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Chilli leaf curl virus disease: a serious threat for chilli cultivation

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Journal of Plant Diseases and Protection
https://doi.org/10.1007/s41348-018-0146-8 (0123456789().,-volV)(0123456789().,-volV)

REVIEW

Chilli leaf curl virus disease: a serious threat for chilli cultivation
Hament Thakur1 • Salesh Kumar Jindal1 • Abhishek Sharma1 • Major Singh Dhaliwal1

Received: 31 July 2017 / Accepted: 12 January 2018

Ó Deutsche Phytomedizinische Gesellschaft 2018

Abstract
Chilli pepper or hot pepper (Capsicum annuum L.,) is an important spice and vegetable crop of family Solanaceae. Chilli is
susceptible to various pathogens involving viruses, which cause heavy production losses. So far 65 viruses have been
reported throughout the world including begomoviruses causing chilli leaf curl virus disease (ChiLCVD). ChiLCVD is the
most destructive virus disease in terms of incidence and yield loss. The disease can be identified by typical upward leaf
curling, crinkling, puckering and reduction in leaf area along with stunting of whole plants. It is transmitted by the whitefly
Bemisia tabaci in persistent manner. Conventional plant breeding techniques remain the major antiviral strategy so far for
the development of resistant chilli varieties. Recently, the concern about viral DNA methylation, activation of gene
silencing machinery and ubiquitination-mediated defence against begomoviruses has been reported. Although a number of
insecticides had been effectively used to manage this pest in the past, it is able to develop resistance very rapidly. This
review provides an overview of ChiLCVD, virus vector relationship, its genome organization, replication, resistant sources,
present status of its spread in different regions of India and strategies employed for controlling it.

Keywords Chilli
Leaf curl virus
Threat

Introduction 1960). It is considered as a facultative cross-pollinating

Chilli pepper or hot pepper (Capsicum annuum L.,) is an
important spice and vegetable crop of family Solanaceae.
Chilli is a native plant of South America and Portuguese
were the first to acquaint it to India from Brazil towards the
end of fifteenth century. India is considered to be the
secondary centre of diversity for chilli, especially of C.
annuum, the most important cultivated species (Dhaliwal
et al. 2014). C. annuum having pungent (chilli syn. hot
pepper) and non-pungent fruits (sweet pepper syn. cap-
sicum, bell pepper) is the most widely cultivated species in
India, among the five cultivated species of the genus
Capsicum. The cultivation of C. frutescens, C. chinense
and C. baccatum is confined to homestead gardening in
different regions (Reddy et al. 2014). Capsicum species are
usually self-compatible (Onus and Pickersgill 2004), and
C. annuum is a partially self-pollinating crop (Allard
& Hament Thakur
hemantt114@gmail.com
1
Department of Vegetable Science, Punjab Agricultural
University, Ludhiana, Punjab 141004, India
species because out-crossing in the field generally ranges
from 7 to 90% (Tanksley 1984; Singh et al. 1994). India is
the largest producer, consumer and exporter of chillies in
the world. According to an estimate for 2014–2015, in
India, green chillies were cultivated on 0.18 million hec-
tares with a total production of 1.9 million tonnes (NHB
2014–2015). India is at the top in terms of international
trade by sharing about 40% of the total world production
and exports 17% of its total production. The largest
importer of Indian chilli is Malaysia (* 30%), followed by
other traditional importers like Bangladesh (* 20%), Sri
Lanka (15%), the USA (9%) and the UAE (8%) (FAO
2014). The export is composed of chilli powder, dried
chillies, pickled chillies and chilli oleoresin.
Chilli is susceptible to various pathogens including
viruses, which can cause heavy production losses. So far 65
viruses have been reported, including begomoviruses
causing chilli leaf curl virus disease (ChiLCVD) infecting
chilli throughout the world (Nigam et al. 2015). ChiLCVD
is the most destructive virus in terms of incidence and yield
loss. In severe cases, 100 per cent losses of marketable fruit
have been reported (Senanayake et al. 2007; Kumar et al.
2011a, b; Senanayake et al. 2012). The typical symptoms

123

consisting of leaf curling, rolling and puckering; blistering
of interveinous areas, thickening and swelling of the veins,
shortening of internodes and petioles, crowding of leaves
and stunting of the whole plant. Till date, genome sequence
of four begomoviruses infecting chilli, viz, Chilli leaf curl
virus (ChiLCV), Tomato leaf curl New Delhi virus
(ToLCNDV), Tomato leaf curl Joydebpur virus (ToLCJV)
and Chilli leaf curl Palampur virus (ChiLCPV) (Khan et al.
2006; Shih et al. 2006; Kumar et al. 2011a, b), has been
characterized in India. Evasive measures, such as pesticide
sprays to control vectors, removal of diseased plants and
agronomic interventions, have been tried without much
success. Exploitation of host plant resistance is effective,
economical, ecologically safe and durable approach to
disease management, especially the ones caused by viruses.
History and distribution
In tropical and subtropical parts of India, ChiLCVD is a
major constraint to chilli (Dhanraj et al. 1968; Chattopad-
hyay et al. 2008). It has been reported by several investi-
gators from India and abroad. However, the viral nature of
the disease has not been proved experimentally by them.
Typical leaf curl symptoms were observed on 15–25% of
the chilli plants under field conditions, and they considered
it to be caused by the Tobacco leaf curl virus (TLCV)
(Pruthi and Samuel 1942). However, no transmission tests
were conducted nor any experimental evidence was given.
Earlier, chilli leaf curl disease was considered to be caused
by mites or thrips (Scirtothrips dorsalis). The natural
occurrence of chilli leaf curl was first reported to be caused
by TLCV (Mishra et al. 1963). The occurrence of another
type of leaf curl symptoms which produces leaf enations in
chilli leaves was also reported (Dhanraj et al. 1968). The
evidence so far available has indicated that the leaf curl
complex in chilli could be due to mites (Polyphagotar-
sonemus latus), thrips (Scirtothrips dorsalis) and a virus
transmitted by whitefly, Bemisia tabaci (Varma 1962). At
that time, begomoviruses were not known, but since 2003,
several begomovirus species were reported to cause leaf
curl disease of chilli in India (Senanayake et al. 2007;
Chattopadhyay et al. 2008; Senanayake et al. 2012). So far
in India and Pakistan, at least four begomovirus species are
known to be consociated with leaf curl disease:
ToLCNDV, ChiLCV, Cotton leaf curl Multan virus
(CLCuMV) and ToLCJV (Hussain et al. 2003; Shih et al.
2003; Hussain et al. 2004; Khan et al. 2006). The geo-
graphical distribution of the begomoviruses is analogous to
occurrence of whitefly in the world (Brown et al. 1995). It
covers almost entire equatorial regions of the Americas,
Africa, Europe, Asia and Australia. It has also been
reported from other countries, like the USA (Stenger et al.
123
Journal of Plant Diseases and Protection
1990), Nigeria (Alegbejo 1999) and Pakistan, Bangladesh
and Indonesia (Fauquet and Stanley 2003).
Classification and structure of pathogen
The viruses belonging to the family Geminiviridae are
among the major limitations that cause huge losses to
vegetable crop production. Geminiviruses are controver-
sially one of the most baleful plant viruses in the entire
world and cause a vast threat to global food security. They
are ample in tropical and subtropical environments, where
insects that spread these viruses are plentiful. The aetiology
of chilli leaf curl disease found in tropical and subtropical
areas had proved to be elusive till 1977 when circular
single-stranded DNA (ssDNA) containing geminiviruses
were reported (Harrison et al. 1977). On the basis of the
geminate morphology of the virus particles and circular
ssDNA as their genomic component, geminiviruses were
perceived as a separate group by International Committee
on Taxonomy of Viruses (ICTV) in 1978 (Rishi 2004).
The genus begomovirus (Geminiviridae) with 288 spe-
cies is the largest genus of all viral taxonomy currently
recognized by the ICTV (Brown et al. 2015). ICTV raised
geminivirus group to the status of family Geminiviridae in
its XI International Congress of Virology held in 1999 in
Sydney. The standards for demarcation of species of the
members of family Geminiviridae were revised by ICTV
and on the basis of genome organization, distinguished
insect vector and host range instead of three, there are four
genera distinguished (Mastrevirus, Curtovirus, Bego-
movirus and Topocuvirus) (Fauquet et al. 2003). Recently
on the basis of genome organization, nucleotide sequence
similarities and biological properties, the geminiviruses are
now classified into nine genera—Becurtovirus, Bego-
movirus, Capulavirus, Eragrovirus, Grablovirus, Mastre-
virus, Curtovirus, Topocuvirus and Turncurtovirus (Zerbini
et al. 2017). Begomoviruses are described by twin icosa-
hedral particles, approximately 18 9 30 nm in size (Stan-
ley et al. 2005). The genomes of begomoviruses commonly
contain one or two circular, single-stranded DNA compo-
nents of 2.5–3 kb in size, known as DNA A and DNA B
(Mayo and Pringle 1998; Hanley-Bowdoin et al. 1999)
The two components of bipartite begomoviruses share a
highly conserved common region (CR), approximately 200
nucleotides (nt) in length which consists of reiterative
sequence-specific replicase (Rep) binding motifs called
iterons and a nonanucleotide stem-loop structure (TAA-
TATTAC), required for replication of the viral genome
(Moffat 1997; Fauquet and Stanley 2003). Most of the
monopartite begomoviruses are consociated with a satellite
molecule of approximately 1.4 kb, known as the
betasatellite, which is necessary for symptom appearance
Journal of Plant Diseases and Protection
but depends fully upon the helper virus for its replication,
encapsidation and cell-to-cell movement (Mansoor et al.
2003; Briddon and Stanley 2006). For the first time, it was
substantiated that chilli leaf curl disease (ChiLCD) was
caused by a complex consisting of the monopartite,
ChiLCV and a betasatellite, Tomato leaf curl Bangladesh
betasatellite (ToLCBDB) (Chattopadhyay et al. 2008).
Later, both bipartite and monopartite begomovirus with
alpha and beta satellites have been reported to be associ-
ated with ChiLCVD (Hussain et al. 2004; George et al.
2014).
Virus replication
Begomoviruses associated with ChiLCVD, like all other
members of Geminiviridae, replicates via using a combi-
nation of a rolling circle mechanism and recombination-
mediated replication, which takes place in the nuclei of
infected cells (Gutierrez 1999; Jeske et al. 2001). There is a
resemblance in the mechanism by which mammalian DNA
tumour viruses activate the host genes required for DNA
replication and the ssDNA phages such as / X174 repli-
cates. This type of replication gives rise to multiple copies
of long continuous double-stranded (ds) DNA intermedi-
ate, the replicative form (RF), which later changes into
genome-sized circular DNA fragments. The proteins
required for replication initiation and for recruitment of the
host replication machinery are formed from the transcrip-
tion of dsDNA intermediates. The virus encodes two pro-
teins which are imperative for effective virus replication,
i.e. C1 (Rep.) and C3. C1 protein serves as the launching
factor and occurs midway the origin detection and DNA
cleavage/ligation to begin and to end up the rolling circle
replication process. The C3 protein alters the C1 activity
and helps in enrolment of host replication enzymes which
thus eases the accretion of high levels of viral DNA. Both
replication and transcription of the virus occur in the
nucleus of the plant cell, so the import of the viral DNA
and/or virions into and out of the host plant cell nucleus is
necessary for efficient completion of the virus’s life cycle.
Therefore, in and out movement of the viral genome in the
nucleus, as well as from cell to cell and in the whole plant,
is very important for viral infection.
Symptoms and disease incidence
The expressions of the disease caused by the manifestation
of the physiological reaction of the plant due to the harmful
activity of the pathogen are called symptoms. The symp-
toms of ChiLCVD consist of abaxial and adaxial curling of
the leaves accompanied by puckering and blistering of
interveinous areas and thickening and swelling of the veins.
In advanced stages of the disease, axillary buds were
stimulated to produce clusters of leaves which were
reduced in size. The whole plant assumed a bushy
appearance and stunted growth. Fewer flowers and fruits
were developed on the diseased plants, and those that were
formed were much reduced in size and curled at the styler
end (Mishra et al. 1963). Two distinct types of symptoms
were observed during a survey of C. annuum at Indian
Agricultural Research Institute (Dhanraj et al. 1968).
Symptoms in the first type were similar to those earlier
reported (Mishra et al. 1963). In another type of symptoms,
the affected plants became erect and bushy and the leaves
were dark green. The leaf tips were curled downwards; the
shape of the leaves became oval to round with no upward
rolling of the edges as seen in the first type, but accom-
panied by severe puckering and leatheriness of the leaves.
On closer examination, it was observed that there was
pronounced vein thickening and leafy outgrowths or ena-
tions on the undersurface of the leaves. The diseased plants
developed fewer flowers and fruits. ‘Churda Murda’ or
malformation disease in chilli was identified (chilli leaf
curl disease) in Vidarbha (Maharashtra, India) and visual-
ized three types of symptoms, i.e. upward curling and
crinkling, downward curling and mottling, crinkling and
puckering (Moghe 1977). Upward curling, puckering and
reduced size of leaves were also observed (Senanayake
et al. 2007). Typical upward leaf curling, crinkling, puck-
ering and reduction in leaf area along with stunting of
whole plants were observed (Kumar et al. 2012).
A leaf curl disease incidence to the extent of 40–55% on
chilli varieties, viz, IC 3471, IC 3432, IC 2345, IC 3412
and NP, was observed (Mishra et al. 1963). Severely
affected plants did not produce fruits and remain stunted. A
very high disease incidence (up to 100% of plants during
December 2004) in farmer’s fields in Narwa and Tinwari
villages at Jodhpur District Rajasthan was also observed
(Senanayake et al. 2007). A disease incidence up to 100%
during December 2008 in Vellanad region of Kerala was
reported. Severe upward curling, stunted plant growth, leaf
thickening and vein clearing were observed at Jodhpur
(Rajasthan) (Senanayake et al. 2012). The severely affected
plants were stunted bearing hardly any fruits. The inci-
dence of the disease varied from field to field and village to
village (14–100%). The incidence was greater in Tinwari
where 100% of the plants of chilli variety Haripur Raipur
showed severe leaf curl, whereas, at Narwan, the incidence
of the disease in the same cultivar varied from 14 to 44%.
A survey was carried out in major pepper growing areas in
Punjab, and a maximum leaf curl incidence was observed
in Ludhiana (79.4%) followed by Tarn Taran (77%),
Sangrur (72.2%), Patiala (68.6%) and Ferozepur (57.5%)
(Kaur et al. 2016).
123

Vector and host range
Association between plant viruses and their insect vectors
is very much complicated. Some plant viruses are carried
in the insect’s feeding apparatus and can be acquired and
inoculated within seconds or minutes (non-persistent
transmission). Other viruses circulate in the body and can
be transmitted only after the incubation period of hours to
days (persistent transmission). ChiLCVD causing by
begomoviruses is transmitted by whitefly B. tabaci in a
persistent manner. Whiteflies are small piercing and
sucking insects of the family Aleyrodidae, order Hemi-
ptera, which have been consociated with agriculture and
with the transmission of plant viruses for many years
(Czosnek et al. 2002). Whitefly B. tabaci was first descri-
bed in Greece in 1889 as a pest of tobacco known as
tobacco whitefly (Aleyrodes tabaci) (Gennadius 1889). In
1897, whitefly was known as sweet potato whitefly (B.
inconspicua) as it was first reported on sweet potato in the
New World in the USA (Brown et al. 1995). Further
extension of its geographical range has occurred to include
temperate climate areas; the species is now globally
assorted and found on all continents except Antarctica
(Martin et al. 2000). It is a polyphagous pest and is noted
on more than 600 plant species spreading more than 60
plant viruses (Rishi 2004).
The non-viral aetiology of leaf curl disease complex was
experimentally proved, and it was concluded that it was the
result of damage caused by thrips (upward curl) and mites
(downward curl) (Amin 1979). On the basis of host range
(C. annuum, C. frutescens, C. microcarpum, Solanum
lycopersicum and Nicotiana tabacum) and transmission, it
was reported that the ChiLCVD has been caused by the
agent of tobacco leaf curl (Muniyappa and Veeresh 1984).
Whitefly was able to transmit ChiLCV from field samples
to 50–100% of chilli test plants, which produced typical
disease symptoms (Senanayake et al. 2007). ChiLCV was
also reported to infect species like Petunia hybrida,
Amaranthus spp, Mentha spicata and Mirabilis jalapa (Al-
Shihi et al. 2014; George et al. 2014; Saeed et al. 2014;
Nehra and Gaur 2015; Jaidi et al. 2017). In an epidemic of
chilli leaf curl disease at Jodhpur (Rajasthan), it was con-
cluded that several isolates were effectually transmitted by
whitefly, all of which produced severe leaf curl symptoms
in chilli (Senanayake et al. 2012). A single whitefly was
able to transmit the virus, and eight or more whiteflies per
plant resulted in 100% transmission. The minimum
acquisition access period (AAP) and inoculation access
period (IAP) were 180 and 60 min, respectively. The virus
was only able to infect five species, viz, C. annuum, Carica
papaya, S. lycopersicum, N. tabacum and N. benthamiana,
out of the 25 species tested from various families, viz,
123
Journal of Plant Diseases and Protection
Asteraceae, Caricaceae, Cucurbitaceae, Euphorbiaceae,
Leguminosae, Malvaceae and Solanaceae (Senanayake
et al. 2012). Infection of ChiLCV and Tomato leaf curl
betasatellite on watermelon was reported first time by
Shahid and Al-Sadi (2017) at Oman.
Role of betasatellites in symptom
development
A large number of monopartite begomoviruses are linked
with a newly recognized class of ssDNA satellites termed
as betasatellites. Satellites are the viruses or nucleic acids
that depend upon a helper virus for their replication, but
lack extensive nucleotide sequence homology to the helper
virus and are not essential for its multiplication (Mayo
et al. 2005). The size of betasatellite molecules is
approximately 1350 bp which is nearly half the size of
helper begomoviruses (Briddon et al. 2003). Betasatellites
have a huge role in inducing symptoms, determination of
host range and overcoming host defences (Briddon and
Stanley 2006). The symptoms induced by the helper viru-
ses are affected by the presence of satellite RNAs. Satellite
RNAs can have an impressive effect on the symptom
development, which varies from symptom amelioration to
an increase in symptom severity (Roossinck et al. 1992). In
a study, the authors suggested that the symptoms induced
by the virus were enhanced in the presence of the
betasatellite, even though viral DNA levels in host plants
were not affected (Khan et al. 2013), whereas high levels of
viral DNA were detected from chilli plants which were
inoculated with begomoviruses and cognate betasatellites
(Kumar et al. 2015). Plants inoculated with betasatellites
may also show an increase in helper viral DNA A and
DNA B levels. It was reported that the DNA B and
betasatellites acted contrary to each other, such that the
presence of betasatellites leads to 16 times higher amount
of DNA B, while accumulation of betasatellites, Cotton
leaf curl Multan betasatellite (CLCuMuB) and Luffa leaf
distortion betasatellite (LuLDB), was reduced by 60% in
the presence of DNA B (Jyothsna et al. 2013). The viral
clone was only able to produce typical leaf curling and
stunting symptoms when the viral clone was inoculated
with the betasatellite (Kumar et al. 2011a, b). Symptom
enhancement due to betasatellites is not restricted to
monopartite begomoviruses; the interaction of bipartite
begomovirus and betasatellite is another example of rapid
changes in begomovirus complexes (Akhter et al. 2014).
The infectivity of a bipartite begomovirus causing ChiLCD
in chillies was first experimentally verified from Pakistan
(Shafiq et al. 2010). A new begomovirus species ChiLCBV
(Chilli leaf curl Bijnour virus) was identified infecting
chilli in natural conditions. When dimers of DNA A and
Journal of Plant Diseases and Protection
DNA b were inoculated into chilli plant, it showed slight
curling and mosaic development in leaves (Kumar et al.
2016). Pathogenicity in ChiLCBV is determined by bC1 of
chilli leaf curl betasatellite. Because the expression of bC1
of ChiLCBV from Potato virus X (PVX) vector exhibit
phenotype typical of cotton leaf curl and therefore ChiLCB
may contribute to the disease symptoms (Tahir and Man-
soor 2011). When Chilli leaf curl Gonda virus (ChiLCGV)
and Tomato leaf curl Bangladesh betasatellite (ToLCBDB)
complexes were agroinoculated in plants, it induced severe
leaf curl symptoms in N. benthamiana (Khan and Khan
2017).
Management of chilli leaf curl virus disease
Resistance breeding
The choice of a breeding method to improve a particular
trait depends upon the type of gene action and its inheri-
tance (monogenic, oligogenic and polygenic). To breed for
begomovirus resistance, major steps involved are the col-
lection of germplasm including wild sources, evaluating
the genetic stocks under natural conditions at hot spots
having ample virus inoculum and vector population with a
conducive environment, identifying the putative resistant
material, further confirmation by artificial inoculation
techniques and transferring resistance by a suitable breed-
ing method. The main methods used in chilli breeding are
mass selection, pedigree method, single-seed descent,
backcross method, recurrent selection and hybridization
(reviewed by Padilha and Barbieri 2016). Out of the above
written methods, backcross method is most promising for
incorporating disease resistance gene(s) in a genotype.
Genetics of resistance to chilli leaf curl disease
For sustainable agriculture, disease resistant plants are one
of the main prerequisites. Genetic basis of resistance needs
to be investigated in great detail in order to understand and
rationally use the naturally occurring disease resistance.
The two genetic mechanisms for disease resistance are
monogenic (qualitative) resistance and polygenic (quanti-
tative) resistance. The former one is based on single gene,
whereas latter, i.e. polygenic resistance, depends on two or
more genes (Keller et al. 2000). In monogenic inheritance,
genes are not active against all the races of the pathogen
and confer complete resistance, i.e. they show a genetic
interaction with genes from the pathogen. Quantitative
resistance slows down the disease development by
increasing latency period and other parameters related to
the epidemic and does not express any obvious genetic
interaction with the pathogen. Monogenic resistances are
easy to work with but are constantly not perpetual.
Accordingly, quantitative resistance is favoured. Genetic
analysis of virus resistance against chilli mosaic and leaf
curl viruses in Punjab during 1989–1990 indicated that
resistance was controlled by monogenic recessive genes
(Bal et al. 1995). While studying the reaction of Pepper
leaf curl virus (PepLCV) resistance in six fields resistant
and three susceptible genotypes, it was reported that
resistance in the Punjab Lal was recessive as F1 plants were
found to be susceptible under field condition as well as
artificially challenged condition (Kumar et al. 2009). The
resistant germplasm against ChiLCV-VNS (Varanasi iso-
late) strain with some minor genes was located, and
markers significantly linked to ChiLCV-VNS resistance
were found; also the resistance was governed by major
recessive genes (Rai et al. 2010). Significant levels of all
types of gene actions (additive, dominance and epistasis)
for yield and virus resistance were revealed in inter-specific
crosses of chilli (C. annuum L. and C. frutescens L.)
(Anandhi and Khader 2011). In an inheritance study of
resistance to PepLCV in a partially compatible inter-
specific cross (PBC-535 9 Bhut Jolokia), monogenic
recessive nature of PepLCV was reported (Rai et al. 2014).
Resistance sources to chilli leaf curl virus disease
Virus diseases are commonly seen in agriculture crops and
have a major impact on their cultivation. A stirring quality
of research has been done in order to find resistant culti-
vars, genotypes and resistant genes to the virus disease in
pepper crop. For the control of viruses, host plant resis-
tance is mostly preferred because it leads to complete and
environmental safer protection from the viruses and also,
the disease is partially managed by controlling the vectors
with pesticides (Kumar et al. 2009). Out of the five culti-
vated species of chilli, C. frutescens shows resistance to
ChiLCVD (Anandhi and Khader 2011). Screening for
resistance started in the late 1960s although most screen-
ings took place under field conditions, assessing disease
incidence and disease severity (Sharma and Singh 1985;
Tewari and Viswanath 1988). Multiple virus-resistant
sources, viz, Perennial, BG-1, Lorai and Punjab Lal, were
developed at Punjab Agricultural University, Ludhiana (P.
A. U, Ludhiana) (Thakur et al. 1987). Recently, a hybrid
CH-27 has been developed at P. A. U, Ludhiana which was
found to be highly resistant to ChiLCVD (Dhaliwal et al.
2015). Pant-C1 and Pant-C2 were reported with lower leaf
curl incidence, but Pant-C1 is better than Pant-C2 in which
disease incidence is almost negligible (Mathai et al. 1977).
Seven varieties, viz, EC. 4020, EC.7299, EC.7338,
EC.6589, EC.9293, Puri Red and Puri Orange, were free of
any infection against leaf curl virus (Singh and Thakur
1977). Three symptom-less resistant sources, viz, GKC-29,
123
 Journal of Plant Diseases and Protection

BS-35 and EC-497636, showed no symptoms after chal-
lenged by grafting and alternate grafting and were also
confirmed by using PCR (Kumar et al. 2006). Six geno-
types of C. annuum, viz., Punjab Lal, CM-334, CV-2, CV-
1, Kalyanpur Chanchal, VR-339, showed the highly resis-
tant reaction of which Punjab Lal and CV-2 were virtually
symptom-less (Kumar et al. 2009). Chilli germplasm and
breeding lines showing resistance/tolerance to leaf curl
viruses in India are shown in Table 1.
Genetically engineered resistance
Geminiviruses hold the competency to exploit many cel-
lular processes of hosts as they have evolved with a mas-
sive potential of recombination. ChiLCVD comes up with a
severe threat to chilli production globally. The conven-
tional breeding system and techniques had been success-
fully used before and still remain the major antiviral
strategy for the development of resistant chilli genotypes.
Therefore, the mechanisms linked to control the viral
accumulation inside host cells, prevention of virus move-
ment within the plant cells and activation of plant defence
mechanisms have been somewhat discussed (Ishibashi
et al. 2007; Hofmann et al. 2009). Recently, the priority
regarding methylation of viral DNA, activation of sequence
silencing machinery and ubiquitylation-mediated defence
against begomoviruses have been reported (Lozano-Duran
et al. 2011; Marino et al. 2012; Sahu et al. 2014a, b). In a
comparison of gene expression between resistant and sus-
ceptible chilli plants, upregulation of several defence-re-
lated genes such as nucleotide-binding site, leucine-rich
repeat (NBS-LRR), thionin, polyphenol oxidase and other
proteins like ATP/ADP transporter was found in the
ChiLCV-resistant variety. This provides novel insights into
the transcriptomics of ChiLCV-resistant chilli plants
(Kushwaha et al. 2015). In order to manage the infection of
chilli-infecting begomoviruses (CIBs), an RNA interfer-
ence (RNAi)-based strategy was applied. Transgenic N.
benthamiana plants bearing two different RNAi constructs
[designated as TR1 (AC1/AC2) and TR2 (AC1/AC2/bC1)]
were generated. Authors observed that two lines having
TR1 construct (13–1 and 2–4) and one line having TR2
construct (5–1) have shown resistance to the most severe
Indian chilli-infecting begomoviruses (Sharma et al. 2015).
Resistant lines accumulated transgene-specific siRNAs,
thus confirming RNAi-mediated resistance against these
viruses. Agrobacterium-mediated transformation of a pure
line variety of hot pepper, RCL 59 M, was carried out. Out

Table 1 Chilli germplasm and breeding lines showing resistance/tolerance to leaf curl viruses in India
S. Sources of resistance References
No.

1. Puri Red, Puri Orange Mishra et al. (1963), Chattopadhyay

et al. (2008)
2. Jwala Tewari and Ramanujam (1974)
3. Surjamani, Perennial, S 118, S 114 (derived from Perennial 9 Long red) Sooch et al. (1976)
4. Perennial, S 5-4, S 20-1, S 41-1, S 118-2—also resistant to Tobacco mosaic virus (TMV) and Singh and Thakur (1977)
Cucumber mosaic virus (CMV)
5. Pant C-1, Pant C-2—tolerant to leaf curl virus Mathai et al. (1977)
6. Delhi Local—tolerant to leaf curl virus—also tolerant to TMV—immune to CMV and PVX Konai and Nariani (1980), Tewari
and Viswanath (1986)
7. Cross 218, EC 121490, IC 18253, IC 18885, JCA 196, Karanja, Pant C-I—less than 30% leaf curl Bhalla et al. (1983)
incidence in the field
8. CA-960, G-4, Jwala Dhanju (1983)
9. Lorai, Longi, Pant C-I, Perennial, S 118-2—resistant/tolerant to leaf curl virus—also Sharma and Singh (1985)
resistant/tolerant to CMV and TMV
10. JCA 196, JCA 218, JCA 248, NP-46-A, Pant C-I, Pusa Jwala Sangar et al. (1988), Brar et al.
(1989)
11. Bangla Green (BG-1), CH-1, Indonesian Selection, Laichi-1, Laichi-2, Lorai, LS-l, MF41-1, MS- Singh and Kaur (1990)
13, Pant C-I, Perennial, Punjab Lal, S 20-1, Surjamani—field resistant to leaf curl virus—also
field resistant to CMV
12. Surajmukhi, Japani Loungi, Pant Chilli-1, Pusa Jwala and PBC-473 Awasthi and Kumar (2008)
13. Punjab Sindhuri and Punjab Tej—moderate resistant to leaf curl virus Dhaliwal et al. (2013)
14. CH-27—F1 hybrid highly resistant to leaf curl virus Dhaliwal et al. (2015)
15. Saurian 2010, Perennial and Japani Loungi Ahmad et al. (2016)
16. DLS-Sel-10, WBC-Sel-5 and PBC-142 Srivastava et al. (2017)

123
Journal of Plant Diseases and Protection
of the twelve plants, seven were tested by Southern blotting
and transgenic integration was confirmed by 0.77 kb band
of coat protein gene. The transgenic plants and non-trans-
genic plants showed normal phenotype and produced
similar fruits (Raghunathachari et al. 2012). A vector-in-
duced gene silencing for chilli leaf curl disease resulted in
systemic silencing of phytoene desaturase (PDS) in the
phloem region of inoculated plants of N. benthamiana. It
was suggested that in the early phase of infection ChiLCV
was found associated with the phloem region and later it
spread to the adjoining nonvascular tissues (Kushwaha and
Chakraborty 2016).
Physical and chemical measures of control
Since last two decades, the B biotype of whitefly (B.
tabaci) has been spreading globally at a rapid rate.
Management of this vector is usually done by synthetic
pesticides, physical barriers and certain agronomic prac-
tices. As the immature forms of the pest are found mostly
underneath leaves and lower part in the plant canopy, so
the conventional chemical control of the whitefly is very
difficult (Glick et al. 2009). The pest is polyphagous in
nature, and therefore the cultivated and weed host are the
major sources of infestation. A number of synthetic and
natural insecticides had been successfully used to control
this pest in the past, but it is able to develop resistance at
a very rapid rate. Several insect growth regulators and
new pyrethroid insecticides may appear promising to
manage this pest. But due to the developing resistance by
the pest, its efficiency will also be of limited duration.
Therefore, depending on chemical control of this pest, it
must be considered a temporary measure and there is a
dire need to develop an integrated pest management
strategy to control this pest in a better way. For con-
trolling virus diseases, as many as preventative measures
should be taken as they are economically justified, as a
single method of control is not likely to keep crops
entirely free from virus infection (Heathcote 1973). Inte-
grated pest management strategy to control chilli leaf curl
virus disease is presented in Table 2.
Conclusion and future prospects
The tropical climate of India supports year-round
intensive crop cultivation and survival of the vector
whitefly. Due to this, a large number of begomoviruses
have been reported in India which cause serious diseases
in many crop plants. Mixed cropping systems of the
country and polyphagous nature of whitefly lead to its
overlapping host range (for example, chilli-infecting
begomoviruses have been reported from plants as diverse
as tomato, papaya and tobacco). The destructive out-
breaks caused by the emergence and re-emergence of
new strains of geminiviruses causing various diseases
have threatened sustainable crop production and are of
serious concern to world agriculture. By studying the
evolution of geminiviruses and their associated satellite
molecules, different strategies can be developed that
may control the speed of their development. The emer-
gence of a new vector biotype (B biotype of B. tabaci)
and increasing vector population are mainly responsible
for the appearance of geminivirus disease problems.
Consequently, there is a dire need for better under-
standing the factors responsible for the increase in the
vector populations in diverse cropping systems. Equally
challenging is the emergence of molecules such as DNA
b and the nanostructured lipid carriers (NLCs) that are
associated with monopartite begomoviruses. The inter-
dependence of the satellites and their helper bego-
moviruses is thus an area of enormous importance for
investigation which will open up new methods of disease
control.
The methods of controlling begomovirus infections in
crop plants are increasing. RNAi suppression by the
begomoviruses is likely to play a major role in such syn-
ergisms; it necessitates a careful look into the mechanisms
of RNAi suppression by begomoviruses prevalent in India.
Well-characterized resistance genes hold a lot of promise
in controlling begomoviruses, and there is need to intro-
gress these genes into popular varieties. Hence, more work
needs to be done to search for natural begomovirus-resis-
tant wild varieties of crop plants, against begomoviruses.
Recently, characterization of new resistance trait in pepper
against the two begomoviruses, Pepper golden mosaic
virus and Pepper huasteco yellow vein virus, in Mexico has
been done (Garcia-Neria and Rivera-Bustamante 2011).
The exciting developments in the plant–virus interactions
promise many more avenues of begomovirus control
123
 Journal of Plant Diseases and Protection

Table 2 Integrated pest management strategy to control chilli leaf curl virus disease
Method Treatments/practice References

Cultural control
Biological control of
vector
Chemical control of
vector (Synthetic)
Natural extracts
@— at the rate of
Use seeds from healthy plants of previous season Reviewed by Kenyon et al.
Growing nursery in protected structures (2014)
Removal of infected seedlings and weed hosts from nursery as soon as seen
Treatment of seedlings with proper systemic fungicides to control vector
Use of yellow sticky traps just above the plants to control insect vectors
Destroying previous year susceptible crops, particularly solanaceous weeds and
volunteer plants
Good weed control in the crop that may be alternative host to virus and vectors
Transplanting dates should be adjusted to avoid peak season of the vector population
Use of reflective (silver colour) plastic mulch
Use of live mulches, border crops or hedges which are more attractive to the vectors
than pepper crop
Predators—Coccinella septempunctata, Clitostethus arcuatus, Orius spp, Chrysoperla Reviewed by Gerling et al.
carnea, Chrysopa spp., Sinea confusa (2001)
Parasitoids—Eretmocerus emiratus, Eretmocerus eremicus, Encarsia accenta,
Encarsia adusta, etc.
Pathogens (Fungi)—Verticillium lecanii and Paecilomyces fumosoroseus, Reviewed by Faria and
Paecilomyces farinosus Wraight (2001)
Mycoinsecticides—BotaniGard, Bea-Sin, Boveril PM, Mycotal, Ago Biocontrol
Verticillium, Pae-Sin
Difenthiuron 50 WP @ 0.75 g per litre Heathcote (1973)
Spraying diazinon, malathion, metasystox at 10 days interval Devi and Reddy (1995)
0.07% monocrotophos with 0.25% wettable sulphur Bhattiprolu and Rahman
(2006)
Diafenthiuron @ 200 ml/litre Hussain et al. (2017)
Imidacloprid 17.8 SL (0.003%) Pandey et al. (2010)
Imidacloprid (0.05%), acephate (0.1%) and malathion (0.05%) Ahmed and Ram (2016)
Neem oil, neem guard, repellin and biosol Chakraborti (2000)
Raw cow milk and Trichoderma Kumar (2006)
Neem seed kernel extract (5%) Pandey et al. (2010)
Seed extract of Sapindus trifoliatus and Solanum trilobatum Ahmed and Ram (2016)
Clerodendrum aculeatum (leaf extract), Terminalia arjuna (bark extract) Chaubey et al. (2017)

opening up in the near future. These need to be urgently to publish this manuscript and are equally responsible and
deployed to assure crop protection against the huge losses accountable.
incurred due to begomoviral infections in India .

Acknowledgements Authors are thankful to Confederation of Indian

Industry, Department of Science and Technology and Verdenta
Hybrid Seeds Pvt. Ltd. for providing Prime Minister’s Fellowship to
Hament Thakur.
Funding This work is funded by Research Grant Number NASF/
ABP-5018/2016-17 from National Agriculture Science Fund (Indian
Council of Agricultural Research).
Compliance with ethical standards
Conflict of interest All the authors hereby declare that they have no
conflict of interest for this manuscript. They hereby give their consent
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