Begomovirus Disease Complex

Plant Diseases and their Sustainable Management | 335
Chapter 17
Begomovirus Disease Complex:
Threat in India
Suresh Chand Meena1 and Anirudha Chattopadhyay2*
1
Department of Plant Pathology, Rajasthan College of Agriculture,
MPUAT, Udaipur, Rajasthan
2
Department of Plant Pathology, C.P. College of Agriculture,
S.D. Agricultural University, S.K. Nagar, Gujarat
Introduction
Plant viruses are widespread and economically important pathogens infecting
all most all the plants that are grown for their food, feed, and fiber. They can be
recognised from many “wild” plants that act as a reservoir. But they have been
mostly studied on cultivated crops due to their financial implications of crop losses.
Many diseases caused by plant virus have been described for just over 100 years, and
some of them like Cacao swollen shoot virus, African cassava mosaic virus, Rice tungro
virus become prevalent and appear in epidemic form at various times and places in
the 19th, 20th and 21st centuries causing serious losses. Among them, three major virus
group viz., Potyviruses, Geminiviruses and Tospoviruses have emerged or re-emerged
as serious threat in different time scale (Rybicki and Pietersen, 1999).
Begomoviruses are the largest genus within the family Geminiviridae. The term
‘Gemini’ was derived from a Greek word “Geninus” meaning twins (Harrison et al.,
1977). Therefore, virus members within family Geminiviridae are characterized
structurally by twinned (geminate) quasi-icosahedral capsids and genetically by
having one or two small circular, ssDNA molecules, and replicate through an
intermediate dsDNA molecule in the nuclei of infected plant cells and using host
DNA replication machinery (Jeske, 2007) as they are lacking of self-machinery system
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* Corresponding Author
336 | Plant Diseases and their Sustainable Management
to replicate themselves (Stanley et al., 2005).They infect a broad range of plants

including both, monocots (monocotyledonous) and dicots (dicotyledonous)
(Gutierrez, 2000) with the production of generalized symptoms like curling of leaves,
yellowing of veins, yellow mosaic patterns, dwarfing of leaves, etc. The members
under family Geminiviridae are classified into four genera on the basis of their genome
organization, host range and insect vector. The genus Begomovirus is the most
important one with its type species Bean golden mosaic virus, now named Bean golden
yellow mosaic virus (Brown et al., 2012). The genus Begomovirus is comprised of about
196 member species, representing the largest genus of family Geminiviridae (Brown
et al., 2012), all infecting dicot plants and transmitted by the whitefly Bemisia tabaci
(Brown, 1994; Markham et al., 1994; Czosnek and Laterrot, 1997; Thresh et al., 1998;
Polston et al., 1999).
In recent years emergence and re-emergence of plant viruses, especially
Begomoviruses particularly in the tropics and sub-tropics, has resulted in enormous
economic losses and in many cases threatened food and nutrition security. During
the last two decades worldwide economic losses due to infections of begomoviruses,
are estimated to be US $1.3-2.3 billion for cassava in Africa due to African cassava
mosaic virus (Thresh and Cooter, 2005), US $5 billion for cotton in Pakistan during
1992-97 due to cotton leaf curl virus (Briddon and Markham, 2001), and US $140
million in Florida (Moffat, 1999), US $50 million in Dominican Republic during
1988-1995(Alvarez and Abud-Antun, 1995), US $4.6 million in the Comayagua Valley
of Honduras in 1992(Caballero and Rueda, 1993), US $40 million in Central America
in 1989 to 1995(Bird et al., 1995) for tomato due to tomato leaf curl virus and other
associated begomoviruses.
In India the emerging threat of begomoviruses has been extensively addressed
earlier by different scientists like Saikia and Muniyappa (1989), Pun and
Doraiswamy(1999), Varma and Malathi (2003), Dasgupta et al. (2003), etc. and the
extent of yield loss caused by some begomoviruses was quantified to be 40-100 per
cent in tomato, 96 per cent in Bhendi, 68-71 per cent in cotton, 18-25 per cent in
cassava, and 21-70 per cent in pulses including blackgram, mungbean and soybean
with estimatedworth of around $300 million rupees per year (Dasgupta et al., 2003;
Varma and Malathi, 2003).
Within the last two decade, a large number of begomoviruses have been
investigated in India, infecting a large number of hosts like legumes, vegetables,
oilseeds, root crops as well as fiber crops. Emerging whitefly, Bemisia tabaci
(Gennadius) transmitted begomoviruses are major pathogens of vegetable, ornamental
and fiber crops throughout the world and including India, particularly in tropical
and sub-tropical regions. Mutation, pseudorecombination and recombination are
driving forces for the emergence and evolution of new crop-infecting begomoviruses.
India, with its large geographical area and diverse agro-climate zones regions, is
endowed with a large number of begomoviruses affecting various cropping systems.
These viruses have a wide host range including cultivated crops, wild genotypes as
well as weeds that provide ideal conditions for the perpetuation of both the viruses
and their vectors. Therefore, emergence and re-emergence of various begomoviruses
are most threatening in Indian subcontinent and becoming a major constraint to
agricultural productivity in all tropical and sub-tropical regions of the world. Recently
they have spread into temperate regions also and emerge in severe form. The changing
agricultural practices and ecological conditions, as well as the global trade of
agricultural products were also encouraging dissemination and severe occurrence of
these diseases. Now, in this chapter we will try to focus on the epidemiology of
Begomoviruses in Indian context to formulate their suitable management strategies.
Genomic Diversity of Begomoviruses

Begomoviruses is a largest and most important genus of the family
Geminiviridaewith 132 species (Fauquet and Stanley, 2005) having single stranded
DNA genome encapsided within characteristic geminate incomplete icosahedral
particles. Its name was derived from type speciesBean golden mosaic virus (van
Regenmortel et al., 1997; Borah and Dasgupta, 2012). They have either bipartite genome
with two DNA components (DNA-A and DNA-B) or monopartite genome (a single
DNA) similar to DNA-A, infecting mostly dicotyledonous plants (Seal et al., 2006;
Borah and Dasgupta, 2012; Brown et al., 2012). DNA-A of bipartite as well as
monopartite begomoviruses typically contain six open reading frames (ORFs) viz.,
AV1/V1(coat protein, CP) and AV2/V2 (AV2/V2 protein) on the virion-sense strand,
and AC1/C1 (replication initiation protein, Rep), AC2/C2 (transcriptional activator,
TrAP), AC3/C3 (replication enhancer, REn) and AC4/C4 (AC4/C4protein) on the
complementary-sense strand. DNA-B contains two ORFs encoding BV1 (nuclear
shuttle protein, NSP) on the virus-sense strand and BC1 (movement protein, MP) on
the complementary-sense strand (Rojas et al., 2005; Seal et al., 2006).This two DNA
components of a bipartitegenome share little sequence similarity except for <“170bp
sequence in the intergenic region (IR), called as common region (CR) (Hanley-Bowdoin
et al., 1999). Although the sequence of CR is usually almost identical in both
components, this may substantially differ between DNA A and DNA B component
as evident in case of Tomato leaf curl Gujarat virus (ToLCGV) and Cotton leaf crumple
virus (CLCrV) with 40 and 37 per cent difference, respectively (Chakraborty et al.,
2003; Idris and Brown, 2004). Despite these differences, sequences critical for
replication are identical between both components of each individual virus and
comprises iterative sequences (iterons) that are recognized and bound by Rep protein
for initiating Rolling Circle Replication (Fontes et al., 1994; Orozco et al., 1998) and a
conserved inverted repeat sequence forming a stem–loop structure from where rolling
circle replication initiates (Laufs et al., 1995; Stanley, 1995). The IR also harbours the
promoter/regulatory elements for expression of the viral genes in both V-sense and
C-sense strand (Jupin et al., 1994; Laufs et al., 1995; Wartig et al., 1997; Borah and
Dasgupta, 2012).
Based on the phylogenetic studies, the genus begomoviruses can be broadly
divided into two groups, the Old World begomoviruses (begomoviruses) (those
originating from Europe, Africa, Asia and Australasia and mostly having monopartite
genome) and the New World begomoviruses (those originating from the Americas
and having bipartite genome) (Rybicki, 1994; Padidam et al., 1999; Paximadis et al.,
1999).
Old World Begomoviruses

Usually those begomoviruses originating from Europe, Africa, Asia and
Australasia, are popularly known as ‘Old World’ Begomoviruses. Although few of
them having bipartite genome, the majority of old world begomoviruses have
monopartite genomes consisting of only a single genomic component which is
homologous to DNA-A of bipartite viruses (Sattar et al., 2013).A small number of
these monopartite begomoviruses are truly monopartite without any satellite molecule,
while a majority of the monopartite begomoviruses are associated with satellite DNA
(Briddon and Stanley, 2006).There are basically two types of DNA satellites, known
as alphasatellites and betasatellites. The alphasatellites (previously known as DNA-
1) are satellite-like, circular ssDNA molecules, about 1.400kb in size, having a single
gene encoding the replication-associated protein (Rep) for initiation of rolling-circle
replication and are capable of autonomous replication in plant cells. They have
homology to the Rep-encoding components of nanoviruses, a second family of plant
infecting ssDNA viruses (Gronenborn, 2004). Therefore, they are believed to be
evolved from nanoviruses, and require a helper begomovirus for movement within
and between plants (Mansoor et al., 1999; Saunders and Stanley, 1999). Whereas, the
betasatellites (previously known as DNA-b) are small circular, single-stranded DNA
satellites (~1.35Kb), associated with monopartite begomoviruses, but do not have
any sequence homology with helper begomoviruses with the exception of sequences
within the apex of two stem-loop structures, containing the ubiquitous geminivirus
TAATATTAC motif (Briddon et al., 2003). They do not encode for any replication-
associated proteins but carry a single ORF (bC1), encoding a multifunctional protein
that acts as a pathogenicity factor. Therefore, it requires a helper begomovirus for
replication, movement and transmission and enhances the pathogenicity of helper
viruses by inducing the disease severity, altering the host range, suppressing host
defense (Kon et al., 2007; Saeed et al., 2007). The old world begomoviruses are very
diverse, as sometimes they are not associated with satellites and sometimes found to
be associated with either one or both alpha- and betasatellite. This type of complexes
mostly prevails in the OW including Asia and Africa. This can be evident from
Tomato yellow leaf curl virus (TYLCV) which is generally not associated with
satellites. Although a single isolate of TYLCV originating from Oman, has been shown
to be associated with both an alpha- and a betasatellite (Idriset al., 2011).
New World Begomoviruses

It has been hypothesised that most of the New World begomoviruses were evolved
more recently than Old World viruses, after the continental separation of the Americas
from Gondwana, approximately 130 million years ago (Rybicki, 1994). Begomoviruses
originating from the New World (NW) typically have bipartite genomes consisting of
two separately encapsidated genomic components, known as DNA-A and DNA-B
(Brown et al., 2012).So far, no monopartite begomoviruses natives to the New World
have been reported, although some monopartite begomoviruses have been introduced
from the Old World (OW) (Zhang and Ling, 2011). Whereas the presence of New
World-like begomoviruses in the Old World was evident from Corchorus yellow vein
Plant Diseases and their Sustainable Management
Figure 17.1: Genome Organization of Begomoviruses and their Associated DNA Satellites (Courtesy, Sattar, 2013).
| 339
virus (CoYVV) from Vietnam suggesting the probable occurrence of New World-like
viruses in the Old World prior to the Gondwana separation (Ha et al., 2007).
Pathogenesis of Begomoviruses
The infection of begomoviruses starts with the feeding of a viruliferous whitefly
(B. tabaci) by directly injectingthe virion particles on the phloem cells of a host plant
leading to the beginning of the chain of pathogenesis. As soon as the feeding starts,
viral particles enter into the vascular system of the plant. From the initially infected
cells, the virus particles are moved to the mesophyll cells of infected tissue, where it
become uncoated and viral DNA enters into the nucleus where viral DNA replication
and transcription occur (Gafni and Epel, 2002). Begomoviruses do not encode their
own polymerases and instead depend on host polymerases and associated factors
(together termed the host replisome) for replication and transcription. The During
replication, viral single-stranded DNA (ssDNA) is released from virions and copied
to generate double-stranded DNA (dsDNA) by using host DNA polymerases, whereas
the dsDNA in combination with nucleosome is transcribed by using host RNA
polymerase II. The viral genome is initially translated intoreplication initiator protein
(Rep) protein which is transported into the nucleus of the infected host cell to assist
with viral DNA replication. Rep commences virus-specific recognition of its cognate
ori-site (Hanley-Bowdoin et al., 1999).
Begomoviruses replicate through a combination of Rolling Circle mechanism
(Saunders et al., 1991) and recombination-dependent replication (RDR) mechanism
(Alberter et al., 2005). The whole replication process is carried out via three phases,
viz., initiation, elongation and termination. During initiation phase, Rep initiates
rolling-circle replication by binding to the IR of the virus and introducing a nick at
the conserved sequence of viral dsDNA to generate a free 32 -hydroxyl end that
primes ssDNA synthesis. This is followed by displacement of the parental strand
and production of a replication fork in coordination with various host factors, i.e.,
RF-C, PCNA, RPA, RAD54, SCE1 and DNA polymerases etc. (Xie et al., 1995;
Bagewadi et al., 2004; Sánchez-Durán et al., 2011; Kaliappan et al., 2012). The chain
elongation takes place at the 5’ to 3’ direction govern by Rep, which now acts as a
helicase (Choudhury et al., 2006); and finally termination of chain synthesis occurs
when Rep cuts and re-ligates the ssDNA to make it circular genome (Singh et al.,
2008). The released ssDNA is converted to dsDNA to re-enter the replication cycle.
Accumulation of viral DNA replication products and intermediates then triggers a
genotoxic response and upregulates the expression of host genes encoding DNA
repair and recombination proteins, resulting in a switch to recombination-dependent
replication (Ascencio-Ibanez et al., 2008; Hanley-Bowdoin et al., 2013). During
recombination-dependent replication, homologous recombination between a partially
replicated ssDNA and a closed, circular dsDNA take place to form a looped molecule
that serves as a template for both ssDNA and dsDNA synthesis. AC3/REn stimulates
viral DNA replication depending upon the interaction of Rep with Replication
enhancer protein (Ren) (Pasumarthy et al., 2011). Moreover, the binding of REn to the
SINAC1 transcription factor also enhances viral DNA replication (Selth et al., 2005).
In late phase infection process, Rep represses its own transcription, leading to
activation of transcriptional activator protein (TrAP) expression, which in turn

activates the expression of coat protein (CP) and nuclear shuttle protein (NSP). Now,
coat protein is used to encapsidate the circular ssDNA to form mature virions, which
are available for whitefly acquisition and nuclear shuttle protein binds to viral DNA
and moves it across the nuclear envelope to cytosol, where movement protein (MP)
traffics it across a plasmodesmata and helps in cell to cell movement (Hanley-Bowdoin
et al., 2013).
Vector Transmissibility of Begomoviruses

Like all other vector transmitted geminiviruses, begomoviruses also rely entirely
on their arthropod vector whitefly Bemisia tabaci (Gennadius) for their plant-plant
transmission in persistent circulative manner. Whiteflies acquire mature virions
during feeding on the phloem of an infected plant. Usually longer feeding enhances
the acquisition of virus. The virions move through the alimentary canal into the
whitefly midgut where they attach to cell membrane and cross the midgut, via a
specialized organ within the midgut called filter chamber (Ghanim et al., 2001) and
enter the hindgut cells by endocytosis and finally rich to the haemolymph and
ultimately transit to the primary salivary glands and finally emptied from the salivary
glands through the salivary ducts into the salivary canal within the stylet of white fly
vector for transmission during the next feeding cycle (Ghanim et al., 2001). The passage
of several begomoviruses within vector have been explored by using several light
and electron microscopy techniques, as well as fluorescence in situ hybridization
(FISH), immunogold and immune-flourescence methods (Ghanim et al., 2001; Czosnek
et al., 2002). Begomoviruses are highly genetically diverse. This diversity, which leads
to variations on the protein level, might explain the specificity at the virus-vector
interactions level (Hogenhout et al., 2008; Power, 2000; Stanley, 2004). This specificity
is determined by certain proteins of both virus and vector origin. The CP is the only
viral-encoded protein required for vector-mediated transmission. On the other hand,
an abundant 60 kDa protein GroEL homologue determines the binding affinity to
virions (Morin et al., 2000). GroEL was synthesised by the secondary endosymbiont,
Hamiltonella spp. of B. tabaci (Gottlieb et al., 2010). Additionally, a whitefly-encoded
HSP70 protein can also play an important role in circulative transmission of various
begomovirus (Gotz et al., 2012).
The virus-vector specificity for begomoviruses is an important feature that
operates below the species level with several different biotypes of B. tabaci. B.tabaci is
a species complex representing different cryptic species for which genetic variation
can be correlated with morphological variation in adults or pupae for discrimination
(Brown, 2007). B. tabaci complex can besub divided into 11-well defined groups
containing 24 species which are morphologically indistinguishable from each other
(De Barro et al., 2011). On the other hand, depending upon different host plant
preferences and virus transmission properties, the indistinguishable B. tabaci
populations are described as distinct biotypes from A to T (De Barro et al., 2005; Seal
et al., 2006). Some begomoviruses are transmitted more efficiently by these specific
biotypes and this can be evident from the vector specificity of 15 begomoviruses with
the “B” biotype of B. tabaci as compared to other biotypes (Bedford et al., 1994).There
are two main exotic biotypes of B. tabaci, the B and Q types. The B biotype is the most
widely distributed worldwide as well as India also. The B and Q biotypes, both have
wide host range including cultivated and uncultivated species, but also have
differential response to insecticides commonly used for whitefly control. The Q biotype
also has a broad host range and has exhibited resistance to the neonicotinoid
insecticides used controlling the B biotype. In certain cases, it found to establish more
mutualistic relationship with specific virus, like Tomato yellow leaf curl virus (TYLCV)
for suppressing host defense and their subsequent spread in China (Shiet al., 2014).
Although Q- biotype is absent in India, but its recent emergence from the Mediterranean
region and rapid introduction into North (Mexico, U.S.) and Central America
(Guatemala), and multiple locations in Asia (China, Japan, among others), poses a
renewed threat to Indian agriculture. Therefore, there is a need for tracking and
monitoring on imported planting materials and the legalized regulation of invasive
introduction of this biotype.
Driving Forces for the Emergence and Evolution of Begomo-

viruses
The emergence and outbreak of certain begomoviral species into new habitats in
different parts of the world is an increasing concern due to havoc crop loss. There are
various factors responsible for the apparent increasing problem of begomoviruses in
world as well as in Indian continent. The transport of plant and their vectors due to
increasing global trade and global human activity and new agricultural practices
coupled with climate change, increases the possibilities of the genetic diversity of
viruses and their strains. Germplasm collecting expeditions, international movement
of plant material, and lowered trade barriers offers opportunities for unknown viruses
to be introduced into new areas. The misuse of pesticides has resulted in multiple
chemical resistances in vectors population also. With the increase in acreage of
transgenic crops carrying viral genes, increasing concern of new virus evolution will
continue. This will disrupt the virus controlling strategy.
Begomoviruses are quite diverse in nature. During the past couple of decades
the prevalence and distribution of different begomoviruses have been increased
throughout the world and that can be evident from the identification and
characterization of more and more begomoviruses from diverse host (Fargette et al.,
2006; Navas- Castillo et al., 2011). In India-Pakistan sub-continent, the majority of
begomoviruses are monopartite associated with satellites representing old world
origin (Nawaz-ul-Rehman and Fauquet, 2009), like Cotton leaf curl viruses (Kirthi et
al., 2004), Pepper leaf curl Lahore virus (PepLCLV) and Bhindi yellow vein mosaic virus
(BYVMV) (Fauquet et al., 2008), etc. While, a small number of them are bipartite such
as Indian cassava mosaic virus (ICMV) and Tomato leaf curl New Delhi virus (ToLCNDV)
(Hong et al., 1993; Padidam et al., 1995). The Emergence of begomoviruses in Indian
subcontinents is due to wider host range of indigenous viruses infecting a large
number of weed and wild host species which facilitates emergence of novel species
through recombination and/or pseudo-recombination (Zhou et al., 1997; Padidam et
al., 1999; Pita et al., 2001) to increase the possibilities of host jump into new species.
This is also directly correlated to high population levels of their whitefly vector. Once
adapt to native plant species, plant viruses are readily and rapidly making their way
into cultivated monoculture system in which they become rapidly diversified and
gain higher pathogenic fitness by employing inter-specific recombination, which
can occur when two or more viruses infecting same plant and reassert heir genomic
components DNA-A and DNA-B during replication. This is mostly common in closely
related species which are sufficiently compatible for replication of repetitive sequences,
but sometimes can also be found in distantly related virus components which are
compatible for recombination in this region. Therefore, Mutation, pseudo-
recombination and recombination are the major driving forces responsible for the
emergence and evolution of new crop-infecting begomoviruses (Singh et al., 2012).
Mutation
Mutation is the abrupt genetic change in genome at nucleotide level which is
heritable in nature. It occurs during different biological processes like replication
slippage or it can be induced by UV-light, chemical treatments etc. The incorporation
or deletion of a non-complementary nucleotide during duplication of DNA or RNA
leads to point mutations, which alters the whole genetic information. Generally it is
thought that RNA viruses are more prone to higher mutation rate than DNA viruses
due to their dependence on error-prone RNA dependent RNA polymerase lacking
proofreading capabilities used for their replication (Steinhauer and Holland, 1986;
Domingo and Holland, 1997; Jenkins et al., 2002). But there is also some evidence of
higher mutation frequency in Geminiviruses, especially begomoviruses and
mastreviruses (Sanz et al., 1999; Arguello-Astorga et al., 2007; van der Walt et al.,
2008). The mutation rate of begomoviruses is influenced by nature of virus, host
plant, age of the host plant and inoculum homogeneity. Begomoviruses have high
mutation rate in wild as well as cultivated hosts due to non-functioning of mutation
repair mechanisms of host DNA dependent DNA polymerases in the geminivirus
cycle (Inamdar et al., 1992). Although recombination is the main source of emergence
of new species and strains (Lefeuvre et al., 2007; Garcia-Andres et al., 2007b), but
accumulation of point mutations also contributes to the viral diversity (van der Walt
et al., 2008) with few exception like Tomato yellow leaf curl Sardinia virus (TYLCSV)
having higher mutation frequency, but low genetic diversity (Sanchez-Campos et al.,
2002).
Recombination
Recombination is the process of segmental exchange of genetic elements between
two strands of DNA or RNA during replication. Genetic recombination is an important
mechanism of evolution of many plant viruses and is very frequent in begomovirus
group. Genetic recombination between viruses is a form of parasexual reproduction
during which two parental viruses each contribute genetic information to an offspring,
or recombinant virus (Martin et al., 2011) and that can be evident from sequence
comparison of different genera of family Geminiviridae, denoting the evolution of
topocuviruses due to recombination between a mastrevirus and a begomovirus
(Briddon et al., 1996; Rojas et al., 2005). Thus, interspecific homologous recombination
is the main driving force for genetic diversity and evolution of begomovirus (Sanz
etal., 1999).This helps to generatemore pathogenic variants also. It can be exemplified
by prevalence of cotton leaf curl Burewala virus (CLCuBuV), a distinct begomovirus

responsible for breaking down resistance in cotton, which was an outcome of
recombination between Cotton leaf curl Multan virus (CLCuKoV) and Cotton leaf curl
Kokhran virus (CLCuMuV) (Amrao et al., 2010). The higher frequency of recombination
in begomoviruses leads rapid changes in the avirulence (Avr) gene(s) (Bonas and
Lahaye, 2002) and this could results in breaking down of host resistance, as seen in
case of soybean mosaic virus (SMV) and African cassava mosaic virus (ACMV) also
(Seo et al., 2009; Seo and Shon, 2011). Emergence of new begomoviruses depends
upon how frequently begomoviruses are recombined. Sometimes, begomoviruses are
also acquiring different types of satellite molecules which enhance the pathogenicity
and further complicate the system (Nawaz-ul-Rehman and Fauquet, 2009; Zaffalon et
al., 2011). This recombination is not only experienced either between genomic
components of different begomoviruses or between genomic component and satellite
molecule of different begomoviruses, but can also be found between two distinct
types of satellites (Urbino et al., 2003; Tao and Zhou, 2008; Nawaz-ul-Rehman and
Fauquet, 2009; Venkataravanappa et al., 2011; Huang et al., 2013)
Pseudorecombination
Pseudorecombination or reassortment is the exchange of DNA-A and DNA-B
genomic components between two viruses (Seal et al., 2006). Pseudorecombination is
very common among the bipartite begomoviruses infecting a large number of hosts.
Some monopartite begomoviruses are also found to have acquired a DNA-B component
permanently under field conditions and converted to bipartite state within host system,
which is popularly called as ‘mono-bipartites’ begomoviruses (Saunders et al., 2002;
Chakraborty et al., 2003). Reassortment is usually observed between closely related
begomoviruses, especially between the isolates of the same begomovirus (Stanley et
al., 1985) owing to the specificity of the replication-associated (Rep) protein for the
cognate origin of replication, i.e., common region (CR) of the components of a bipartite
begomovirus(Rojas and Gilbertson, 2008). This even was also reported to occur between
distantly related bipartite begomoviruses, i.e., from different phylogenetic clades
(Garrido-Ramirez et al., 2000), like the reassortment between Tomato mottle
virus(ToMoV) and Bean dwarf mosaic virus(BDMV) (Gilbertson et al., 1993). This
event is very frequent among legumeinfecting begomoviruses (Borah and Dasgupta,
2012). The evidence of co-infectingfive different DNA-A molecules in associationwith
one DNA-B of MYMV-Vig within a single blackgram (V. mungo) plant was very
interesting (Balaji et al., 2004). Pseudo-recombination between DNA-A and DNA-B of
MYMIV was reported to occur in almost all legume hosts,viz., blackgram, soybean
except in cowpea, showing its host-specificity (Surendranath et al., 2005)and role in
symptom development (Mahajan et al., 2011).But in certain cases, re-assortment is
not enough for emergence of new bipartite begomoviruses. Therefore some sorts of
secondary genetic changes will often are needed after interspecific reassortmentfor
better biological fitness and wider host adaptation (Harrison and Robinson, 1999).
Emerging Diseases Caused by Begomoviruses in India

Till date, a large number of plant disease caused by begomoviruses are reported
in India (Table 17.1). Some of them are appearing in epidemic form and remain
prevalent through the years, whereas others are sporadic in nature. Many new plant
viruses are also continuously emerge out in our intensified agroecosystem with
changing climatic scenario. Some of these emerging begomovirus disease complex
are discussed here.
Cotton Leaf Curl Disease
Cotton (Gossypium hirsutum L.) is one of the most important cash crops in India.
Among various constrains in cotton production in Indian subcontinent,leaf curl
disease of cotton is becoming a serious problem causing huge losses due to complex
nature of the pathogen and prevalence of whitefly vector (Khan and Ahmad, 2005).
There are different virus species, all belonging to the genus Begomovirus, associated
with this disease.The involvement of six species, viz., Cotton leaf curl Alabad virus
(CLCuAV), Cotton leaf curl Gezira virus (CLCuGV), Cotton leaf curl Kokhran virus
(CLCuKV), Cotton leaf curl Multan virus (CLCuMV) and Cotton leaf curl Rajasthan virus
(CLCuRV) (Fauquet et al., 2003) and recently identified two new isolates, CLCuV-
SG01 and CLCuVSG02 from Rajasthan and their frequent recombination with each
other makes the disease very complex (Kumar et al., 2010). The genetic variability of
begomoviruses in India is also increased due to associated satellite molecules
responsible for typical symptoms production of leaf curl disease, viz., cupping of
leaves and curling of leaf margins, swelling and darkening of leaf veins with
characteristic enation at lower side of the leaf (Kirthi et al., 2004). Virus-infected
plants are symptomless or exhibit very mild symptoms unless also infected with the
DNA-b (Mansoor et al., 1997; Harrison et al., 1997).Therefore, it was spread very
rapidly in entire cotton growing areas of Rajasthan, Punjab and Haryana (Narula et
al., 1999) and incidence in some areas reached up to 97 per cent with 17.48 per cent
reduction in boll weight, 32.57 per cent reduction in seed weight and 33.77 per cent in
seed (Sharma, 2002)
Yellow Mosaic Disease of Legumes
Yellow mosaic disease (YMD) of pulses is one of the major serious problems that
farmers have faced in different pulse growing regions of India as well as Asia, which
may cause up to 85–100 per cent yield loss (Nene, 1973).It is a kind of “disease
complex” which is caused mainly by whitefly-transmitted geminiviruses, causing to
yellow mosaic and golden mosaic diseases. Swanson et al. (1992) classified legume
infecting geminiviruses in India broadly into two groups. One group comprises
dolichos yellow mosaic virus and the other group includes the yellow mosaic viruses
that infect blackgram, cowpea, french bean, horsegram, pigeonpea, soybean,
mungbean, etc. On the basis of sequence identity analyses, the bipartite begomovirus
isolates, namely, mungbean yellow mosaic virus (MYMV), mungbean yellow mosaic
India virus (MYMIV) and horse gram yellow mosaic virus (HgYMV) are recognized
as the causal agents of yellow mosaic disease of legumes across India and southern
Asia (Vanitha Rani et al., 1996; Qazi et al., 2007; Malathi and John 2008a; Ilyas et al.,
2010). Although they are closely related and have distinct but overlapping host ranges,
they differ in their infectivity, prevalence and genome sequences. Among them, two
species viz; Mungbean yellow mosaic India virus (MYMIV) and Mungbean yellow
mosaic virus, are prevalent and the remaining two, i.e., Dolichos yellow mosaic virus
(infecting Lablab purpureus) and Horsegram yellow mosaic virus, occur rarely (Fauquet
and Stanley, 2003; Maruthi et al., 2006). Of these viruses, mungbean yellow mosaic
virus (MYMV) is important as it infects five major leguminous species, blackgram,
mungbean, frenchbean, pigeonpea and soybean, causing an annual loss of yield of
about $300 million (Varma et al., 1992). Mostly mix infection of these begomoviruses,
sometimes in association with other viruses, viz., carmoviruses is a serious problem.
The ability of these viruses to exchange genetic material by recombination/pseudo-
recombination, enrich the genetic diversity in population of begomoviruses and
increases the probability of emergence of new virus or viral strains to cause epidemics
in previously unaffected crops or elite cultivars of the same crops.
Tomato Leaf Curl Disease

Tomato leaf curl disease (ToLCD) is a most common and most destructive disease
of tomato in India as the infection starts from very early stage during nursery or
transplanting and continues up to maturity, resulting havoc loss in fruit yield (Rishi,
2004). In Indian sub-continent, this disease is becoming a serious concern due to
wide host range of pathogen infecting about 23 plant species (Saikia and Muniyappa,
1989) and involvement of six different species of begomovirus, viz., Tomato leaf curl
Bangalore virus (ToLCBV), Tomato leaf curl Bangladesh virus (ToLCBDV), Tomato leaf
curl Gujarat virus (ToLCGV) Tomato leaf curl Karnataka virus (ToLCKV), Tomato leaf curl
New Delhi virus (ToLCNDV), and Tomato leaf curl Sri Lanka virus (ToLCVSLV) (Fauquet
et al., 2003). Interestingly, prevalence of bipartite begomovirus, viz., ToLCNDV,
ToLCGV in north India, and that of monopartite begomovirus, viz., ToLCBV, ToLCKV
in south India signify the higher population diversity of tomato leaf curl viruses in
India (Chatchawankanphanich et al., 1993; Hong and Harrison 1995: Srivastava et
al. 1995; Padidam et al., 1995; Muniyappa et al., 2000; Chakraborty et al., 2003).
Chilli Leaf Curl Disease
Chilli leaf curl disease is a threatening problem to chilli production in India due
to complex etiology of the disease along with infestation of thrips and mites. Chilli
leaf curl virus (ChiLCV) (Kumar et al., 2006). This disease is mainly caused by a
monopartite begomovirus, i.e., Chili leaf curl virus (ChiLCV) (Khan et al., 2006;
Senanayake et al., 2006). Sometimes, Tomato leaf curl Joydebpur virus was also
found to be associated with this disease (Shih et al., 2006). The ChiLCV has a chimeric
genome perhaps derived through recombination between ChiLCV and ToLCV (Khan
et al., 2006). Therefore, emergence of different variants of ChiLCV, infecting chilli in
North India, is very common. Intensive use of insecticides targeting whitefly and
development of resistant/tolerant germplasm can be employed to control this disease
(Kumar et al., 2006; Rai, 2010).
Yellow Vein Mosaic Disease of Okra
Yellow vein mosaic disease (YVMD) of okra (Abelmoschous esculentus L. Moench)
is the most important and destructive viral disease in India. It produces very complex
symptoms like network of yellow veins enclosing green tissues, curling of infected
leaves, reduction in the leaf size and stunting of the plant, and finally yellow deformed,
small sized and tough in textured fruits affecting the yield adversely.Infection rate
may reaches up to 100 per cent but in field yield loss ranges between 50 per cent and
94 per cent depending on the stage of crop growth (Sastry and Singh, 1975). The
yellow vein mosaic disease of okra (YVMD) is caused by a whitefly transmitted
begomovirus, Bhendi yellow vein mosaic virus (BYVMV) having a monopartite
genome (Kulkarni, 1924). The monopartite genome is responsible for the production
of mild symptoms only (Jose and Usha, 2003), but typicalvein yellowing symptom
was induced only in associationwith the cognate betasatellite, due to the enhancement
of pathogenicity by suppression of host silencing activity of the bC1,reported later
(Gopal et al., 2007).
Cassava Mosaic Disease

Cassava mosaic disease (CMD) is another most important disease in India caused
by begomovirus which is first time reported in 1966 and subsequently become
prevalent in southern India (Calvert and Thresh, 2002), resulting 10–15 per cent
yield losses. Involvement of two bipartite begomoviruses, viz., Indian cassava mosaic
virus (ICMV) and Sri Lankan cassava mosaic virus (SLCMV) (Hong et al., 1993; Patil et al.,
2005; Saunders et al., 2002) and recombination among the population of cassava
infecting-begomoviruses in India (Rothenstein et al., 2006) make the disease very
complex. In addition, production of def-DNA during recombination between DNA-
A and DNA-B of ICMV and SLCMV enrich the genetic diversity of the virus population
(Patil et al., 2007) and complexity of the disease.
Management Strategies of Begomoviruses

Management of begomoviruses is very difficult due to complex nature of the
disease. Wide host range and efficient vector transmission of begomoviruses in most
cases make the disease very complex. The dynamics of the virus-vector complex and
their interaction with host plants is very important and may vary according to habitat,
property of virus, vector behaviour, nature of host crop and other epidemiological
factors (Brown and Bird, 1992). This presents a challenge for devising suitable
management strategies. Therefore, adequate information on both the biology of plant
viruses like host range, mode of replication, mode of survival, etc. and the ecology
and behaviour of vector population like feeding, oviposition, reproduction, virus
transmission, existing/overlapping generations round-year, etc. should be generated
to estimate their significance in maintaining disease pressure (Salati et al.,
2002).Generic approaches mostly including various cultural practices and chemical
practices with the aim of avoidance of inoculum sources and prevention of vector
population are usually practiced. Various cultural practices like removal of reservoir
host and weeds to affect their survival, roguing of infected plants to assist in delaying
virus spread into healthy host, crop rotation to break the life cycles of plant viruses as
well as insect vectors are very popular. Whereas, practices of intercropping with
insusceptible crop and use of trap crop to restrict vector populations by changing the
behaviour of whitefly (viz., feeding, movement between plants) are commonly
preferred. These cultural practices may not be able to totally prevent the spread and
development of disease, but infection rate may be delayed and the incidence of viral
disease may be lessened throughout the cropping season or year (Rampersad,
2003).These cultural methods for disease suppression should be supplemented with
chemical based management. The regulated application of chemical like synthetic

insecticides like Neonicotinoids (imidacloprid) and non-neurotoxic insect growth
regulators (buprofezin and pyriproxyfen) can also be used to control Bemisia tabaci.
But availability of effective viricides for controlling plant viruses is still lacking.
Integration of these generic approaches along with some specific approaches will be
most effective for the management of viral diseases of plants in India.
Among various specific approaches, use of crop specific resistant cultivar is the
only solution for plant virus management, as there are no therapeutic control measures
against them. Although approach is considered to be economically cheapest and
environmentally safest one, but rapid emergence of resistant breaking strains of plant
viruses and lack of sources of resistance are make the breeding programme very
difficult. Genetic resistance against plant viruses is considered to be the one of the
most efficient if suitable germplasm is available. The genes conferring such resistance
phenotypes can be transferred to elite variety by conventional breeding, which is also
very time consuming. Therefore, molecular breeding has provided new path for rapid
development of suitable cultivar through marker assisted selection. Introgression of
resistance genes, viz., Ty-1 (and its allele, Ty-3), Ty-2, Ty-4, ty-5, and Ty-6into cultivated
tomato (Solanum lycopersicum L.) primarily from wild tomato (Solanum chilense) against
Tomato yellow leaf curl virus (TYLCV) is few such evidence. Deployment of these
resistance genes would be best way to utilise our resistance sources in long run.
Therefore, crop varieties with durable resistance by ‘pyramiding’ resistant genes is
preferred over monogenic resistance. Pyramided tomato lines carrying different
combination of Ty series genes could be important genetic resources for sustainable
tomato production against various begomoviruses (Prasanna et al., 2014; Hutton et
al., 2015).
Micro-propagation of more than 100 species of horticultural plants also helps in
mass production of virus free seeds and planting materials. Establishment of virus
indexing facilities and certification system of micro-propagated plants also ensure
the quality of planting material in large scale and check the spread of viral diseases
through tissue culture raised plants. Advancement in genetic engineering also opens
a path to develop virus resistant transgenic plants to manage economically important
viral diseases of a variety of agricultural and horticultural crops. This transgenic
approach is very popular in many countries as the non-conventional strategy for
virus resistant. Transgenic plants are developed either through exploitation of
pathogen derived genes or non-pathogen genes. Transgenic resistance against
begomoviruses has been achieved in a number of plants using a variety of strategies
including expression of viral proteins like Coat Proteins, movement proteins,
Replication proteins and its derivatives, etc. and expression of non-viral proteins
having an anti-viral effect like toxic protein dianthin, antibodies raised against viral
CP, etc. (Vanderschuren et al., 2007). The efforts are being made in India also. But
regulatory body are concern about the biosafety issues related to transgenic plants.
Post transcriptional gene silencing (PTGS) mediated by RNAi is the latest approach
for mitigating the problems of plant viruses via non-transgenic manner. The success
of RNAi as a tool in curing infection of many begomoviruses, like ACMV, VMYMV,
CLCuV, TYLCV have been achieved with the production of virus specific siRNA.
RNAi technology when applied against African cassava mosaic virus (ACMV)
showed 99 per cent decrease of Rep transcripts and 66 per cent reduction in viral
DNA due to transiently expression of siRNA into the protoplast effective against the
replicase (Rep) coding sequence of the ACMV (Vanitharani et al., 2003).More recently,
novel resistance approaches, like expressing the GroEL protein of endosymbiotic
bacterial origin in the phloem tissue of tomato plants, have resulted in the viral
particles getting trapped within the plants, thereby resulting in resistance (Akad et
al., 2007).
Conclusion
A large number of plant diseases caused by various begomoviruses have been
reported from India. These diseases are becoming a serious problem to Indian farmers,
due to havoc crop loss. With the intensification of agricultural practices, the existing
plant diseases are spreading very rapidly and some new diseases are emerging as a
major one. There are various factors responsible for this. Some major factors, like the
overlapping host range, the polyphagous nature of the vector whitefly and intensive
cropping systems that are prevalent in this country, give a chance of frequent genetic
recombination events between various begomoviruses infecting same host. This would
increase the genetic diversity within the population of begomoviruses. Due to this
higher recombination potential, increasing host range, and efficient transmission by
whitefly vector, begomoviruses pose a serious threat to crop production and thus
food security in India.
Therefore, much attention has to be paid in the research to explore the population
dynamics and epidemiology of begomoviruses in India. Genomic profiling of existing
begomoviruses and detection of possible genetic recombination using bioinformatic
tools is essential to critically analyse the epidemiology of the disease and will be
helpful to formulate suitable management practices. Efforts should also be given to
anticipate the synergistic effects of multiple infections of begomoviruses resulting in
the emergence of new virulent strains. Through investigation on mechanism of
suppression of host defense and break down of host resistance by different
begomoviruses is also scientifically fascinating way to find out new methods of
controlling begomoviral diseases in India. Although resistance breeding against
begomovirus is promising to manage this problem, but searching of natural
begomovirus-resistant wild crop plants, characterization of resistance genes and
subsequent introgression into popular varieties is very cumbersome process. Hence,
the scope and possibility of plant virus resistant-transgenic is expanding. Deciphering
the interaction of begomoviruses with the vector whiteflies is also very crucial for the
spread and prevalence of begomoviruses in the field, Therefore, there is an urgent
need of carefully look on multiple aspects of complexity of begomovirus diseases in
India.
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Begomovirus Disease Complex

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Plant Diseases and their Sustainable Management | 335

to replicate themselves (Stanley et al., 2005).They infect a broad range of plants

Genomic Diversity of Begomoviruses

Old World Begomoviruses

New World Begomoviruses

activation of transcriptional activator protein (TrAP) expression, which in turn

Vector Transmissibility of Begomoviruses

Driving Forces for the Emergence and Evolution of Begomo-

by prevalence of cotton leaf curl Burewala virus (CLCuBuV), a distinct begomovirus

Emerging Diseases Caused by Begomoviruses in India

Tomato Leaf Curl Disease

Cassava Mosaic Disease

Management Strategies of Begomoviruses

chemical based management. The regulated application of chemical like synthetic

molecule associated with some monopartite begomoviruses. Virology.312: 106–

nontransmissible begomoviruses in the yeast two-hybrid system. Virology. 276:

Characterization of an infectious clone, virus monitoring in whiteflies and

Seo, J. K., Lee, S. H. and Kim, K. H. (2009). Strain-specific cylindrical inclusion

Swanson, M. M., Varma, A., Muniyappa, V. and Harrison, B. D. (1992). Comparative

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