCuV-[Jessore]) were reported in Bangladesh
(Akanda, 1991; Akanda et al., 1991a, 1991d; Maruthi et al., 2007;
Rashid et al., 2007). The incidence of CMV in chilli pepper has been
reported up to 100% in Bangladesh (Rashid et al., 2007). The molecular
identification of CMV suggested the occurrence of sub-group IB CMV in
Bangladesh. CMV and potyviruses (PVY and ChiVMV) limit commercial
pepper production in Bangladesh. Screening for resistance was attempted in thirteen pepper lines, but none of them showed resistance to
CMV or ChiVMV (Rashid et al., 2007).
Begomoviruses are an emerging threat to chilli cultivation.
However, the causal virus species is yet to be identified. Leaf curl disease occurs in epidemic proportion (up to 100% incidence) in North
Bangladesh. Under field conditions, 40 local and exotic genotypes of
chilli were screened against leaf curl disease, and severity of leaf curl
was assessed using a 0–5 scale, where three genotypes were found field
resistant, and three other genotypes were moderately resistant. In another study, seven out of 46 genotypes were found free from leaf curl
disease, sixteen genotypes were moderately resistant, twelve genotypes
were susceptible, and four genotypes were highly susceptible to the leaf
curl disease.
Garlic (Allium sativum) is one of the most important culinary herbs
in the Indian subcontinent and widely cultivated spices crop in
Bangladesh. Viruses, especially those belonging to the genera Potyvirus,
Carlavirus, and Allexivirus are the most important viral pathogens of
garlic in Bangladesh. In Gazipur, two viruses, shallot latent virus (SLV)
and leek yellow stripe virus (LYSV) were identified in garlic based on
DAS-ELISA and DIBA (Akanda et al., 1991a). Although only two garlic
infecting viruses have been identified in Bangladesh, garlic plants were
frequently observed with a variety of symptoms eg., mosaic, leaf distortion, stunting and degenerating of cloves. It is possible that several
other viruses, onion yellow dwarf virus (OYDV), garlic common latent
virus (GarCLV) and garlic virus X are introduced through importing
new cultivars from India and other countries, where the viruses are
known to be present (Baranwal et al., 2011; Majumder and Baranwal,
2009). A systematic study for the identification and characterisation of
viruses infecting garlic in Bangladesh is important for sustainable garlic
production.
In Bangladesh, 125,101 ha land is under onion (Allium cepa) cultivation in the winter and summer seasons. The mean yield of onion in
Bangladesh is very low (4 tons/ha) compared to the world average
(17.27 tons/ha). Every year, Bangladesh imports onion from other
countries to meet its demand. The onion crop suffers from a viral disease that causes mosaic, leaf distortion and stunting. The outbreak of
such a virus disease has been observed at Taherpur of Rajshahi District
during 2010, which might be due to the infection of OYDV. Although so
far, no specific documentation of onion viruses is available in
Bangladesh.
About 16% of total cultivable land in Bangladesh is under vegetable
cultivation. Members of the Solanaceae, Cucurbitaceae, Malvaceae families are widely grown in Bangladesh as summer, winter or year-round
vegetables, which contribute 3.2% of the agricultural gross domestic
product. Viral diseases are major threats to vegetables production in
Bangladesh (Supplementary Tables 2 and 3 &4).
Several species of cucurbits, such as cucumber (Cucumis sativus),
sweet gourd/summer squash (Cucurbita moschata), bottle gourd
(Lagenaria siceraria), white gourd/wax gourd (Benincasa hispida),
pumpkin (Cucurbita maxima), bitter gourd (Momordica charantia) and
ridge gourd (Luffa acutangula) are cultivated as major vegetable crops
in Bangladesh (Rashid, 1976; Rabbani, 1984). Some of these cucurbits
are very important as they provide a year-round source of vegetables.
Various types of viral diseases affect cucurbits, but systematic studies
on these diseases and the causal viruses are lacking. Whitefly-transmitted viral diseases are emerging problems in cucurbits in Bangladesh
and other countries (Tsai et al., 2007). Severe disease symptoms like
yellowing and chlorotic spots on foliage are frequently observed in
several cucurbit crops throughout Bangladesh, but the causal agent of
those diseases have not yet been addressed.
11.1. Cucurbitaceous vegetables
Potyviruses, PRSV and WMV have been reported in ash gourd in
Bangladesh (Akanda et al., 1991a; Muqit et al., 2007). The effect of
trichome density on aphid (Aphis gossypii and Myzuz persicae) population and the incidence of viral diseases in four accessions of ash gourd
were studied in local Sylhet genotype, local round, exotic high female
and exotic CQ-10-90 (Khan et al., 2000). The numbers of aphid were
lowest on the terminal and young leaves of ash gourd compared with
mature and senescent leaves, this is due to the presence of higher trichome density in the former leaf categories. Trichome density was
found to have a significant negative influence on the number of aphids
and the occurrence of viral diseases.
The virus disease symptoms such as mosaic, vein clearing and yellowing are commonly observed in bottle gourd. The attempt to identify
the associated viruses in bottle gourd in Gazipur using antisera to CMV,
PRSV, WMV, ZYMV, CGMMV and SqMV by DAS-ELISA and DIBA revealed the presence of PRSV (Akanda et al., 1991b, 1991c). The further
study indicates the presence of other unknown filamentous viruses in
bottle gourd (Akanda et al., 1991a).
Two potyviruses (PRSV and WMV), a cucumovirus (CMV) and a
comovirus (SqMV) have been identified in cucumber based on DASELISA and DIBA (Akanda et al., 1991b; 1991c; Akhter et al., 2008; Ali
et al., 2007). In northern Bangladesh (Rajshahi district), high prevalence CMV and PRSV-W were recorded (Ali et al., 2007; Aktar et al.,
2008). Yellow mosaic disease is a serious problem of cucumber production in Bangladesh (Fig. 2e). Begomoviruses are emerging problems
in vegetables in Bangladesh due to the high prevalence of whitefly
vector. In cucumber, ToLCNDV has also been identified based on the
complete sequence of DNA-A genome (GenBank accession no.
EF450316). Pumpkin, a common vegetable is affected by PRSV alone or
with WMV and ZYMV (Masud et al., 2009). A survey was conducted in
four southern districts, Faridpur, Khulna, Gopalgong and Magura,
which showed a high incidence (up to 89.23%) of viral diseases in
pumpkin (Saifullah et al., 2003). CMV is another common viral pathogen, and about 24.0% incidence of CMV was recorded in southern
Bangladesh (Saifullah et al., 2003). Yellow vein mosaic disease is a
serious disease of pumpkin. The disease causes yellowing, stunting of
plant and reduces both the quality and yield of fruit. The genome sequence analysis of two isolates from Jessore revealed the association of
squash leaf curl China virus (Maruthi et al., 2007).
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Several tomato cultivars were released by BARI: BARI Tomato-2, BARI
tomato-4, BARI Tomato-5, BARI Tomato-6 (Chaity), BARI tomato-7
(Apurba), BARI Tomato-11 and BARI Tomato-12. Field evaluation of
these cultivars showed a high occurrence of leaf curl disease (Gupta,
2000; Rahman et al., 2006).
Tospoviruses are the emerging threat to tomato cultivation in the
Indian subcontinent including Bangladesh (Mandal et al., 2012). GBNV
causing leaf mottling and necrotic veins, short internodes, necrosis of
terminal buds and concentric rings on fruits of tomato has emerged as a
significant problem (Fig. 2 f, g). The most of the popular tomato cultivars, Sobal, Abhiruchi, Salamat, Bangobir, and BARI hybrid Tomato-5
and -6 are susceptible to this tospovirus (Farooq and Akanda, 2007a,
2007b; Akhter et al., 2012).
11.2. Malvaceous vegetables
Okra or bhendi (Abelmoschus esculentus) is an important vegetable
grown in the late summer season when very few other vegetables are
available. Yellow vein mosaic is a significant constraint in the production of okra in Bangladesh (Ahmed, 1984b). The disease is widely
spread in all the okra production regions and occurs at an epidemic
proportion (Akanda et al., 1991d). Most of the cultivars are highly
susceptible to yellow vein mosaic disease. Two okra accessions, IPSADherosh and BARI Dherosh-1 were released as resistant cultivars
against yellow vein mosaic disease (Ali, 1999; Ali et al., 2000; Rashid
et al., 2002), but none of them continued to show resistance anymore.
Bhendi yellow vein mosaic virus (BYVMV) (genus Begomovirus) was
detected in okra from Jessore, that showed very close sequence similarities to the BYVMV isolates occurring in India (Maruthi et al., 2007).
12. Viral disease in tuber crops
The important tuber crops grown in Bangladesh include potato,
sweet potato, aroid, yam, cassava and yam bean. A list of plant viruses
infecting tuber crops is presented in (Supplementary Table 5).
Potato occupies the third position in acreage after rice and wheat in
Bangladesh. Two main categories of potato cultivars are grown in
Bangladesh: indigenous cultivars and exotic high yielding cultivars. Six
viruses, PVY, PLRV, potato virus X (PVX), potato virus S (PVS), potato
virus M (PVM) and potato virus A (PVA) have been reported in
Bangladesh. Among these viruses, PLRV and PVY are two most prevalent viruses that were recorded to cause yield loss up to 78% and
35%, respectively (Hossain et al., 1989, 1993; Hossain and Ali, 1992).
The potato plant infected with PVY and PLRV was recorded to degenerate in the successive generations (Bari et al., 1998). Assessment and
production of virus-free seeds are the acute problems in seed potato
production in Bangladesh (Ali and Khan, 1990; Khan et al., 1991).
Symptoms severity due to PLRV varied with vegetative generations of
potato seed tubers (Rahman and Akanda, 2010). Eleven high yielding
exotic second vegetative generation seed potato cultivars, Baraka, Remarka, Victoria, Voyager, Felsina, Febula, Bellini, Fontane, Sinora,
Martene and Diamond, were evaluated for resistance against PVY and
PLRV, none of them was found to be resistant against these viruses and
the infection of these viruses increased in the second year of the experiment compared to the first year (Rahman and Akanda, 2009). In
2012, the genome sequence analysis of PVY isolates from Bangladesh
revealed the presence of NTN strain (necrosis strain) (GenBank accession no JX088119). PVX was detected as a mixed infection with PVY in
2012, and coat protein gene sequence revealed that the PVX isolate was
closely related to the European isolates (GenBank accession no. JX
273242). These are the first sequence data of potato viruses in Bangladesh, but more sequence information is needed to study population
diversity of RNA viruses infecting potato in Bangladesh.
Bangladesh Government imports E-class seed potato from Holland
every year, and it is said to be virus-free. Bangladesh Agricultural
Development Corporation (BADC) multiplies them to produce foundation and certified seeds, which are distributed to farmers for cultivation
purpose. BADC also produces virus-free seed potato by using sprout and
stem cutting method from E-class imported potato. The least incidence
of PVY and PLRV was recorded for the seed tubers developed from
sprout cutting and stem cutting method, but the highest incidence of
these viruses was recorded in the seed tubers developed from conventional farmer's practices (Rahman and Akanda, 2009). To manage potato virus, farmers frequently spray insecticides to control vectors.
Spraying of insecticide against insect vectors did not show significant
influence on plant growth and tuber yield (Rahman and Akanda, 2010).
However, indiscriminate use of chemicals has led to increasing resistance in insects.
Five plant viruses, sweet potato feathery mottle virus (SPFMV),
sweet potato mild mottle virus (SPMMV), sweet potato latent virus
(SPLV), sweet potato chlorotic fleck virus (SPCFV), sweet potato leaf
curl virus (SPLCV) have been suspected to infect sweet potato in
11.3. Solanaceous vegetables
Brinjal or egg-plant (Solanum melongena) is one of most commonly
cultivated crops in Bangladesh. A large number of brinjal cultivars is
grown in Bangladesh, which shows a wide range of variations in yield
performance and disease reaction. Mosaic, vein clearing and yellowing
symptoms are commonly observed in brinjal. PVY and TMV were detected in brinjal based on serological methods (Akanda et al., 1991a).
However, the virus etiology with most of the diseases are not well established. Recently, CMV has been reported to affect 90% of the brinjal
plants that showed mosaic and mottling symptoms in Barishal district of
Bangladesh (Bagewadi et al., 2015).
Sweet pepper (Capsicum sp.), a high-value vegetable crop, is gaining
popularity in the supermarkets in Bangladesh. Sweet pepper is grown in
the winter season (October–March). Viral diseases are the main constraint of capsicum production in Bangladesh. The crop has been observed to suffer from a different virus-like disease symptoms, mosaic,
mottling, curling and yellowing. Tentative identification of TMV, CMV,
PVY and begomovirus with these diseases was reported (Akanda eat al.,
1991a, 1991c; Rashid et al., 2007).
Tomato (Solanum lycopersicum) is cultivated in both winter and
summer seasons in Bangladesh. Several viral diseases were recorded in
tomato (Supplementary Table 3), and many of them are of serious
problems. Leaf curl is the most important disease of tomato, which is
prevalent throughout the country and causes serious crop loss (Akanda
et al., 1991a, Green et al., 2001, Maruthi et al., 2005a; 2005b, 2005c).
During the last two decades, leaf curl disease has emerged as a devastating disease causing economic loss up to 100% in many tropical and
sub-tropical regions including Bangladesh (Akanda, 1994, Varma and
Malathi, 2003). Different types of symptoms are developed on tomato
plants due to begomovirus infection. The disease symptoms range from
mild leaf curl to yellow leaf curl and severe curling and stunting. The
infection at an early stage of plant growth resulted in severe curling,
stunting and complete loss of yield (Maruthi et al., 2005a).
A few benchmark research approaches such as PCR based detection,
sequencing and management of the disease with resistant/tolerant
cultivars and vector control using insecticides have been conducted on
begomoviruses that infect tomato in Bangladesh (Green et al., 2001;
Maruthi et al., 2005a, 2005b; 2005c, 2007; Muqit, 2006). So far, four
begomoviruses species, Tomato leaf curl Bangladesh virus, Tomato leaf
curl Joydebpur virus (ToLCJV), ToLCNDV, Tomato leaf curl Karnataka
virus (ToLCKV) have been recorded to infect tomato in Bangladesh
(Green et al., 2001; Maruthi et al., 2005a, 2005b; 2005c, 2007). The
high genetic diversity of tomato-infecting begomoviruses is expected,
which poses a challenge for the management of tomato leaf curl disease
in Bangladesh (Maruthi et al., 2005a). Four tomato cultivars, TLB111,
TLB131, TLB133 and TLB182, which are known to be resistant/tolerant
to southern India, were evaluated in Bangladesh. These cultivars were
tolerant to leaf curl as low incidence of disease (6–45%) was observed
compared to the local cultivars (68–100%) (Maruthi et al., 2005a).
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16. Virus free planting materials
Bangladesh (Supplementary Table 5). Among the viruses, SPFMV is the
major one (Hossain et al., 1999). Under the field conditions, 49 genotypes of sweet potato were tested for the incidence of different viral
diseases. Three viral diseases, feathery mottle, mild mottle and leaf curl
prevailed with the disease incidence of 100%, 50% and 60%, respectively. None of the genotypes has been found free from SPFMV infection
(Hossain et al., 2004).
Tissue culture techniques were successfully employed for the eradication of virus diseases of potato. PLRV, PVY and PVX were reported
to be eradicated through thermotherapy and meristem culture (Hossain
et al., 1993). Utilization of true potato seed could produce virus-free
potato and increase the yield in potato (Akhtar et al., 2001).
17. Resistant cultivars
13. Viral disease management
Lack of resistant cultivars is a major limiting input for the management of virus diseases, however, limited numbers of virus resistant/
tolerant cultivars were released for a few crops by the major crop research institutions in Bangladesh. Five cultivars of mungbean viz. BARI
Mung-5, BARI Mung-6, BINA Mung-5, BU Mung-1 and -2 were reported
to be tolerant to yellow mosaic disease (Afzal et al., 2004). Okra cultivars, BARI Dherosh-1 and IPSA Okra-1 were released as yellow vein
mosaic resistant okra (Hossain, 2000; Ali, 1999; Ali et al., 2000). Four
cultivars of black gram, BARI Mash-1, -2, -3, and BINA Mash-1 were
released as yellow mosaic tolerant cultivars (Afzal et al., 1999). Six
cultivars of potato, Heera, Dheera, Chamak, Cardinal, Diamant and
Granola were reported to be tolerant to virus diseases (Hossain et al.,
2002).
Management plant virus diseases is a difficult task as no direct
chemical solutions are available. Molecular diagnosis and transgenic
resistance have been applied for the management of plant viruses in the
developed nations, but the modern approaches are yet to be utilized in
Bangladesh. However, traditional control strategies have been employed in the managing plant virus diseases in Bangladesh.
14. Cultural management
Alteration of planting time was shown beneficial to reduce virus
infection in okra, mungbean and tomato. The substantial reduction of
okra yellow vein mosaic disease was observed when okra was sown in
February–March as compared to May–October planting. If okra was
sown in January–March, April–September and October–December, it
took 111, 28 and 47 days, respectively for initiation of disease (Muqit
et al., 1999). The incidence of yellow mosaic disease of mungbean was
reduced when the crop was planted in the 3rd week of January. The
disease incidence was further reduced in the early sown crop when four
sprays of insecticide were applied. Tomato leaf curl is a year-round
problem, however, avoidance of active phase of crop growth during the
period of abundance of vector whitefly helps reduce the disease pressure. For example, early summer planting (February) of tomato resulted
in lower incidence of leaf curl disease compared to late summer (April)
planting (Rahman et al., 2006). Leaf curl disease was reduced
by > 40% when the tomato was planted in the 1st week of December as
compared to the first week of November (Muqit, 2006).
There trap crops, mungbean and marigold were planted in the chilli
field in order to minimize the incidence of chilli leaf curl disease.
Intercropping okra with amaranthus reduced the incidence of okra
yellow vein mosaic disease (Aminullah, 2003).
18. Integrated management
Combining multiple management tactics was useful in managing
viral disease. Integration of netting of seed-bed, polyethylene mulch,
trap crop together with three sprays of imidachloprid, azadirachtin
(neem based insecticide) and soybean oil at 10-day interval could effectively reduce tomato leaf curl (Muqit et al., 2006). Early sowing,
intercropping with amaranthus, polyethylene strip hanging together
with foliar spray of systemic insecticides reduced the incidence of
yellow vein mosaic disease in okra that contributed an increase of
∼40% fruit yield (Sanker, 2004).
19. Concluding remarks
Plant viral diseases are severe threats to sustainable crop production
in Bangladesh. Of the several virus diseases recorded in many crops,
some of them are endemic and some are epidemic in nature. Vegetables
and pulse are worst affected by viruses. Whitefly and thrips-transmitted
viruses are of high economic significance. Many recurring epidemics of
leaf curl disease in tomato and chilli, yellow vein mosaic in okra,
ringspot disease in papaya and yellow mosaic in pulses were witnessed
(Alam, 1995; Gupta, 2000; Maruthi et al., 2007; Akanda, 1991; Akhter
and Akanda, 2008; Ahmed et al., 1981; Ahmed, 1984a, 1984b; Islam
et al., 2012). Assessment of yield loss and the economic impact of the
major virus diseases is necessary. The viral genera, Cucumovirus, Begomovirus, Potyvirus and Tospovirus are economically important in Bangladesh (Mandal et al., 2012; Akhter et al., 2012). Some of the viruses
are tentatively identified based on serology (Akanda et al., 1991a,
1991d). The complete genome sequence information of a few begomoviruses and partial genome sequence of a few other viruses eg., CMV,
PRSV, PVY and PVX have been generated during the last eight years
(Maruthi et al., 2005a, 2005c; Akhter et al., 2013). Genome sequence
information of the viruses affecting major crops is required to establish
the identity of the prevailing viruses and further the genomic information will serve the basis of developing molecular diagnostic reagents and transgenic resistance.
Traditionally, for the control of virus diseases, farmers adopt a
large-scale application of chemical pesticides without the knowledge of
the cause of diseases either by fungus, bacteria or virus
(Schreinemachers et al., 2015). As a result, indiscriminate use of insecticides directly affects the economics of cultivation as well as creates
an ecological and environmental imbalance. The resistant cultivar is the
15. Vector control
Insecticides are used widely for controlling insects and viral diseases. Spraying of systemic insecticides at the 15-day interval for the
control of aphid vector was suggested for the management of mosaic
and leaf roll diseases of potato (Hossain, 2005). Systemic insecticide
spray at 15-day intervals starting from 20 days after germination is
recommended for the management of yellow vein mosaic of okra. Admire (imidachloprid), Bayer Crop Science Limited was effective in reducing the incidence of tomato leaf curl through controlling the vector
whitefly in the early season (Muqit, 2006). Rouging and spraying of
insecticides were observed more effective for the management of
mungbean and black gram yellow mosaic (Afzal et al., 2004, Afzal
et al., 1999) and bunchy top of banana (Huq and Hossain, 2001). Oil
emulsions were used to control aphid and whitefly vectors. In potato,
the application of Finavestan TS (emulsion oil) Total Fluides, France,
resulted in a reduced level of leaf roll and mosaic diseases. Soybean oil
emulsion was found effective in reducing the incidence of tomato leaf
curl under open field conditions (Aktar et al., 2008).
Not many studies are available in Bangladesh for the effective
control of virus and vector using botanical extracts. However, one study
showed some satisfactory results in managing virus diseases of tomato
by using allamanda leaf extract (Mostatfa, 2004).
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most important input in virus disease management (Schreinemachers
et al., 2015). The precise identification of resistant sources using molecular diagnostics is essential in developing breeding for virus resistant
cultivars (Nicaise, 2014). Developing virus resistant cultivars is a longterm and intricate process. Alternatively, import of resistant cultivars
developed through classical breeding or transgenic approach in the
other countries may offer a quick solution, but it needs a prior evaluation before introduction. Capacity building in the area of plant virology specifically genomics, molecular diagnosis, genetics of resistance,
breeding for resistance, vector biology and disease epidemiology is
required for addressing the viral disease problems in Bangladesh agriculture. Further, there is a trans-boundary circulation of viruses
through insect vectors and planting materials among the neighbouring
countries. Pathogen diagnostic network laboratories with the special
emphasis on virus diagnosis network among the adjoining countries
under the international organization like Bay of Bengal Initiative for
Multi-Sectorial Technical and Economic Cooperation and SAARC
Agriculture Centre will be highly benefiting the production crops in
Bangladesh and thereby the trade in agriculture among the South and
South East Asian countries.
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Acknowledgement
The first author is thankful to The World Academy of Sciences for
the fellowship to work at the Advanced Centre for Plant Virology,
Division of Plant Pathology, Indian Agricultural Research Institute, New
Delhi-110012, India. The first author also acknowledges to Ministry of
Education, Culture, Sports, Science and Technology, Japan (MEXT) for
the fellowship.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.cropro.2018.11.023.
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