Mungbean yellow mosaic virus (MYMV): a threat to green gram ( Vigna radiata ) production in Asia

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Mungbean yellow mosaic virus (MYMV): a threat togreen gram (Vigna radiata) production in AsiaA. Karthikeyana, V.G. Shobhanaa, M. Sudhaa, M. Raveendrana, N. Senthila, M. Pandiyanb &P. Nagarajana

a Department of Plant Molecular Biology & Biotechnology, Centre for Plant MolecularBiology, Tamil Nadu Agricultural University, Coimbatore, Indiab National Pulse Research Centre, Tamil Nadu Agricultural University Vamban,Pudukkottai, IndiaPublished online: 26 Nov 2014.

To cite this article: A. Karthikeyan, V.G. Shobhana, M. Sudha, M. Raveendran, N. Senthil, M. Pandiyan & P. Nagarajan(2014) Mungbean yellow mosaic virus (MYMV): a threat to green gram (Vigna radiata) production in Asia, InternationalJournal of Pest Management, 60:4, 314-324, DOI: 10.1080/09670874.2014.982230

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Mungbean yellow mosaic virus (MYMV): a threat to green gram (Vigna radiata)

production in Asia

A. Karthikeyana*y, V.G. Shobhanaay, M. Sudhaay, M. Raveendrana, N. Senthila, M. Pandiyanb and P. Nagarajana

aDepartment of Plant Molecular Biology & Biotechnology, Centre for Plant Molecular Biology, Tamil Nadu Agricultural University,Coimbatore, India; bNational Pulse Research Centre, Tamil Nadu Agricultural University Vamban, Pudukkottai, India

(Received 28 February 2014; final version received 17 October 2014)

Mungbean yellow mosaic virus (MYMV) disease is one of the most vicious diseases of green gram and has been renownedin India for more than five decades. It is caused by a group of geminiviruses belonging to the genus, begomovirus of thefamily, Geminiviridae. They are transmitted through whitefly in a persistent manner. The economic losses due to this virusaccount up to 85% in green gram which is spreading faster towards newer areas. The escalating economic importance ofMYMV has resulted in the call for accurate detection and identification procedures that inspire rigorous research effortsfocussing on the biology, diversity and epidemiology of the virus, so that viable management strategies could be designed.Breeding for resistance or tolerance appears to be the best approach to control this disease. However, the commerciallyoffered genotypes are only partially resistant. Therefore, the hunt for newer sources of disease resistance needs to beintensified. This review updates all the accessible information on MYMV and outlines the areas in which advance researchis indispensable.

Keywords: Begomoviruses; mungbean yellow mosaic virus; Vigna radiata; whitefly

1. Introduction

Vigna radiata (L.) Wilczek, commonly known as green

gram or mungbean (originated in India or the Indo-

Burmese region), is a vital crop grown throughout Asia,

Australia, West Indies, South and North America, tropical

and subtropical Africa. It is well suited to a large number

of cropping systems and constitutes an important source

of cereal based diets, worldwide, covering more than six

million hectares per annum. However, Asia, alone,

accounts for 90% of world’s mungbean production. India

is the world’s largest mungbean producer accounting for

about 65% of world’s acreage and 54% of its global pro-

duction (Singh 2011). Mungbean contains carbohydrate

(51%), protein (24%�26%), minerals (4%) and vitamins

(3%). Besides, it has the remarkable quality of serving the

symbiotic root rhizobia to fix atmospheric nitrogen and

hence, augments soil fertility. Due to the importance of

mungbean in Asian countries, the World Vegetable Center

(formerly known as, Asian Vegetable Research and

Development Center � AVRDC) has been actively work-

ing on mungbean for the past four decades. Prior to incep-

tion of AVRDC, national partners in mungbean producing

countries released more than 100 improved mungbean

cultivars for yield and resistance against pests and dis-

eases in South and South East Asia and most parts of the

world (Somta et al. 2009). The standard worldwide yield

of mungbean is very low (384 kg/ha) and its production

has not considerably increased yet. The main reason for

the low yield is the susceptibility of the crop to insects,

weeds and diseases caused by fungus, virus or bacteria.

Among the three, the viruses are the most important group

of plant pathogens affecting the production of the crop.

They cause severe diseases and economic losses in mung-

bean by plummeting seed yield and quality (Kang et al.

2005). Mungbean yellow mosaic disease is transmitted by

the vector, the whitefly (Bemisia tabaci). It is found to

spread the begomoviruses, the major hazard to the flour-

ishing production of mungbean in India, Sri Lanka, Paki-

stan, Bangladesh, Papu New Guinea, Philippines and

Thailand (Honda et al. 1983; Chenulu & Verma 1988;

Varma et al. 1992; Jones 2003; Haq et al. 2011a). Based

on 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 MYMD in different

regions of the world (Qazi et al. 2007; Malathi & John

2008a; Ilyas et al. 2010). The most conspicuous symptom

on the foliage starts as small yellow specks along the vein-

lets and spreads over the lamina; the pods become thin

and curl upwards. Extensive records from the past showed

that the disease occurs with different intensities in all of

the mungbean producing areas in and around Asia.

Depending on the severity of the disease infection, the

yield penalty may reach up to 85%. Quite a lot of disease

management strategies have been developed or imple-

mented for MYMV disease and so far, no complete resis-

tance to this disease has been incorporated into any of the

commercially available mungbean cultivars. The disease

still poses a major crisis to the economic production of

*Corresponding author. Email: [email protected] A. Karthikeyan, V.G. Shobhana and M. Sudha contributed equally on this work.

� 2014 Taylor & Francis

International Journal of Pest Management, 2014

Vol. 60, No. 4, 314�324, http://dx.doi.org/10.1080/09670874.2014.982230

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this crop in the Asian subcontinent. This review considers

the understanding of the MYMV disease and highlights

the urging scope to promote further research.

2. Historical perspectives and distribution

Capoor and Varma (1948) of India were the first to report

yellow mosaic disease of lima bean (Phaseolus lunatus)

and later in Dolichos (Capoor & Varma 1950). In the mid-

dle of 1950, it was noted that the experimental host range

of yellow mosaic disease (YMD) included numerous vari-

eties of all groups of legumes. It was first identified as a

problem in a mungbean field in India in 1955, at the

experimental farm of the Indian Agricultural Research

Institute, New Delhi. Nariani (1960) first described the

yellow mosaic disease on mungbean and linked it with the

virus. Nene (1968) named the virus as MYMV. After the

initial discovery of MYMV disease in India, other coun-

tries also confirmed its presence in their own territories. It

was confirmed in Pakistan (Ahmad 1975), Bangladesh

(Jalaluddin & Shaikh 1981), Thailand (Thongmeearkom

et al. 1981) and Sri Lanka (Shivanathan 1977). The distri-

bution of MYMV in Asia has been illustrated in Figure 1.

Between 1960 and 1980, most of the MYMD research

was involved on managing the disease and so, more often,

was based on the interaction of the vector population with

insecticides, and resistance breeding. Studies were

performed (1970) to find out the chief vector of MYMV

and white fly (Bemisia tabaci) was identified as the most

prime vector at least in the Asian subcontinent. Muruge-

san and Chelliah (1977) reported a yellow mosaic on

green gram which was higher during the months of March

to May (summer season). The increased disease incidence

might be attributed to the higher temperatures that were

prevalent in summer season, which was favourable for the

vector to develop and multiply. Thongmeearkom et al.

(1981) were the first research group to see the MYMV

particles in the leaf cells of Vigna radiata. MYMV was

first purified by Honda et al. (1983). Various workers

reported that the inheritance of resistance to the MYMV

is controlled by a few set of genes (recessive gene (Singh

& Patel 1977), a dominant gene (Sandhu et al. 1985),

complementary recessive genes (Shukla & Pandya 1985)

and two recessive genes (Verma & Singh 1988)). In 1990,

MYMV had emerged as a great menace in mungbean pro-

duction. The disease incidence was as high as 100% in the

fields of farmers in the Asian subcontinent, often resulting

in considerable yield losses (Varma et al. 1992). There-

fore, in 1990s, AVRDC has accorded the high-priority

mungbean improvement programmes and they started to

work on the objective of incorporating the resistant genes

for MYMV into the advanced breeding lines. The first

complete sequence of an MYMD virus was isolated from

mungbean reported by Morinaga et al. (1993). The genes

Figure 1. Distribution of mungbean yellow mosaic disease (MYMD) in Asia.

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of MYMV were mapped using different mungbean popu-

lations (Shanmugasundaram 1996). These genes will be

the first targets of marker-assisted breeding with random

fragment length polymorphism (RFLP) markers. In north-

ern Thailand, a severe outbreak of MYMD in mungbean

occurred in 1997. This caused major losses to production

and initiated a shift in cropping practices. Due to occur-

rence of mungbean yellow mosaic disease, improvement

in production and productivity of mungbean is becoming

tricky and the disease is a major problem in Asian coun-

tries (Varma & Malathi 2003). Most of the reported resis-

tance screening to date has been done only in India and

Pakistan (Malathi et al. 2005).

2.1. A begomovirus associated with mungbean yellow

mosaic disease

MYMV disease is caused by begomoviruses, popularly rec-

ognized as geminiviruses which are the leading and the

most significant genus within the family, Geminiviridae.

They are plant-infecting single-stranded DNA viruses and

have archetypal geminate incomplete icosahedral particles.

They are branded as monopartite (a single DNA) or a bipar-

tite (with two DNA components: DNA-A and DNA-B)

(Figure 2), based on their genome organization (Mansoor

et al. 2003; Jeske 2009), infecting mostly dicotyledonous

plants like mungbean, urdbean and soybean (Haq et al.

2011a). The two DNA components namely, DNA-A and

DNA-B, are roughly 2.8 kb in size (Borah & Dasgupta

2012). Bipartite begomoviruses, namely MYMIV, MYMV

and horsegram yellow mosaic virus (HgYMV), are accepted

as causal agents of MYMD in different regions of the world

(Qazi et al. 2007; Malathi & John 2008a; Ilyas et al. 2010).

Of all these viruses, HgYMV is the least studied. Its com-

plete sequence is available in the databases but no detailed

studies are conducted on this virus. The other two pathogens

namely, MYMV and MYMIV, occur across the Indian sub-

continent. Among the two, MYMV was studied extensively

and was reported from Thailand. The northern, central and

eastern regions of India are dominated by MYMIV infesta-

tions (Usharani et al. 2004) but MYMV is more ubiquitous

in the southern (Karthikeyan et al. 2004; Girish & Usha

2005) and western regions of the country. The viral

genomes consist of two circular single-stranded DNA

components (DNA-A and DNA-B) which are about 2800

nucleotides in length (Qazi et al. 2007). The isolates of the

larger DNA of the two components (the DNA-A) of

MYMIV and MYMV share only 82% identity between their

DNA sequences and so justify their separation into distinct

species. There are numerous DNA-B components associated

with yellow mosaic viruses (John et al. 2008). The cognate

DNA-Bs of groups (i), (iii) and (iv) represent MYMIV,

MYMV and HgYMV. The second group of DNA-B compo-

nents are associated with either MYMV or MYMIV. These

are closely associated to each other. They are more related

to MYMIV than to MYMV (92%). DNA-A is involved in

various nuclear functions. It encodes for all the factors

required for viral DNA replication (the replication associ-

ated protein (Rep; a rolling-circle replication-initiator pro-

tein) and DNA helicase (Choudhury et al. 2006) and the

replication enhancer protein (REn), regulation of gene

expression (the transcriptional activator protein (TrAP)) and

encapsidation/insect transmission [the coat protein (CP))).

The functions of the V2 and C4 proteins remain unclear. In

other begomoviruses, these two proteins have been shown

to have a possible role in movement and overcoming plant

host defences mediated by post-transcriptional gene silenc-

ing (PTGS). In MYMIV, the AC5 protein, encoded by a

gene (not well conserved between the begomoviruses) has

been shown to have a potential function in the viral DNA

replication (Raghavan et al. 2004). The DNA-B component

encodes two genes. They are the nuclear shuttle protein

(NSP) and the movement protein (MP) act together to move

the virus from one cell to the other within the plant. In depth

analysis of the gene expression, studies of MYMV have

shown the splicing of transcripts in a begomovirus for the

first time (Shivaprasad et al. 2005).

2.2. Transmission and epidemiology of disease

MYMV disease is transmitted principally by the polypha-

gous pest Bemisia tabaci (Figure 3) in a persistent (circu-

lative) manner and grafting but not by sap, seed or soil.

The latent period of whitefly is less than four hours, so it

is a tremendously efficient vector for virus transmission.

A single viruliferous adult is capable of transmitting the

dreadful virus and it can transmit the virus within an

acquisition and inoculation access period of 24 hours.

Acquisition and inoculation by whitefly adults can be

affected in a minimum of 15 minutes. The insect may

attain the virus after a single bite and its transmission

Figure 2. (Color online) Genome organization of bipartitebegomovirus � DNA-A and DNA-B.

Figure 3. (Color online) Polyphagous vector � whitefly(Bemisa tabaci).

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efficiency increases with time on the source plant of virus

as well as on the healthy mungbean plant (Malathi & John

2008a). The most efficient female and male adults in a

population can retain infectivity for 10 and 3 days, respec-

tively. Thus, the female adults are three times more effi-

cient as vectors than males. Neither female nor male

adults can retain infectivity throughout their life span.

Nymphs of B. tabaci can acquire the virus from diseased

leaves and the virus does not pass through eggs of B.

tabaci. Nevertheless, the cropping seasons highly influ-

ence the vector population. Whitefly is found to be high

during summer season compared to spring and rainy sea-

sons. They thrive best under hot and humid conditions

and the population also towers with higher temperatures.

Moreover, the spread of MYMV on a local (within and

between fields) and a regional basis reflects its dispersal.

Its population is correlated with disease incidence. High

populations appear on the crop that are 20�30 days old

leading to higher disease incidence (on the 45th day).

Spring and rainy seasons attribute to unfavourable condi-

tions for the multiplication of the whitefly. Therefore, the

disease incidence is not high during those seasons. Nath

(1994) studied the effect of the weather parameters on the

population of whitefly and the incidence of yellow mosaic

virus on green gram. He reported a simple positive signifi-

cant correlation between the disease incidence and the

population of the fly, temperature, the relative humidity,

rainfall and the number of rainy days necessary for the

infection. Honda et al. (1983) reported the mechanical

transmission of the isolate of MYMV of Thailand and

they obtained the highest transmission rates with 0.1 M

potassium or sodium phosphate buffer of pH�7.8. There-

after no one reported any infestation caused by mechani-

cal transmission. Attempts were made by Grewal (1988)

to transmit the disease by sap inoculation by rubbing

freshly extracted sap of mosaic affected leaves on the

healthy young seedlings of mungbean. However, the dis-

ease could not be transmitted in this manner.

2.3. Impact of MYMD infection on mungbean

Each group of the virus isolates (genetically distinct

strains, reassortants and recombinants) may have a differ-

ent level of stability or virulence, as reflected by the sever-

ity of the symptom in each line of mungbean. The whitefly

delivers the virus through proboscis to the phloem cells of

the host plant where it gets multiplied. In leaf cells, the

virus particles often form loose aggregates that sometimes

fill the nuclei of infected phloem cells. In mungbean,

hypertrophied nucleoli, aggregates of virus particles and

fibrillar bodies appear in the nuclei of phloem cells as

early as two days before the appearance of the symptom.

Virus particles are often scattered in distribution but occa-

sionally form aggregates having a paracrystalline or dou-

ble cylindrical arrangement in the vacuoles of infected

sieve elements (Thongmeearkom et al. 1981). It causes

yellow-coloured spots scattered on young leaves followed

by yellow mosaic pattern. Later, the spots gradually

increase in size resulting in complete yellowing of leaves

(Figure 4). The yellow leaves slowly dry and wither.

Infected plants bear few flowers and pods with some

immature and deformed seeds, thus affecting the yield

both qualitatively and quantitatively. Pods of the infected

plants are reduced in size and turn yellow in colour. In

severe cases, other plant parts become completely yellow

(Figure 4). Disease infection decreases the photosynthetic

efficiency and as a consequence the yield of the crop is

affected (Malathi & John 2008b). The economic impact

of MYMV on yield depends upon the time of virus

infection and is related to the plant development. Early

infection by the virus gives the highest reduction in yield.

If the infection occurs after three weeks from planting,

then the yield loss surmounts to 100%. However, the

losses will be meagre if infestation occurs after eight

weeks from planting. Over a broad geographic range, the

yield reductions between 10% and 85% have been

reported (Grewal JS 1988; Varma et al. 1992; Khattak

et al. 2000; Varma & Malathi 2003; Kang et al. 2005).

2.4. Source of inoculum for disease development

MYMV disease causes heavy damage when infection

occurs in early growth stages in mungbean (Varma &

Malathi 2003). Therefore, elimination of the primary

sources of inoculums will facilitate disease management.

This is particularly so in view of the lack of commercial

cultivars with MYMV resistance. Perennial weeds and

summer whitefly are potential sources of MYMV during

the early growth stages (Malathi & John 2008b; Ilyas

et al. 2009; Akthar et al. 2011; Ara et al. 2012). Roles of

whitefly and weed reservoirs (alternate hosts) in the epide-

miology of MYMV are yet to be critically assessed. The

potential for disease control through management of the

whitefly will be enhanced by accurate identification of

source(s). The increased disease incidence might be attrib-

uted to the higher temperatures prevalent during summer

season, which was favourable for the whitefly to develop

and multiply. The only concern might be that infected tol-

erant plants could remain as the sources of virus inocu-

lum, as well as promoting the adaptation of the virus to

overcome resistance. The agriculturally significant hosts

of MYMV include mungbean and urdbean (V. mungo),

mothbean (V. aconitifolia), pigeon pea (Cajanus cajan),

soybean (Glycine max), cowpea (V. unguiculata) and

common bean (Phaseolus vulgaris) (Varma et al. 1992;

Usharani et al. 2004; Karthikeyan et al. 2004; Malathi

et al. 2005; Qazi et al. 2007). Alternatively, other legumi-

nous hosts may provide a means for the virus and

could serve as virus reservoirs. In India, wild V. species,

namely, V. hainiana and V. trilobata, have recently been

established to be naturally infected with MYMIV

(Naimuddin & Aditya 2011).

2.5. Options for disease management

In general, strategies for controlling MYMV disease

include the following: planting resistant or tolerant varie-

ties, insect vector management, managing with alternative

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weed or crop hosts of viruses and changing crop cultural

practices to those less favourable for disease development.

2.6. Vector management

Plummeting the whitefly populations (vector) is an effec-

tive strategy to administer MYMV disease. At the same

time, the management of whiteflies is very complex

because whitefly does not go round in ones or twos but

they go round in hordes of hundreds and even one attack

can severely weaken a plant. They are not well controlled

by any of the available management practices such as cul-

tural, mechanical, botanical and chemical. Among the

various methods of whitefly management, chemical con-

trol is the primary method adopted. Systemic chemical

insecticides viz., acetamiprid, ethion, imidachlorpid, tria-

zophos, provide better control of whiteflies; they also kill

on contact, but are also taken inside the plant where they

go onto protect against further attack for more than a few

weeks (Wang et al. 2009). Younger stages are generally

more sensitive to insecticides as compared to older stages

and higher toxic levels of certain insecticides work well

against the first and second instar nymph stages. Nymphs

of whitefly are more susceptible to insecticides; failure in

control in crop fields may be due to the incomplete expo-

sure on the underside of leaves (to the insecticides) where

nymphs are present. Ghosh (2008) showed that imidaclo-

prid reduced the whitefly populations to significant levels,

if the insecticidal treatments are directed on the underside

of the leaves, preventing the spread of MYMV and

achieved more seed yield. Basal application of botanical

insecticides controls the whitefly population in plants.

Application of neem seed kernel extract (NSKE) and

foliar spray of neem oil had a major impact by preventing

the “nymphal” stage from developing into an adult; the

nymphs tend to disappear from the treated plants (Dubey

et al. 2011). Whitefly management should be achieved

when their population is lower through cultural practices.

Maintenance of good field sanitation by destroying and

removing the crop residues and weeds is an effectual prac-

tice against whiteflies. Exclusion of leaves by hands in

plants profoundly infested with the non-mobile nymphal

and pupal stages may trim down populations to levels that

natural enemies can contain. Water sprays (syringing)

may also be useful in dislodging adults. Avoiding a lot of

nitrogen fertilizer, including manures, is advised as

Figure 4. (Color online) Symptoms exhibited by mungbean plants infected with mungbean yellow mosaic virus: (A) healthy plants inthe field, (B) plant showing symptoms in young leaves, (C) yellow mosaic symptom in matured plants with fewer pods, (D) infectedpods and (E) MYMD-infected field.

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succulent growth will amplify whitefly populations. Other

methods to control whitefly populations resourcefully

without environmental spoil can however be a useful

component in the development of sustainable disease

control.

2.7. Breeding for resistance

Breeding for resistance to MYMV disease has been known

to virologists and plant breeders since 1970. It is largely

advocated as the key scheme for the control of MYMV in

mungbean. The bringing into play of host resistance is

most effectual, easy on the pocket and ecological for man-

aging MYMV. Upon infection, the susceptible (virus read-

ily infects and/or replicates and/or invades) or resistant

(virus infection and/or replication and/or invasion is

restricted) plant reactions show a range of tolerance or sen-

sitivity. Resistance to MYMV was visualized by symptom-

atology. Symptomless lines were assumed to be resistant.

In a few circumstances, some germplasms of mungbean

showed no symptoms even after infection. Hence, these

lines could not be used as resistant lines. Screening of

germplasm will hopefully reveal the resistance genes. In

the absence of a true source of resistance, these lines could

be used as tolerant lines. The levels of tolerance among

lines vary among the available germplasm and several dif-

ferences in response have been identified among various

germplasm sources. Resistance in mungbean germplasm

against MYMV has been recognized earlier by different

workers by using a common acceptable scale based on the

severity of the disease (Marappa et al. 2003; Peerajade

et al. 2004; Khattak et al. 2008; Iqbal et al. 2011; Pandur-

anga et al. 2011). However, it is crucial that the germplasm

evaluation considers the diversity among the various strains

of the virus too. For breeding resistant cultivars, informa-

tion on the inheritance and sources of resistance genes is

very important. Several resistance sources have been

reported for MYMV disease. The inheritance of resistance

to MYMV (in the intraspecific as well as in the interspe-

cific crosses) has been reported in mungbean and is con-

ferred by a single recessive gene (Reddy & Singh 1995;

Saleem et al. 1998; Reddy 2009), a dominant gene (Sandhu

et al. 1985), two recessive genes (Verma & Singh 1988;

Ammavasai et al. 2004) and complementary recessive

genes (Shukla & Pandya 1985). Commonly, intraspecific

hybridization is used for the improvement of resistance to

MYMV in mungbean. Resistance to MYMV has also been

recognized in the wild species (V. umbellata and V. sublo-

bata) of mungbean and may consent the introduction of

such resistance by means of interspecific hybridization

(Monika et al. 2001; Bisht et al. 2005; Pandiyan et al.

2008; Sudha et al. 2013a). Through the practices of intra-

and inter-specific hybridization, several promising lines

which are not only tolerance/resistance to MYMV but are

also high yielding have been developed and released for

commercial cultivation (Reddy & Singh 1995; Saleem

et al. 1998). However, this has been attributed to the

increased disease infestation and whitefly populations and

unstable levels of resistance. Due to the rapid explosion of

new isolates of MYMV, the understanding of its molecular

mechanism through conventional breeding approaches has

become very tricky and time consuming. Under such cir-

cumstances, a combination of plant breeding approaches

along with the traditional methods becomes obligatory for

the development of the resistant lines.

2.8. Marker-assisted selection (MAS)

The development of DNA markers (RFLP, random ampli-

fied polymorphic DNA (RAPD) markers, inter simple

sequence repeat (ISSR), simple sequence repeat (SSR),

single-nucleotide polymorphism (SNP)) has irreversibly

changed the disciplines of plant genetics and breeding.

While there are several applications of DNA markers in

breeding, the most promising for cultivar development is

called marker-assisted selection (MAS). Studying the

diversity among the germplasms, finding the linked

marker for resistant gene and construction of QTL maps

through molecular markers, has increased the efficiency

in the breeding programmes conferring resistance for

MYMV (Sudha et al. 2013a). By determining the allele of

a DNA marker, plants that possess particular genes or

quantitative trait loci (QTLs) may be identified based on

their genotype rather than their phenotype. Different

markers are used to study genetic diversity (Chattopad-

hyay et al. 2005; Roopa et al. 2008; Zhao et al. 2010;

Datta et al. 2012; Raturi et al. 2012; Zhong et al. 2012)

and tag the MYMV resistance genes in mungbean (Selvi

et al. 2006; Chen et al. 2012; Karthikeyan et al. 2012;

Dhole & Kanda 2013; Sudha et al. 2013a). MAS, to a

great extent, has improved the efficiency of resistance

breeding in MYMV and has shown some significant suc-

cess too. New sources of resistance to MYMV, for exam-

ple, the use of donors from interspecific sources, have

been identified and newer molecular markers linked to

resistance genes are becoming more accessible these days

(Maiti et al. 2011; Chen et al. 2012). These resistant geno-

types will be tested to conclude whether they are able to

offer good shield against the major strains of both MYMV

and MYMIV in hot spot regions.

2.9. Pathogen-derived resistance

Diverse transgenic mechanisms have been developed for

engineering virus resistance in crops. In the midst of all of

them, pathogen-derived resistance (PDR) is considered as

one of the best options offered for crop protection. In the

absence of resistance in the commercial mungbean culti-

vars, researchers have resorted to transgenic resistance

utilizing PDR. The concept of PDR, first proposed by

Sanford and Johnston 1985, has been successfully utilized

over the past 17 years to confer resistance against viruses

in many crop plants (Di et al. 1996; Chellappan et al.

2004; Zhang et al. 2013). The expression of viral genes in

the host plant and the subsequent disruption of the essen-

tial pathogenic processes to confer resistance are referred

to as PDR. PDR has been attained, by expressing various

forms of functional or dysfunctional viral CP, replicase,

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protease and MP genes inside the host plants. The pheno-

types resulting out of PDR-mediated protection exhibit

various conspicuous characters such as delayed develop-

ment of symptoms, reduced symptoms, and virion accu-

mulation to apparent immunity. The variety of PDR

phenotypes suggests multiple mechanisms underlying the

resistance that is attained. For example, the expression of

full-length and truncated REP genes from MYMV iso-

lated in tobacco plants showed an inhibition of viral repli-

cation in transgenic tobacco (Shivaprasad et al. 2006).

The resistance generated by the use of REP sequences is

very tight; a high dosage of input virus can be resisted eas-

ily by the transgenic plant. The PDR can also be achieved

without the expression of such proteins through mecha-

nism of gene silencing and antisense RNA. In blackgram,

DNA-A bidirectional promoter from MYMV has been

used in a transient assay to activate PTGS against yellow

mosaic virus but the transgenic plant did not show any

resistance reaction (Pooggin et al. 2003). Haq et al. (2010)

reported that the plants inoculated with infectious

MYMIV clones showed 64% infection in mungbean.

Those clones contain the complementary-sense gene

(ACI) encoding replication initiation protein (Rep) which

helps in the development of resistance against MYMIV.

At the same time in the plants co-inoculated with the Anti-

Rep construct, the symptom severity as well as the per-

centage of infection was almost negligible. It was only

20% in mungbean plants. The mungbean co-inoculated

with antisense construct showed 44% reduction in infec-

tivity. The symptoms were attenuated and the plants

almost appeared healthy. CP deletion (N0 terminal dele-

tion of 75 and 150 amino acids) showed the mutation of

MYMIV. It affected the systemic spread and pathogenic-

ity in mungbean (Haq et al. 2011b). The hairpin constructs

of CP has 35s promoter (1.3 kb) with the sense sequence

of MYMIV (130 bp), followed by an intron (741 bp), after

which the antisense (130 bp) target sequence with the

OCS terminator (765 bp) are placed and cloned in a clon-

ing vector called Phannibal. The results indicate that co-

agroinoculation of the CP hairpin construct (Cphp) pre-

vented the viral pathogenesis (Kumari & Malathi 2012).

Screening the germplasms using different MYMV isolates

through agroinoculation technique is the effective method

for assessing the genetic diversity for MYMV resistance

in mungbean (Karthikeyan et al. 2011). Recently, Sudha

et al. (2013b) screened the mungbean germplasms using

two different MYMV isolates. The results show that

among the seventy eight mungbean genotypes screened,

four genotypes exhibited resistance to the isolates of

MYMV.

2.10. Current status and challenges in managing

MYMV

The available evidence gathered since the 1960s suggests

that the diversity of crop plants and the geographical area

affected by the incidence of MYMV disease in mungbean

have increased gradually. This can be attributed to an

increase in the intensity of farming which requires

sustaining with the increasing population of southern

Asia, so particularly in India. MYMV disease is the result

of a three-way interaction between the host, the pathogen

and the environment (Singh et al. 2004). An epidemic

develops only if all the three of these factors are favour-

able. Therefore, the disease can be controlled by the nega-

tive manipulation of one or more of these factors so that

conditions become unsuitable for replication, survival or

infection by the pathogen. The control of the losses due to

MYMV disease requires the amalgamation of methods

aiming at preventing or delaying the infection of crop. All

the resistance found in mungbean, to date, appears to be

only the tolerance against the infection (infection with

mild symptoms) rather than complete immunity.

Recently, AVRDC released lines NM 92 and NM 94

which are known for their resistance to MYMV. NM 94

shows resistance to the disease during the summer season,

but is susceptible during the kharif (June�July sowing)

season. Resistance has been attributed to various factors,

including increase in disease and whitefly populations,

and unstable levels of resistance (Nair et al. 2013). It

shows that available strategies have not been enough and

they are not able to control the disease and develop resis-

tance: breeding methods are used to understand the differ-

ent responses of the cultivars under the attack of the

pathogen in the field. Knowing the molecular mechanism

of virus and developing the resistant lines for every infec-

tious virus strain are some major challenges. Meanwhile,

considering the vector management option, reduction of

vector populations in the field has been proven to be diffi-

cult and is, as yet, seldom used in yellow mosaic virus dis-

ease. Besides, control of vectors does not put a selection

pressure on the virus to evolve to higher plant virus titre

and at the same time increases the density of healthy

plants. Thus, vector control has a small risk of failure due

to selection for more damaging strains of the virus. In

recent times, the use of molecular biotechnological

approaches such as MAS and genetic engineering for

developing the resistance against MYMV disease has

shown greater triumph. However, supplementary research

is required on these areas to succeed in MYMD studies.

3. Future research direction

The prime goal of classifying the MYMV strains is to

carry out a fundamental and applied research so as to dis-

sect its genetic diversity. A universally accepted, uniform

set of differentiation for the strains of this virus has not

yet been developed anywhere in the world. Due to the

non-homogeneous classifications of virus strains, the

establishment of breeding programmes for resistance to

disease is not well-built, but, instead, has only led to the

rise of confusions among the breeders of mungbean. The

identification of resistance sources, exchange of resistance

information and utilization of the germplasm resources

are still indistinct. A uniform differential system is needed

for identifying strains so that scientists can exchange

information and resistance germ materials based on that

standard classification. Additionally, the determination of

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the population structure of the pathogen from a wider geo-

graphic area is required in order to develop a database on

virus isolates and consequently determine the best strat-

egy for the deployment of resistance and or to incorporate

the non-matching resistance genes to the existing patho-

gen. Genome research is not well developed in mungbean.

Although some progress in genome research has been

made in mungbean, it is still far behind the other major

legume crops such as soybean, cowpea, urdbean and com-

mon bean, or even with comparison with one of its rela-

tive, but the less economically important, azuki bean. A

variety of genomic resources like markers, e.g. RFLPs,

RAPDs, AFLPs, SSRs and ISSRs, have been developed to

speed up the MAS by discerning the genetic diversity and

finding the linked markers for the MYMV resistant gene

in mungbean so far; but no map contains enough number

of markers to resolve all the 11 linkage groups.

Tagging and mapping of genes and QTLs resistant to

MYMV use markers of other related legume such as azuki

bean, common bean, cowpea and soybean. However, in all

such marker programmes, either the markers are not

closely linked to the trait (>5 cM), or proper linkage or

validation studies were not performed. Therefore, an

urgent need to initiate development and validation of

tightly linked molecular markers for genes resistant to

MYMV has arisen. This could be rapidly transferred to

the susceptible mungbean genotypes through MAS. The

expressed sequence tags (ESTs) and genomic database of

the legumes of related genera or species will be supportive

in the development of high throughput markers such as

SSRs and SNPs. These resources have the potential to

develop a large number of markers especially SSRs and

SNPs that would enable to identify the genomic regions

(QTL) that underlie resistance to MYMV and on these

QTL regions the examination of the reference genome

will give the pipeline for identifying the candidate genes

responsible for MYMD resistance. Continuous efforts are

made in the production of BAC libraries in green gram

that would smooth the progress of the research in map-

based cloning of the genes and QTLs resistant to MYMV.

Furthermore, development of near-isogenic lines (NILs)

is suggested from a self-cross of residual hetero zygote

lines (RHLs) derived from recombinant inbred lines

(RILs) which is a useful and simple protocol for validat-

ing the QTLs. This also facilitated in the isolation of genes

identified as QTLs. This is because resistance against the

mungbean yellow mosaic disease is difficult to evaluate

under reproductive conditions in plants.

Furthermore, MYMV disease resistance in mungbean

has mainly concentrated on race-specific resistance. This

kind of resistance is conferred by genes with major effects

and recognized by their characteristic low-infection types.

A battery of resistance genes (R genes) are derived from

exotic germplasms which are used in this regard. In the

exploitation of wild relatives of mungbean, with a bal-

anced population design such as F2 or RILs, the problem

is that a large number of negative traits from the donor

parent will dominate the overall phenotype of the popula-

tion, hampering the detection of positive QTLs due to the

poor agronomic performance of the individuals (Anusuya

2009; Sudha 2009). Advanced backcross quantitative trait

locus (AB-QTL) is a competent method to utilize wild

species by the simultaneous discovery and transfer of

valuable QTLs with good agronomic performance from

unadapted germplasm into elite breeding lines (Tanksley

& Nelson 1996). The efficacy of the AB-QTL approach

has been tested in numerous crop species in various dis-

eases and has been proved to be a realistic method in crop

breeding (Liu et al. 2004; Naz et al. 2008; Schmalenbach

et al. 2008; Manosalva et al. 2009). The application of the

AB-QTL strategy in mungbean will identify the source

and beneficial alleles, and thus provides a means for quick

progress in developing improved virus resistant mungbean

lines. However, the development of the transgenic lines

resistant to MYMV and their incorporation/merging into

the commercial cultivars is a successful approach for the

development of the resistant varieties of MYMV in mung-

bean. The genetically engineering mungbean plants that

are resistant to viral pathogens have shown considerable

feat, which have paved way for improving the resistance

for MYMV in mungbean. The use of viral CP as a trans-

gene, exploitation of agroinoculation to screen the germ-

plasms using artificial isolates of MYMV and engineering

the disease resistance using RNAi are successful strategies

for producing disease-resistant plants but even more

research is vital in these areas. At last, we imply that the

development of resistance to MYMV is compulsory for

the flourishing production of mungbean. The early

attempts to control MYMD by conventional methods

have progressed only in field studies with a very little suc-

cess. Even later, it was unsuccessful in developing a resis-

tant variety due to rapid explosion of new isolates of

MYMV and also due to the complex mechanism that con-

trols the resistance reaction of MYMV. Advances in plant

molecular genetics now provide accurate gene detection

(R gene) for resistant lines and has a great promise to

assist plant breeders in understanding the molecular

mechanisms of the plant viruses. Recently, it shows some

success in the research groups involved in MYMV and

hence doing extensive research on these areas with wide

application of these technologies by the side of conven-

tional methods will be certainly powerful and promising

for the development of resistance reaction against the

virus.

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