MOLECULAR PLANT PATHOLOGY (2007) 8(4), 343–348
DOI: 10.1111/J.1364-3703.2007.00402.X
Pathogen profile Blackwell Publishing Ltd
Legume yellow mosaic viruses: genetically isolated begomoviruses J AVA R I A Q A Z I , M U H A M M A D I LYA S , S H A H I D M A N S O O R A N D R O B W. B R I D D O N * Plant Biotechnology Division, National Institute for Biotechnology and Genetic Engineering, Jhang Road, Faisalabad, Pakistan
S U M M A RY The yellow mosaic diseases of a number of legumes across Southern Asia are caused by four species of whitefly-transmitted geminiviruses (genus Begomovirus , family Geminiviridae): Mungbean yellow mosaic virus , Mungbean yellow mosaic India virus, Dolichos yellow mosaic virus and Horsegram yellow mosaic virus. They cause losses to a number of important pulse crops, a major source of dietary protein in the region. The viruses have host ranges limited to plants of the family Fabaceae and efforts to limit losses are hampered by limited availability of conventional resistance sources and/or the lack of durability of the resistance that has been identified. There is ample evidence for genetic interaction between these begomoviruses within the legumes, in the form of both classical recombination and component exchange, but little evidence for interaction with viruses that infect other plants. This is indicative of genetic isolation, the viruses in legumes evolving independently of the begomoviruses in plant species of other families. This has implications for the development of engineered resistance in legumes, which holds the promise of durability but has yet to be transferred to the field. Taxonomy: The viruses causing yellow mosaic diseases of legumes across southern Asia, four of which have been identified so far, are bipartite begomoviruses (genus Begomovirus, family Geminiviridae): Mungbean yellow mosaic virus, Mungbean yellow mosaic India virus, Horsegram yellow mosaic virus and Dolichos yellow mosaic virus. Physical properties: The legume yellow mosaic viruses (LYMVs), like all members of the Geminiviridae, have geminate (twinned) particles, 18–20 nm in diameter, 30 nm long, apparently consisting of two incomplete T = 1 icosahedra joined together in a structure with 22 pentameric capsomers and 110 identical protein subunits. Disease symptoms: Symptoms caused by LYMVs are largely dependent on host species and susceptibility. Initially symptoms appear as small yellow specks along the veins and then spread over the leaf. In severe infections the entire leaf may
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become chlorotic. In blackgram the chlorotic areas sometimes turn necrotic. Infections of French bean usually do not produce a mosaic but instead induce a downward leaf curling. Disease control: Control is based mainly on preventing the establishment of the whitefly vector, Bemisia tabaci, in the crop by application of insecticides. Changes in agricultural practices, such as moving the cropping period out of periods of high vector incidence (the wet period in late summer) to times of low vector incidence (dry season in early summer) have met with some, albeit short-term, benefits. The use of natural, host plant resistance is efficacious, although the available sources of resistance in most legume crops are limited. In mungbean the resistance is attributed to two recessive genes which are used effectively to control the disease. Useful websites: http://www.danforthcentre.org/iltab/geminiviridae/, http://www.iwglvv.org/
INTRODUCTION History of yellow mosaic disease of legumes in Southern Asia Yellow mosaic disease (YMD) was first reported from western India in the late 1940s in Lima bean and later in mungbean in northern India (Capoor and Varma, 1948; Nariani, 1960). Similarly, in the regions of the subcontinent now forming part of Pakistan, YMD was first reported in cowpea in the vicinity of Lyllpur (now known as Faisalabad; Vasudeva, 1942). Across the subcontinent, including India, Bangladesh, Pakistan and Sri Lanka, YMD is a major constraint to the production of most of the major legume crops. In Thailand YMD is a minor sporadic problem in legumes. However, in northern Thailand a severe outbreak of YMD in mungbean occurred in 1997. This caused major losses to production and initiated a shift in cropping practices. Since this time YMD has remained a minor problem and the first complete sequence of a YMD virus was isolated from mungbean originating from this country (Morinaga et al., 1993).
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Aetiology of YMD of legumes Four species of bipartite begomoviruses (family Geminiviridae) are at this time recognized as causing YMD of legumes in southern Asia. These viruses are closely related and have distinct but overlapping host ranges. Mungbean yellow mosaic virus (MYMV) and Mungbean yellow mosaic India virus (MYMIV) occur across the Indian subcontinent, with MYMV also reported from Thailand, and affect the majority of legume crops including mungbean (Vigna radiata), blackgram (Vigna mungo), pigeonpea (Cajanus cajan), soybean (Glycine max), mothbean (Vigna aconitifolia) and common bean (Phaseolus vulgaris). Additionally, MYMV is reported to infect yard-long bean ( Vigna sesquipedalis) and MYMIV Lablab purpureus. Dolichos yellow mosaic virus (DoYMV) has only recently been recognized as a distinct species of begomovirus (Maruthi et al., 2006). The virus is reported to have a very narrow host range consisting of only the host from which it was isolated, dolichos (Lablab purpureus). Horsegram yellow mosaic virus (HgYMV) is the least well characterized of the four viruses; a complete sequence is available in the databases but no publication has yet reported the infectivity or host range of the virus. This virus occurs in horsegram ( Macrotyloma uniflorum). Historically the virus is reported to affect a number of legume species, including Cajanus cajan, Glycine max, hairy indigo (Indigofera hirsute), Macrotyloma uniflorum, Phaseolus lunatus, P. vulgaris, V. mungo and V. radiata. This host range determination was conducted prior to full (sequence) characterization of the virus and, in view of the overlapping host ranges of the legume viruses, is not necessarily representative of the virus presently described as HgYMV. The four species of begomovirus causing YMD of legumes are typical bipartite begomoviruses, which we shall henceforth refer to as legume yellow mosaic viruses (LYMVs). Their genomes consist of two circular single-stranded DNA components (~2800 nucleotides in length; Fig. 1). The larger of the two components, known as DNA A, encodes all factors required for viral DNA replication [the replication associated protein (Rep; a rolling-circle replication-initiator protein 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, although for other begomoviruses they have been shown to have a possible role in movement and overcoming plant host defences mediated by post-transcriptional gene silencing (PTGS), respectively. For MYMIV the AC5 protein, encoded by a gene not well conserved between begomoviruses, has been shown to have a possible function in viral DNA replication (Raghavan et al., 2004). The DNA B component encodes two genes, the nuclear shuttle protein (NSP) and the movement protein (MP), which act cooperatively to move the virus cell-to-cell within plants.
Fig. 1 Genome arrangement of the components of LYMVs. The genomes consist of two ~2800 nucleotide components designated as DNA A and DNA B, which encode genes bidirectionally from an intergenic region that also contains a sequence of approx. 200 nucleotides, known as the common region (CR), which is highly conserved between the two components. The position and orientation of genes are denoted as arrows. Shown are the coat protein (CP), replication-associated protein (Rep), transcriptional activator protein (TrAP), replication enhancer (REn), nuclear shuttle protein (NSP) and movement protein (MP). The functions of the products of the AV1 and AC4 genes remain unclear. The product of AC5 has been implicated in viral DNA replication. The position of the conserved hairpin structure, containing the nonanucleotide sequence, within the CR is also shown.
A recent in-depth analysis of the gene expression strategy of MYMV has shown for the first time for a begomovirus splicing of transcripts (Shivaprasad et al., 2005). Well documented for mastreviruses, in being essential to express Rep (Wright et al., 1997), splicing in the case of MYMV occurs in the leader sequence of the MP, removing some potentially inhibitory sequences from the leader, which may up-regulate translation.
H O S T A DA P TAT I O N O F T H E L E G U M E Y E L L O W MOSAIC VIRUSES MYMV and MYMIV (the only LYMVs which have been studied in any detail) are unusual in having highly variable DNA B components. An isolate of MYMV obtained from blackgram (MYMV[IN:Vig]) was shown to be associated with two distinct types of DNA B. The first (KA27) showed 97% sequence identity to the DNA B of the MYMV isolate from Thailand. The other (represented by four clones, KA21, 22, 28 and 34) was only 71–72% identical to the Thai isolate (Karthikeyan et al., 2004). Infectivity analysis showed the DNA A component of this virus to be able to support both DNA B components at the same time and to induce only mild symptoms in blackgram in the presence of DNA KA27 but typical disease symptoms in this host in the presence of the other DNA B components. The authors suggested that the presence of two distinct DNA B components could allow an extended host range of the virus but did not show this experimentally. For an isolate of MYMIV (MYMIV-[Cp]) from cowpea, the presence of a distinct DNA B was shown to extend the host range of
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Fig. 2 Comparison of the phylogenetic trees of the DNA A (left) and DNA B (right) of LYMVs. Cognate DNA A and DNA B components are joined by lines and crossingover indicates likely pseudo-recombination. The trees were arbitrarily rooted on the sequences of the DNA A and DNA B components of Tomato leaf curl New Delhi virus, respectively. Numbers at nodes indicate bootstrap confidence scores (1000 replicates).
this virus to cowpea. These clones were not well adapted to blackgram, inducing severe symptoms but accumulating to only low levels in this species (Malathi et al., 2005). Furthermore, an isolate of MYMV isolated from soybean (MYMV-[IN:Mad:Sb]) is associated with a DNA B with high sequence identity to the DNA B of HgYMV (96%). The DNA B of HgYMV is the most distinct amongst the LYMV DNA Bs (Fig. 2), showing only 70–73% identity to the DNA B components of MYMV and MYMIV. These findings indicate that component exchange (so called pseudo-recombination) is common-place for the LYMVs (Fig. 2), both within and between species and is probably an adaptation allowing a change in host range. For bipartite begomoviruses the DNA A and DNA B components share a region of sequence (~200 nucleotides) with high sequence identity that contains the origin (ori) of virion-strand DNA replication. The ori consists of a conserved hairpin structure containing the ubiquitous (for geminiviruses) nonanucleotide motif (TAATATTAC; which is nicked by the virus-encoded Rep to initiate virion-sense, rolling-circle DNA replication) and repeated motifs (‘iterons’) that are the sequencespecific recognition sequences for Rep (Argüello-Astorga et al., 1994). The interaction between Rep and the iteron is highly specific, in most cases preventing interaction between components of distinct begomovirus species (Chatterji et al., 2000; Fontes et al., 1992, 1994; Orozco et al., 1998). Thus, the integrity of the bipartite
genomes of begomoviruses is maintained by each component having the same (or at least a closely related) ori containing the same iterons. MYMV, MYMIV and DoYMV (for which only DNA A sequences are available at this time) share similar iteron sequences (predicted to be GGTGT) whereas HGYMV has the predicted iteron motif GGTAT and would not be expected to be able readily to exchange components with the other LYMVs. However, component capture between distinct species does occur if, by recombination, the ori of DNA B is replaced by that of the DNA A (so-called ‘origin donation’). This appears to be the case for the HgYMV-like DNA B of MYMV-[IN:Mad:Sb], which contains the MYMV/MYMIV iteron motifs GGTGT (Girish and Usha, 2005). However, this isolate was also associated with a normal, MYMV DNA B (Fig. 2).
R E L AT I O N S H I P TO OT H E R B E G O M OV I R U S E S The four viruses infecting legumes in southern Asia are amongst the most unusual of the begomoviruses. They are distinct from the numerous legume-infecting begomoviruses that occur in the Americas (as are all Old World begomoviruses; Stanley et al., 2004). In phylogenetic analyses the LYMVs are always basal to the Old World begomoviruses (Padidam et al., 1995). This is a feature the LYMVs share with two other legume-infecting viruses, Cowpea golden mosaic virus (from Nigeria) and Soybean crinkle leaf virus
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[a monopartite begomovirus occurring in Thailand (Samretwanich et al., 2001)], as well as a group of monopartite viruses isolated from Ipomoea spp. (including sweetpotato), which are widespread and whose precise geographical origins remain unclear (Lotrakul et al., 2002). Recombination plays a defining role in the evolution of geminiviruses. The present taxonomic division of the Geminiviridae into four genera is in part attributable to recombination between progenitor viruses; for example, viruses of the genus Curtovirus, geminiviruses that are leafhopper-transmitted but with the replication genes more similar to the whitefly-transmitted geminiviruses, most likely result from a recombination event between an ancestral whitefly-transmitted geminivirus (donating the replication genes of these viruses) and an ancestral leafhopper-transmitted geminivirus (donating the coat protein that determines leafhopper transmissibility). Recombination continues to be the major driving force in geminivirus evolution and is particularly well documented for the begomoviruses (Padidam et al., 1999; Pita et al., 2001; Seal et al., 2006). The most prominent examples of the significance of geminivirus recombination to agriculture are the involvement of a recombinant strain of East African cassava mosaic virus (known as the ‘Uganda Variant’) in an ongoing pandemic of cassava mosaic disease in Africa, which also involves interspecific synergism between begomoviruses (Pita et al., 2001; Zhou et al., 1997), and the diversity of begomoviruses involved in the epidemic of cotton leaf curl disease which swept across Pakistan and north-western India during the 1990s (Sanz et al., 2000). For the LYMVs there is little evidence for recombination. Girish and Usha (2005) have shown some evidence for limited recombination between isolates of MYMIV. In addition, the component exchanges (a form of recombination) discussed in the previous section with its probable ‘origin donation’ indicate that the viruses within the legumes in southern Asia do interact, requiring the infection of a single cell with the two virus isolates or species, for classical recombination and component exchange, or at the very least a mixing of the two viruses in a single vector insect for component exchange. However, there is little, if any, evidence for the interaction of the LYMVs with viruses that do not infect legumes. This finding is unusual for begomoviruses. Most begomoviruses show extensive evidence of recombination between quite distinct species. The most prominent examples of this are the viruses involved in causing cotton leaf curl disease across Pakistan and India (Idris and Brown, 2002; Sanz et al., 1999, 2000) and the viruses causing tomato yellow leaf curl disease across the Mediterranean basin (García-Andrés et al., 2007). This lack of interaction with other begomoviruses is probably indicative of genetic isolation. The LYMVs, as far as has been determined, have a natural host range almost entirely within the legumes and for the most part the other begomoviruses in the region do not naturally infect legumes, and thus there is little opportunity for mixing other than possibly in the vector.
A similar case for genetic isolation might be made for the begomoviruses causing cassava mosaic disease in Africa. These show extensive recombination and component exchange within cassava but little evidence for interactions with viruses in other hosts, as well as having a very limited host range (Bull et al., 2006; Ndunguru et al., 2005). It is likely that the presence of a cassavaspecific vector biotype and co-adaptation between the virus and the insect vector also play a part. Whether these factors also play a part in the genetic isolation of the legume-infecting begomoviruses of southern Asia remains to be determined. The genetic isolation of these viruses clearly has implications for the development of resistance. Diversity is a strong counterindicator for the durability of resistance (García-Arenal and McDonald, 2003), either natural host plant resistance or engineered resistance, and the lack of diversity suggests that any resistance employed should be resilient.
FUTURE PROSPECTS The available evidence gathered since the 1940s suggests that the diversity of crops, as well as the geographical area affected by the yellow mosaic viruses of legumes, has increased. This can be attributed to an increase in the intensity of farming which has been required to sustain the increasing population of southern Asia, particularly so in India. Efforts to avoid, or at least reduce, losses due to these viruses by changing cropping patterns, such as growing the crop earlier to avoid the periods of high vector incidence, rapidly lead to earlier appearance of both the vector and the viruses in the field. The emergence of YMD of cowpea, which until the late 1970s was not affected by the disease, was attributed to the introduction of exotic, and highly susceptible, varieties from West Africa (Varma et al., 1992). This possibly led to the adaptation of both MYMIV (Malathi et al., 2005) and MYMV to this host. Subsequent to this even cowpea varieties not previously susceptible to YMD showed symptoms of infection. An unexpected recent development has been the identification of DNA β satellites in mungbean associated with MYMIV. The DNA β components are a recently identified group of circular, single-stranded DNA satellites associated with begomoviruses (Briddon and Stanley, 2006). The majority of DNA β are associated with monopartite begomoviruses. The satellite, for the majority of these viruses, although not strictly essential, is required to infect hosts efficiently and to induce symptoms. Possibly the satellite is required to overcome host plant defences by suppressing post-transcriptional gene silencing, a double-stranded RNA-mediated process which is believed to be part of a plant’s defences against foreign nucleic acids, including viruses (Dunoyer and Voinnet, 2005; Voinnet, 2001). Over the past few years, however, DNA β satellites have increasingly been identified in association with bipartite begomoviruses, specifically MYMIV (Rouhibakhsh and Malathi, 2005) and Tomato leaf curl New Delhi virus (a bipartite
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Fig. 3 Typical yellow mosaic symptoms of MYMIV in mungbean (a), mothbean (b), soybean (c), cowpea (d) and blackgram (e). The severe leaf curling and crumpling of a mungbean plant infected with MYMIV and a DNA β satellite is also shown (f).
virus occurring across the subcontinent in solanaceous hosts). For both these viruses, the presence of both the DNA β satellite and the DNA B of the virus causes more severe symptoms than either the DNA A and DNA B or the DNA A with the satellite (Dr V. G. Malathi, personal communication). For MYMIV, these symptoms include a severe leaf curl and crumpling (Fig. 3). Whether this tripartite aetiology will remain stable over time or whether these viruses will ultimately evolve by dispensing with DNA B is unclear. The association of DNA β with LYMVs needs a broader study to determine the precise nature of the interaction. In the absence of effective and stable host plant resistance to the LYMVs, efforts have been made to develop resistance to the viruses based on the concept of pathogen-derived resistance. The concept was shown to have promise in a transient assay system where blackgram plants experimentally infected with MYMV were biolistically inoculated with a construct designed to express a hairpin RNA spanning the promoter region of the DNA A of the virus (in the intergenic region) (Pooggin et al., 2003). Plants treated in this way recovered from the infection (becoming asymptomatic), although very low levels of viruses could be detected. It is likely that transgenic plants expressing such hairpin constructs will be useful in reducing losses to LYMVs in legumes. The only concern might be that infected tolerant plants could remain sources of virus inoculum, as well as promoting the adaptation of the virus to overcome the resistance.
AC K N O W L E D G E M E N T S M.I. was supported by the Higher Education Commission (HEC, Pakistan) under the ‘Indigenous 5000 Fellowship Scheme’. J.Q.
was supported by a research grant from the HEC. R.W.B. was supported by the HEC under the ‘Foreign Faculty Scheme’. The authors are grateful for the support of NIBGE.
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