Begomovirus disease complex: emerging threat to vegetable production systems of West and Central Africa
© Leke et al.; licensee BioMed Central. 2015
Received: 5 August 2014
Accepted: 16 December 2014
Published: 21 January 2015
Vegetables play a major role in the livelihoods of the rural poor in Africa. Among major constraints to vegetable production worldwide are diseases caused by a group of viruses belonging to the genus Begomovirus, family Geminiviridae. Begomoviruses are plant-infecting viruses, which are transmitted by the whitefly vector Bemisia tabaci and have been known to cause extreme yield reduction in a number of economically important vegetables around the world. Several begomoviruses have been detected infecting vegetable crops in West and Central Africa (WCA). Small single stranded circular molecules, alphasatellites and betasatellites, which are about half the size of their helper begomovirus genome, have also been detected in plants infected by begomoviruses. In WCA, B. tabaci has been associated with suspected begomovirus infections in many vegetable crops and weed species. Sequencing of viral genomes from crops such as okra resulted in the identification of two previously known begomovirus species (Cotton leaf curl Gezira virus and Okra yellow crinkle virus) as well as a new recombinant begomovirus species (Okra leaf curl Cameroon virus), a betasatellite (Cotton leaf curl Gezira betasatellite) and new alphasatellites. Tomato and pepper plants with leaf curling were shown to contain isolates of new begomoviruses, collectively referred to as West African tomato-infecting begomoviruses (WATIBs), new alphasatellites and betasatellites. To study the potential of weeds serving as begomovirus reservoirs, begomoviruses and satellites in the weed Ageratum conyzoides were characterized. Sequence analyses showed that they were infected by isolates of a new begomovirus (Ageratum leaf curl Cameroon virus) that belong to the WATIBs group, a new betasatellite (Ageratum leaf curl Cameroon betasatellite), an alphasatellite and two types of defective recombinants between a begomovirus and an alphasatellite. Putative recombinations were detected in begomovirus genomes for all four plant species studied, indicating that recombination is an important mechanism for their evolution. A close relationship between the begomoviruses infecting pepper and tomato and A. conyzoides and the detection of the same alphasatellite in them support the idea that weeds are important reservoirs for begomoviruses and their satellites. With this high diversity, recombination potential and transmission by B. tabaci, begomoviruses and ssDNA satellites pose a serious threat to crop production in West and Central Africa.
KeywordsBegomoviruses Okra leaf curl disease Whitefly Tomato leaf curl disease West and Central Africa Viral satellites
Genome organization of bipartite begomoviruses
Except for a short sequence of ~200 nts, referred to as the ‘common region’ (CR), the DNA-A and DNA-B components share no sequence similarity. The CR contains the nonanucleotide TAATATTAC sequence, where rolling circle replication is initiated, and that is conserved among members of the family Geminiviridae [10-12]. Both genomic components contain protein-coding sequences on the viral sense strand and on the complementary strand. Six genes seem to be universally present in all bipartite begomoviruses. The DNA-A component contains one gene (AV1) on the viral sense strand and three genes (AC1, AC2, AC3) on the complementary strand for the New World (NW) bipartite begomoviruses  and an additional gene AV2 in the viral sense strand and C4 on the complementary strand for the Old World (OW) bipartite begomoviruses . The sense and complementary strands of the DNA-B component each contains one gene, BV1 and BC1, respectively  (Figure 1A).
Genome organization of monopartite begomoviruses
The genome of monopartite begomoviruses contains six open reading frames (ORFs). The coat protein gene (CP or V1), and V2, are expressed from the viral sense strand, and C1 (replication-associated (activator) protein (Rep)), C2, C3, and C4, are expressed from the complementary strand  (Figure 1B).
DNA satellite molecules associated with monopartite begomoviruses
Satellites are defined as viruses or nucleic acids that depend on the helper virus for their replication but lack extensive nucleotide sequence identity to the helper virus and are dispensable for its proliferation . Satellite viruses encode a structural protein, which encapsidates its own nucleic acid, while satellite nucleic acids rely on the helper virus structural protein for encapsidation and do not necessarily encode additional non-structural proteins. A third type of agent, referred to as satellite-like nucleic acid, also depends on the helper virus for its replication but provides a function that is necessary for the biological success of the helper virus and is therefore considered as part of the helper virus genome . The first satellite RNA was identified in 1969 in association with the nepovirus Tobacco ringspot virus , and since then, a large number of satellite RNAs, associated with several groups of plant viruses, have been reported , with the majority of the satellites interfering with the replication of the helper viruses, resulting in attenuated symptoms. Some satellites exacerbate disease symptoms induced by the helper virus or produce novel symptoms which are usually not associated with the helper virus infections .
The first begomovirus satellite DNA to be discovered was found to be associated with the monopartite begomovirus Tomato leaf curl virus (ToLCV) from Australia . This 682 nt circular ssDNA depends on ToLCV for its replication and encapsidation, but its replication can also be supported by other begomoviruses. It has no proven effects on the viral replication or on symptoms caused by ToLCV. It has no extensive ORFs and has little sequence similarity to its helper virus (ToLCV) except for the nonanucleotide TAATATTAC sequence presents in the stem loop of all geminiviruses . Failure to reproduce yellow vein symptoms in Ageratum conyzoides (goat weed) by re-introduction of Ageratum yellow vein virus (AYVV) [22,23], suggested that another factor was required to restore pathogenicity in the natural host. In a search for additional viral components, a number of small circular recombinant components, each containing the AYVV origin of replication together with sequences of unknown origin, were isolated from infected goat weed . Similar recombinants were also identified for the begomoviruses associated with cotton leaf curl disease (CLCuD) [25-27]. The significance of the unidentified sequences within the recombinants was not appreciated at the time, but they were to provide a vital clue in the discovery of a new class of satellites. As was observed for AYVV, the cloned genomic component of cotton leaf curl virus (renamed Cotton leaf curl Multan virus, CLCuMV) failed to induce typical CLCuD symptoms, suggesting the presence of another factor , whose search resulted in the isolation of a small circular ssDNA molecule, referred to as DNA-1 , which is a representative of a new class of components associated with monopartite begomoviruses .
Recently, many monopartite begomoviruses have been identified that associate with a type of satellite molecule referred to as betasatellite, composed of ssDNA, ~1.3 kb in size and approximately half the size of the helper begomoviruses (Figure 1D). Many of the betasatellites are required for typical disease symptom development [22,27,30-33]. Despite their recent discovery, betasatellites may have existed for many centuries, e.g., Eupatorium yellow vein betasatellite.
(EpYVB) in association with Eupatorium yellow vein virus (EpYVV) have been demonstrated to cause eupatorium yellow vein disease (EpYVD), which was described about 1250 years ago . All betasatellites require a helper begomovirus for replication, local and systemic spread, and whitefly vector-mediated transmission, and some have been shown to modulate symptom severity . To further show the role that betasatellites play in begomoviral disease etiology, the βC1 (Figure 1D) has in one instance been shown to be responsible for the suppression of jasmonic acid signaling involved in at least one gene silencing pathway . The transgenic plants of Arabidopsis thaliana expressing βC1 of Tomato yellow leaf curl China betasatellite (TYLCCNB) were shown to develop disease symptoms like that observed in begomovirus-infected tobacco plants, in that plants exhibited upward leaf curling, foliar enations, and sterile flowers . All betasatellite molecules contain one ORF (βC1) (Figure 1D), an A-rich region ~240 nts long and a satellite-conserved region (SCR), of ~220 nts. Apart from the nonanucleotide sequence, betasatellites do not share any significant sequence similarity with the helper begomoviruses.
The begomovirus/betasatellite complexes are often associated with a second type of circular ssDNA satellite, initially referred to as DNA-1 [28,29,36,37], but now called alphasatellites . Alphasatellites encode a single protein that shares high nt identity with the Rep (Figure 1C), a rolling-circle replication initiator protein encoded by viruses in the genus Nanovirus, family Nanoviridae that also have a genome of circular ssDNA . Consequently, alphasatellites are capable of autonomous replication but require a helper begomovirus for spread in plants and for whitefly vector transmission. In addition to Rep, alphasatellites also have an A-rich region, ~200 nts long, downstream of the Rep-encoding region. Recently, it has been demonstrated that the alphasatellite associated with Tobacco curly shoot virus (TbCSV) can be used as a virus-induced gene silencing (VIGS) vector . In contrast to betasatellites, alphasatellites possess in their stem loop the nonanucleotide sequence TAGTATTAC which is also found in the stem loop of viruses in the family Nanoviridae. Alphasatellites can affect both begomovirus titer and symptom development in host plants [36,41]. Initially it was thought that satellite molecules were limited to the OW, but recently, alphasatellites have been found associated with NW begomoviruses [42,43], thus expanding the geographical distribution of satellite molecules associated with begomoviruses.
Diversity and distribution of begomoviruses and ssDNA satellites in West and Central Africa
In West and Central Africa, Bemisia tabaci has been associated with suspected begomovirus infections in many crop species, including cassava, bean, cotton, eggplant, pepper, squash, tomato, okra, and watermelon as well as weeds of the genera Ageratum, Asystasia, Clerodendrum, Emilia, and Malvastrum. This observation was based on the consistent presence of B. tabaci on plants exhibiting characteristic symptoms of begomovirus infection (leaf curling and distortion, green or yellow foliar mosaic, stunting, reduced yields). Thus, there is a pressing need for additional information on the diversity and distribution of begomoviruses and satellites in vegetable crops and/or dicotyledonous weeds, which likely serve as virus reservoirs. This review thus presents a tip of the iceberg on the diversity of begomoviruses and associated satellite DNAs infecting vegetable crops in West and Central Africa.
Economic impact of begomoviruses/ssDNA satellites on vegetable production systems and food security in West and Central Africa
Vegetables have been grown and utilized traditionally in most if not all of the African countries for home consumption and domestic markets. Of late, vegetable production has shifted from subsistence to include export markets representing an important driver for growth due to employment opportunities in production, processing, and trade. Vegetables have proven to be important rain-fed crops , and several advantages and potentials of vegetable production are still not being fully exploited.
With the rapid urbanization and population growth, market-oriented vegetable production is increasing in peri-urban areas and has considerable potential for earning foreign exchange, thus generating employment opportunities and income, improving food security, alleviating poverty, and enhancing development in the region. Vegetables account for an estimated 40% of the market sales of products in the region . Vegetables are mainly grown and traded by women in domestic markets with substantial regional market linkages . Increased and sustained growth in this sector will translate into more income for women and associated benefits for household nutrition and food security, health, and educational status of children .
Potential for control
The sustainable management of begomovirus diseases in West and Central Africa will depend on the use of an integrated pest management (IPM) approach. The use of resistant/tolerant cultivars is an important part of disease control as well as the use of different methods for limiting begomovirus spread by the whitefly vector. However, the breeding for resistance to begomoviruses is complicated by their high diversity, ability to form new genotypes by recombination, and the occurrence of DNA satellites.
The local tomato cultivars in West and Central Africa as well as old cultivars such as Moneymaker and Roma are susceptible to important diseases, including tomato leaf curl/tomato yellow leaf curl (ToLCD/TYLCD) [73,74]. Recently, tomato cultivars with resistance to begomoviruses have been widely adopted throughout the world. They are not immune to infection but may give an acceptable yield even when infected [75,76]. The resistance has been crossed into tomato from wild relatives . Common resistance genes in tomato are the allelic genes Ty-1 and Ty-3, which originate from accessions of Solanum chilense. These resistance genes have been cloned and found to encode an RNA-dependent RNA polymerase, and the resistance involves increased cytosine methylation of the viral genome . Field trials carried out in Mali under a high infection pressure of begomoviruses showed that breeding lines of tomato with the resistance genes Ty-1 and Ty-3 produced a higher yield than the commercial susceptible cultivars . In a recent survey, 41 tomato varieties from different sources were screened in the field in Senegal for resistance to TYLCD . The trial included also commercial varieties with resistance or tolerance to TYLCD. A substantial variability was observed with a disease incidence from 0% to 100% and a severity of 0% to 89%. Twelve genotypes were identified as having a high level of resistance and being suitable for cultivation under a high disease pressure. Similar studies were carried out simultaneously in Benin, Burkina Faso, Ghana, Mali, and Togo, using the same varieties, but the varieties turned out to perform differently in the different countries . It will be important to identify the factors causing this difference in resistance, and one factor would likely be the viruses. The screens were completely based on symptoms, and there could have been infection with different begomoviruses and DNA satellites as well as with other viruses. The resistance conferred by the gene Ty-1 has, for example, been compromised when plants become infected with multiple RNA viruses . Also in pepper, there are variations in the susceptibility to begomovirus infections. In Nigeria, moderate resistance in four pepper cultivars has been identified . In addition to the conventional breeding, different transgenic approaches for achieving resistance or tolerance have been tested against begomoviruses infecting tomato and pepper [80-82] and this may be a way forward for obtaining durable resistance.
In West and Central Africa, leaf curl disease is regarded as the most important biotic stress for okra, and there is a lack of viral resistance/tolerance [58,83]. However, okra has been regarded as a crop of minor importance, and the breeding efforts for okra in the region have been limited.
In India and Bangladesh, screens have revealed resistance and tolerance to be present in some cultivated varieties and wild species of okra against yellow vein mosaic disease (OYVMD), which is also caused by begomoviruses . The genetic material identified in these screens may be of value also for adoption in breeding programs for resistance/tolerance to begomoviruses present in Africa. Screens of genetic material in the region will probably also reveal useful breeding material [58,83]. In a field trial in Burkina Faso with four accessions of a local okra cultivar and four improved commercial okra cultivars, the incidence of OLCD was higher in the local cultivar compared to the commercial cultivars . The difference was suggested to be related to a possible resistance in the commercial cultivars to the whitefly vector.
Whitefly vector management
Insecticides are frequently used to control B. tabaci in different crops, and it is often the main way of control. However, besides the detrimental effects on human health and the environment, the repeated use of the same types of insecticides will lead to the selection for resistance in the insect and may also reduce the numbers of beneficial insects which are natural enemies of whiteflies. Cotton is heavily sprayed for management of insects, and this practice also affects the control of whiteflies in vegetable crops. Tests on B. tabaci populations from cotton fields in Burkina Faso showed that they were resistant to the recommended doses of several chemicals, suggesting that selection for resistance was likely to occur . The systematic use in cotton of pyrethroids, organophosphates and neonicotinoids has probably lead to the observed reduction in susceptibility or even resistance in populations of B. tabaci in Benin, Togo and Burkina Faso . Transgenic cotton varieties with Bacillus thuringiensis (Bt) resistance against lepidopteran larvae have been introduced into Burkina Faso. The cultivation of these varieties involves less insecticide with a reduction in the amount of chemicals used. However, neonicotinoids are applied to the Bt cotton for control of whiteflies, and this leads to the selection of the resistant Q-biotype of B. tabaci [86,87]. Therefore, it is important that insecticides are managed in a sustainable manner and in combination with other control methods.
In West and Central Africa, tomato is produced all around the year, which aggravates the problem with diseases. ToLCD/TYLCD is a large constraint, especially during the dry season, when the whitefly populations are highest . The implementation of host-free periods has been a successful way for control of begomovirus infections of tomato, for example, in Israel and the Dominican Republic [88,89]. A host-free period with no tomato or solanaceous crop is also used in some areas of West Africa with a high incidence of ToLCD/TYLCD [78,90]. The establishment of such a period can be difficult to implement since our knowledge of alternative hosts of begomoviruses is very limited and may lead to an associated reduction in farmers’ income because they will be out of production during this period. Still, in Mali, a host-free period of 2 months has been reported to be successful for managing begomovirus infections of tomato . As part of an IPM approach, other agricultural practices for management of ToLCD/TYLCD and other diseases caused by begomoviruses include eradication of source plants, cultivation of bait plants, reflective mulches and inclusion of physical barriers, and use of virus-free transplants [89-92]. In Nigeria, early planting of pepper or tomato has been found to reduce disease incidence . Practices suggested for vegetable production in tropical Africa have also been intercropping to divert whiteflies or changed sowing times to avoid periods of peaks with pest populations . The best-suited practices for control of begomovirus infections will depend on the local conditions, and different types of management methods will have to be tested.
Besides the crop plants, the begomoviruses have weeds and wild plants as hosts. For complete understanding of the epidemiology and for developing appropriate control measures, the identification of alternative hosts is an important aspect of the study which has been somewhat neglected in the past. Presently, the begomovirus reservoirs remain largely unknown. A recent study showed that the common weed A. conyzoides in Cameroon is host to a complex consisting of Ageratum leaf curl Cameroon virus (ALCCMV), Ageratum leaf curl betasatellite (ALCCMB), and Ageratum leaf curl Cameroon alphasatellite (ALCCMA) . Sequence analyses revealed that the begomovirus was most closely related to a group of tomato-infecting begomoviruses from West Africa suggesting that these viruses may have common hosts. The betasatellite of A. conyzoides has now also been detected in tomato . Of late, a new betasatellite, Tomato leaf curl Togo betasatellite (ToLCTGB), has been identified infecting tomato in Togo and with its closest relative being ALCCMB . That uncultivated (wild) hosts serve as reservoirs for these viruses are further demonstrated by the recent identification of Lamium amplexicaule (family Lamiaceae) as a host of Tomato yellow leaf curl virus (TYLCV) in Korea . These results further stress the urgent need for the search of alternative hosts of begomoviruses and associated ssDNA satellites infecting vegetables in West and Central Africa.
Whitefly B. tabaci vector: biological and genetic variability
The whitefly B. tabaci (Genn.) sibling species group  is a group of morphologically indistinguishable haplotypes that exhibit different biological characteristics, including host range, fecundity, dispersal behavior, virus transmission efficiency, and insecticide resistance . Regardless of these and other phenotypic differences between certain haplotypes or biotypes (well-defined) [96-98], as a group, they are the only insect vectors of the genus, Begomovirus, worldwide. These differences and similarities can have important bearings on the epidemiology of begomovirus-incited diseases of vegetable, fruit, and fiber crops [96,99], and in some instances are known to drive begomoviral diversification . The size of a whitefly vector population is often directly associated with begomovirus disease incidence, including a number of outbreaks [44,47,50,52,54,56,64,101,102] and epidemics in Africa such as the CMD pandemic in East and Central Africa . However, in some instances, extremely high incidence has been observed even when population levels are low.
The overall genetic diversity of the B. tabaci sibling species group in western Africa is not well studied. Burban et al.  first showed host-associated differences among populations of B. tabaci from cassava and okra and other host plants in Côte d'Ivoire, based on isozyme electrophoresis and experimental host range studies. This report was corroborated by the presence of cassava and non-cassava haplotypes based on RAPD-PCR markers and the internal transcribed spacer-1 (ITS-1) . The haplotype colonizing okra and other vegetable plant species appears to be polyphagous, whereas the cassava-associated haplotype was found colonizing only cassava plants. Gueguen et al.  reported three haplotypes in Burkina Faso, a sub-Saharan type, a silvering type (B-like clade), and a close relative of the Spanish Q (Q-like clade) [96,98,99]. Recently, Gnankiné et al.  sampled B. tabaci populations in 20 locations and seven cultivated plant hosts in Burkina Faso, Benin, and Togo and obtained a result similar to the latter study. However, they additionally demonstrated evidence for host and geographical affiliations, in that, in Benin and Togo, the B-like, silvering and sub-Saharan African non-silvering types predominated. In contrast, Q-like haplotypes were most widespread in Burkina Faso. In some instances the B-like silvering and Q-like haplotypes overlapped in host and location. In cassava plantings, an invasive-like non-B/non-Q type that also differs genetically from the sub-Saharan non-silvering type found in the above three countries, has been reported accompanying the rapidly spreading CMD, as it appears to be spreading toward and/or into Cameroon and neighboring countries .
Diagnostic approaches for begomoviruses
The majority of approaches currently being used for begomovirus epidemiological and other studies rely nearly entirely on molecular methods. A number of DNA extraction methods have been used to isolate and purify total genomic DNA from plant leaves, stems, and roots/tubers suspected to harbor begomoviruses. Most commonly, the CTAB method of Doyle and Doyle  is used along with a variety of its modifications and methods optimized for difficult-to-handle plants . Manufactured kits tailored for isolation of total genomic DNA from plants are also widely implemented. The method of choice is best selected based on the characteristics of the plant host from which total genomic DNA will be isolated. Plant sap from leaves or other parts of begomoviral-infected plants have been successfully applied to and the total genomic DNA eluted from FTA cards. This has been shown to be effective for short-term storage of total genomic DNA that is amenable to PCR amplification of viral DNA fragments , or as template for RCA of begomoviral circular DNA genomes .
PCR  is a widely used method for the initial amplification of begomoviral genomic fragments to demonstrate begomoviral presence. Several broad-spectrum primer pairs have been designed that are useful in many instances, but thus far, no single pair of primers can be guaranteed to amplify all begomoviruses given the extensive genomic variation occurring within the genus worldwide. The most common PCR target is the begomoviral coat protein (CP) gene, or a region of it that is accessible for most isolates using degenerate PCR primers that target the middle, or ‘core’ region, of the ORF, designated AC1048/AV494 [114,115]. Modified degenerate core CP primers have been designed to have more broad-spectrum capabilities. They are based on the substantially greater number of sequences available in the GenBank database by 2011 and are available upon request (J.K. Brown, personal communication). The CP gene has proven to be an ideal target because it is relatively highly conserved across the genus. Two other sets of primers with broad-spectrum amplification of bipartite begomoviruses that amplify fragments of both the DNA-A and DNA-B components have been reliable for PCR amplification of primarily the Western Hemisphere begomoviruses  and some bipartite viruses from the Eastern Hemisphere. A third set also primarily useful for PCR amplification of bipartite begomoviruses targets conserved regions in the intergenic/common region and the Rep gene . Immuno-capture PCR has also been used successfully when an antibody to the virus or related viruses is available . Universal primers [119,120] have been designed to facilitate PCR amplification, cloning, and sequencing of betasatellite molecules that associate with a number of monopartite begomoviruses. They are particularly prevalent among begomoviruses endemic to Africa, Asia, and Latin America and most commonly are essential for infectivity and/or pathogenicity of the ‘helper’ begomovirus, encoding a single multifunctional protein that functions as a suppressor of host gene silencing among others.
Recently, the most widely applied method for detecting and cloning begomoviral genomes is the non-sequence-specific approach that uses bacteriophage phi29 DNA polymerase [121,122], now referred to as RCA . In virology research, it was used first for the detection of papillomaviruses . It was first applied to begomoviruses by Inoue-Nagata et al.  and since has become routinely used for begomoviral diagnostics and molecular cloning of whole viral genomes to facilitate their characterization and enable the relatively efficient construction of infectious clones  and many others. RCA also has been used to enrich for and prepare template for begomoviral deep sequencing employing next-generation approaches such as Illumina .
The most important considerations for implementing RCA for begomovirus diagnostics are to avoid repeated freezing and drying of the DNA so that breaks do not occur in the circular template DNA strands . The amount of input DNA required is variable, depending on the source of the template, but in general, only a small amount of circular DNA (~1 ng) needs to be available for RCA. The most common approach for confirming that the amplification step has produced viral fragments or genomic components of interest is to digest the multimeric high molecular weight product with one or more diagnostic restriction enzymes that are known to or might yield a full-length genome of a particular sized diagnostic fragment. The endonuclease digested dsDNA products are readily visualized by gel electrophoresis in 0.7%–1.2% agarose, with the concentration adjusted to accommodate the range of fragment sizes. Further processing of RCA products including cloning, direct sequencing or additional PCR amplification is carried out. Additional PCR amplification using virus or group-specific primers can be carried out using the RCA product as template when the method is used to enrich for or pre-amplify viral circular DNA. A number of protocols have been published, and some of these are summarized in .
With this high diversity, recombination potential, limited knowledge of alternative hosts, and transmission by B. tabaci, begomoviruses and their associated ssDNA satellites pose a serious threat to crop production and thus food security in West and Central Africa.
We sincerely thank the anonymous referees for useful comments that strengthened this review.
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