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Begomoviruses: what is the secret(s) of their success?
Abstract
Begomoviruses constitute an extremely successful group of emerging plant viruses transmitted by whiteflies of the Bemisia tabaci complex. Hosts include important vegetable, root, and fiber crops grown in the tropics and subtropics. Factors contributing to the ever-increasing diversity and success of begomoviruses include their predisposition to recombine their genomes, interaction with DNA satellites recruited throughout their evolution, presence of wild plants as a virus reservoir and a source of speciation, and extreme polyphagia and continuous movement of the insect vectors to temperate regions. These features as well as some controversial issues (replication in the insect vector, putative seed transmission, transmission by insects other than B. tabaci, and expansion of the host range to monocotyledonous plants) will be analyzed in this review.
... Begomoviruses (family Geminiviridae) are a group of plant single-stranded DNA (ssDNA) viruses that are transmitted by whiteflies of the Bemisia tabaci complex [11,12]. The genus Begomovirus is now the largest in the entire virosphere as recognized by the International Committee on Taxonomy of Viruses [11]. ...
... The genus Begomovirus is now the largest in the entire virosphere as recognized by the International Committee on Taxonomy of Viruses [11]. Moreover, in recent decades begomoviruses have exacted a heavy toll on the production of many solanaceous, cucurbitaceous, malvaceous and leguminous crops in warm and temperate regions around the globe [12]. Diseases caused by begomoviruses that are of particular significance include tomato yellow leaf curl, cotton leaf curl and cassava mosaic [12]. ...
... Moreover, in recent decades begomoviruses have exacted a heavy toll on the production of many solanaceous, cucurbitaceous, malvaceous and leguminous crops in warm and temperate regions around the globe [12]. Diseases caused by begomoviruses that are of particular significance include tomato yellow leaf curl, cotton leaf curl and cassava mosaic [12]. Begomoviruses can be either monopartite or bipartite depending on the number of genomic components [11]. ...
The genomic components of multipartite viruses are encapsidated in separate virus particles, and the frequencies of genomic components represent one of the key genetic features. Many begomoviruses of economic significance are bipartite, and the details of the association between their genomic components remain largely unexplored. We first analyzed the temporal dynamics of the quantities of DNA-A and DNA-B and the B/A ratio of the squash leaf curl China virus (SLCCNV) in plants and found that while the quantities of DNA-A and DNA-B varied significantly during infection, the B/A ratio remained constant. We then found that changes in the B/A ratio in agrobacteria inoculum may significantly alter the B/A ratio in plants at 6 days post inoculation, but the differences disappeared shortly thereafter. We next showed that while the quantities of DNA-A and DNA-B among plants infected by agrobacteria, sap transmission and whitefly-mediated transmission differed significantly, the B/A ratios were similar. Further analysis of gene expression revealed that the ratio of the expression of genes encoded by DNA-A and DNA-B varied significantly during infection. Finally, we monitored the temporal dynamics of the quantities of DNA-A and DNA-B and the B/A ratio of another bipartite begomovirus, and a constant B/A ratio was similarly observed. Our findings highlight the maintenance of a constant ratio between the two genomic components of bipartite begomoviruses during infection and transmission, and provide new insights into the biology of begomoviruses.
... In recent decades, the production of many crops has been increasingly threatened by plant viral diseases [1]. In tropical, subtropical and warm temperate regions, geminiviruses (family Geminiviridae), the largest group of plant viruses, have caused many devastating crop disease epidemics [2][3][4]. Among the 14 genera in the family Geminiviridae, the genus Begomovirus comprises the largest number of viral species [5,6]. ...
... Among the 14 genera in the family Geminiviridae, the genus Begomovirus comprises the largest number of viral species [5,6]. Additionally, members of the genus Begomovirus exhibit the widest geographic distribution [2][3][4]7]. Begomoviruses can infect many important dicotyledonous crops such as tomato, cotton and cassava, causing yield losses of up to 100% [2][3][4]. ...
... Additionally, members of the genus Begomovirus exhibit the widest geographic distribution [2][3][4]7]. Begomoviruses can infect many important dicotyledonous crops such as tomato, cotton and cassava, causing yield losses of up to 100% [2][3][4]. Under field conditions, begomoviruses are essentially transmitted by whiteflies of the Bemisia tabaci complex [8,9]. ...
The begomovirus–betasatellite complex constantly threatens crops in Asia. However, the quantitative relationship between begomoviruses and betasatellites remains largely unknown. The quantities of tobacco curly shoot virus (TbCSV) and its betasatellite (TbCSB) and their ratio varied significantly in initial infection, and thereafter, the ratio tended to become constant. The TbCSB/TbCSV ratio in agrobacteria inoculum significantly affected that in plants in the initial infection but not thereafter. Null-mutation of βC1 that encodes a multifunctional protein important for pathogenesis in TbCSB significantly reduced the TbCSB/TbCSV ratio in plants. Viral inoculum plants with higher TbCSB/TbCSV ratios promoted whitefly transmission of the virus. The expression of AV1 encoded by TbCSV, βC1 encoded by TbCSB and the βC1/AV1 ratio varied significantly in the initial infection and thereafter the ratio tended to become constant. Additionally, the temporal dynamics of the ratio between another begomovirus and its betasatellite was similar to that of TbCSV and was positively regulated by βC1. These results indicate that the ratio between monopartite begomoviruses and betasatellites tend to become constant as infection progresses, and is modulated by βC1, but a higher betasatellite/begomovirus ratio in virally inoculated plants promotes virus transmission by whiteflies. Our findings provide novel insights into the association between begomoviruses and betasatellites.
... The estimated economic loss due to begomoviruses in the 1990s was USD 1.3-2.3 billion for cassava in Africa, USD 5 billion for cotton in Pakistan, USD 300 million for grain legumes in India, and USD 140 million in Florida, USA, for tomato alone [1]. Despite efforts to contain begomoviruses, they continue to emerge and re-emerge in diverse crops and regions [2][3][4][5][6][7]. ...
... DNA A encodes proteins for replication, control of gene expression, and coat proteins. The DNA B component encodes two proteins involved in the intercellular movement of the virus in host plants and symptom development [1,6]. It is interesting that the ORF AV2 of DNA A is found only in begomoviruses occurring in the Old World [24]; it may have made DNA B redundant, resulting in the evolution of monopartite begomoviruses and its role taken over by the satellites associated with begomoviruses in the Old World. ...
Begomoviruses have emerged as destructive pathogens of crops, particularly in the tropics and subtropics, causing enormous economic losses and threatening food security. Epidemics caused by begomoviruses have even spread in regions and crops that were previously free from these viruses. The most seriously affected crops include cassava; cotton; grain legumes; and cucurbitaceous, malvaceous, and solanaceous vegetables. Alphasatellites, betasatellites, and deltasatellites are associated with the diseases caused by begomoviruses, but begomovirus–betasatellite complexes have played significant roles in the evolution of begomoviruses, causing widespread epidemics in many economically important crops throughout the world. This article provides an overview of the evolution, distribution, and approaches used by betasatellites in the suppression of host plant defense responses and increasing disease severity.
... An example of a mono-partite particle is CLCuV (Liu et al., 1998;Mansoor et al., 1999). PCR amplification of CLCuDinfected cotton indicated the presence of CLCuV (Fiallo-Olivé and Navas-Castillo, 2023). CLCuV possesses a circular single-stranded deoxyribonucleic acid (ssDNA) molecule, tightly encapsulated inside a geminate particle. ...
... Recently, this family has been increased from nine recognized genera to fourteen genera (Materatski et al., 2021). Begomoviruses is the largest group of Geminiviruses with around 520 accepted viral species ((Uniyal et al., 2019;Ouattara et al., 2022;Fiallo-Olivé and Navas-Castillo, 2023). ...
Cotton (Gossypium hirsutum L.) is a significant fiber crop. Being a major contributor to the textile industry requires continuous care and attention. Cotton is subjected to various biotic and abiotic constraints. Among these, biotic factors including cotton leaf curl virus (CLCuV) are dominant. CLCuV is a notorious disease of cotton and is acquired, carried, and transmitted by the whitefly (Bemisia tabaci). A cotton plant affected with CLCuV may show a wide range of symptoms such as yellowing of leaves, thickening of veins, upward or downward curling, formation of enations, and stunted growth. Though there are many efforts to protect the crop from CLCuV, long-term results are not yet obtained as CLCuV strains are capable of mutating and overcoming plant resistance. However, systemic-induced resistance using a gene-based approach remained effective until new virulent strains of CLCuV (like Cotton Leaf Curl Burewala Virus and others) came into existence. Disease control by biological means and the development of CLCuV-resistant cotton varieties are in progress. In this review, we first discussed in detail the evolution of cotton and CLCuV strains, the transmission mechanism of CLCuV, the genetic architecture of CLCuV vectors, and the use of pathogen and nonpathogen-based approaches to control CLCuD. Next, we delineate the uses of cutting-edge technologies like genome editing (with a special focus on CRISPR-Cas), next-generation technologies, and their application in cotton genomics and speed breeding to develop CLCuD resistant cotton germplasm in a short time. Finally, we delve into the current obstacles related to cotton genome editing and explore forthcoming pathways for enhancing precision in genome editing through the utilization of advanced genome editing technologies. These endeavors aim to enhance cotton’s resilience against CLCuD.
... In the last decades, the ever-increasing emergence of members of the genus Begomovirus has threatened crop production in the tropics, subtropics, and warm temperate regions around the world (7). It is generally believed that begomoviruses are transmitted by whiteflies of the Bemisia tabaci complex in a persistent circulative manner (3,6). ...
... It is generally believed that begomoviruses are transmitted by whiteflies of the Bemisia tabaci complex in a persistent circulative manner (3,6). It should be noted, however, that studies are emerging showing that at least one begomovirus tomato yellow leaf curl virus (TYLCV) may replicate in their whitefly vectors (6)(7)(8)(9)(10). Nevertheless, amid the journey of begomoviruses within whitefly vectors, virus entry into and/or movement within the midgut and primary salivary gland (PSG) dictates virus transmission efficiency (6,(11)(12)(13). ...
Begomoviruses are significant constraints to the production of many crops worldwide. Efficient passage of the circulatively transmitted begomoviruses through the midgut and primary salivary gland (PSG) of their whitefly vector is an essential step in productive virus transmission. While how begomoviruses transport across the whitefly midgut wall has been characterized, the mechanisms underlying the trafficking of begomoviruses through whitefly PSG remain poorly understood. In this study, we combined direct injection of purified virions into the whitefly hemolymph with inhibitor and dsRNA treatment and investigated the roles of endocytosis and endosomes in the entry and intracellular trafficking of begomoviruses in whitefly PSG. We found that clathrin-mediated endocytosis and early endosomes mediated the entry of tomato yellow leaf curl virus (TYLCV) into whitefly PSG. Additionally, late and recycling endosomes were not involved in TYLCV trafficking in PSG. Notably, the regulating proteins of vesicle trafficking such as Arp2/3 complex; CORVET complex subunits Vps8, Vps11, and Vps33a; and sorting nexin Snx12 did not seem to play a role in TYLCV entry into PSG. Furthermore, clathrin-mediated endocytosis and early endosomes were found to mediate the entry of another begomovirus into PSG, indicating it might be a conserved pathway exploited by begomoviruses to enter PSG. Our results uncovered the key whitefly components that mediate the trafficking of begomoviruses in PSGs of their insect vectors.
IMPORTANCE
Many plant viruses are transmitted by insect vectors in a circulative manner. For efficient transmission, the entry of the virus from vector hemolymph into the primary salivary gland (PSG) is a step of paramount importance. Yet, vector components mediating virus entry into PSG remain barely characterized. Here, we demonstrate the role of clathrin-mediated endocytosis and early endosomes in begomovirus entry into whitefly PSG. Our findings unravel the key components involved in begomovirus transport within the whitefly body and transmission by their whitefly vectors and provide novel clues for blocking begomovirus transmission.
... Many begomoviruses associate with episomal DNAs that are not essential for infection but often influence disease processes. These episomes are generally satellites that are transmitted as part of a begomovirus complex (Nawaz-ul-Rehman et al., 2021;Fiallo-Olivéand Navas-Castillo, 2023). The presence of a satellite can increase pathogenicity, overcome plant resistance, and influence virus movement and host range (Gnanasekaran et al., 2019;Nawazul-Rehman et al., 2021;Fiallo-Olivéand Navas-Castillo, 2023). ...
... These episomes are generally satellites that are transmitted as part of a begomovirus complex (Nawaz-ul-Rehman et al., 2021;Fiallo-Olivéand Navas-Castillo, 2023). The presence of a satellite can increase pathogenicity, overcome plant resistance, and influence virus movement and host range (Gnanasekaran et al., 2019;Nawazul-Rehman et al., 2021;Fiallo-Olivéand Navas-Castillo, 2023). An earlier study showed that SEGS-1 and SEGS-2 episomes occur in CMB-infected cassava, raising the possibility that they are begomovirus satellites (Ndunguru et al., 2016). ...
Cassava is a major crop in Sub-Saharan Africa, where it is grown primarily by smallholder farmers. Cassava production is constrained by Cassava mosaic disease (CMD), which is caused by a complex of cassava mosaic begomoviruses (CMBs). A previous study showed that SEGS-1 (sequences enhancing geminivirus symptoms), which occurs in the cassava genome and as episomes during viral infection, enhances CMD symptoms and breaks resistance in cassava. We report here that SEGS-1 also increases viral disease severity in Arabidopsis thaliana plants that are co-inoculated with African cassava mosaic virus (ACMV) and SEGS-1 sequences. Viral disease was also enhanced in Arabidopsis plants carrying a SEGS-1 transgene when inoculated with ACMV alone. Unlike cassava, no SEGS-1 episomal DNA was detected in the transgenic Arabidopsis plants during ACMV infection. Studies using Nicotiana tabacum suspension cells showed that co-transfection of SEGS-1 sequences with an ACMV replicon increases viral DNA accumulation in the absence of viral movement. Together, these results demonstrated that SEGS-1 can function in a heterologous host to increase disease severity. Moreover, SEGS-1 is active in a host genomic context, indicating that SEGS-1 episomes are not required for disease enhancement.
... Among the whitefly-transmitted viruses, BGVs (Geminiviridae), criniviruses (Closteroviridae), and torradoviruses (Secoviridae) are considered the most destructive. Begomoviruses (BGVs) are DNA viruses that are categorized as monopartite or bipartite, having circular single-stranded DNA genomes (also known as DNA-A and DNA-B), and being encapsulated in twinned icosahedral capsids [1,2]. The prevalence of monopartite BGVs is greater in the Old World (OW), while the number of reported cases in the New World (NW) is relatively low [2,3]. ...
... Begomoviruses (BGVs) are DNA viruses that are categorized as monopartite or bipartite, having circular single-stranded DNA genomes (also known as DNA-A and DNA-B), and being encapsulated in twinned icosahedral capsids [1,2]. The prevalence of monopartite BGVs is greater in the Old World (OW), while the number of reported cases in the New World (NW) is relatively low [2,3]. Being one of the largest Thus, our primary objective was to identify and describe the patterns of mutations that indicate positive selection in the coat protein (CP) of both OW and NW viruses, as well as to assess how these patterns change over different geographical regions. ...
Begomoviruses, belonging to the family Geminiviridae and the genus Begomovirus, are DNA viruses that are transmitted by whitefly Bemisia tabaci (Gennadius) in a circulative persistent manner. They can easily adapt to new hosts and environments due to their wide host range and global distribution. However, the factors responsible for their adaptability and coevolutionary forces are yet to be explored. Among BGVs, TYLCV exhibits the broadest range of hosts. In this study, we have identified variable and coevolving amino acid sites in the proteins of Tomato yellow leaf curl virus (TYLCV) isolates from Old World (African, Indian, Japanese, and Oceania) and New World (Central and Southern America). We focused on mutations in the coat protein (CP), as it is highly variable and interacts with both vectors and host plants. Our observations indicate that some mutations were accumulating in Old World TYLCV isolates due to positive selection, with the S149N mutation being of particular interest. This mutation is associated with TYLCV isolates that have spread in Europe and Asia and is dominant in 78% of TYLCV isolates. On the other hand, the S149T mutation is restricted to isolates from Saudi Arabia. We further explored the implications of these amino acid changes through structural modeling. The results presented in this study suggest that certain hypervariable regions in the genome of TYLCV are conserved and may be important for adapting to different host environments. These regions could contribute to the mutational robustness of the virus, allowing it to persist in different host populations.
... Most of these viruses belong to the genus Begomovirus (family Geminiviridae), the largest genus in the entire virosphere, with 409 recognized species [1]. Begomoviruses constitute an extremely successful group of emerging plant viruses, present in both the Old and New World [2]. Indeed, the two major phylogenetic groups within the genus are related to geographical origin: Old World (OW) and New World (NW) begomoviruses; the others being the legumoviruses and the sweepoviruses. ...
... This suggests a relevant role for this perennial wild cucurbit in ToLCNDV epidemiology in the Mediterranean basin by acting as a source of inoculum. ToLCNDV, as with all begomoviruses, is transmitted in a persistent manner by whiteflies of the B. tabaci cryptic species complex [2]. Surprisingly, however, it has been reported that another whitefly species, Trialeurodes vaporariorum (Westwood), the greenhouse whitefly, was able to transmit a ToLCNDV isolate found infecting chayote [Sechium edule (Jacq.) ...
Tomato leaf curl New Delhi virus (ToLCNDV) is a bipartite begomovirus (genus Begomovirus, family Geminiviridae) persistently transmitted, as with all other begomoviruses, by whiteflies (Hemiptera: Aleyrodidae) of the Bemisia tabaci cryptic species complex. The virus, originally from the Indian subcontinent, was recently introduced in the Mediterranean basin, where it is currently a major concern for protected and open-field horticulture. The Mediterranean ToLCNDV isolates belong to a novel strain named “Spain strain” (ToLCNDV-ES), which infects zucchini and other cucurbit crops but is poorly adapted to tomato. Recently, it has been reported that another whitefly, Trialeurodes vaporariorum, is able to transmit an isolate of ToLCNDV from India which infects the chayote plant, a cucurbit. The present work aimed to clarify some aspects of whitefly transmission of ToLCNDV-ES. It was shown that T. vaporariorum is not able to transmit ToLCNDV-ES between zucchini plants. In addition, Ecballium elaterium may not act as a relevant reservoir for this virus strain in the Mediterranean basin, as B. tabaci Mediterranean (MED), the most prevalent species of the complex in the region, is not an efficient vector of this begomovirus between cultivated zucchini and wild E. elaterium plants.
... As most of the cultivated, wild alternative, and weed species are the hosts for begomoviruses, seed transmission can help the virus to persist in these plant populations, which can further act as reservoirs (Regassa et al., 2021). Recent studies reported the expansion of begomovirus host range to monocotyledons, the movement of B. tabaci vector to temperate regions, and the transmission of begomoviruses by whiteflies other than B. tabaci complex (Idriss et al., 1997;Kriticos et al., 2020;Kil et al., 2021;Fiallo Olive and Navas-Castillo, 2023). In such cases, seed-transmitted novel begomovirus variants and species may spread across the globe through seed trade and insect vectors and responsible for epidemics in host and non-host species under changing global climate scenario. ...
Begomoviruses (family Geminiviridae) are known for causing devastating diseases in fruit, fibre, pulse, and vegetable crops throughout the world. Begomoviruses are transmitted in the field exclusively through insect vector whitefly (Bemisia tabaci), and the frequent outbreaks of begomoviruses are attributed largely due to the abundance of whitefly in the agri-ecosystem. Begomoviruses being phloem-borne were known not be transmitted through seeds of the infected plants. The recent findings of seed transmission of begomoviruses brought out a new dimension of begomovirus perpetuation and dissemination. The first convincing evidence of seed transmission of begomoviruses was known in 2015 for sweet potato leaf curl virus followed by several begomoviruses, like bhendi yellow vein mosaic virus, bitter gourd yellow mosaic virus, dolichos yellow mosaic virus, mungbean yellow mosaic virus, mungbean yellow mosaic India virus, pepper yellow leaf curl Indonesia virus, tomato leaf curl New Delhi virus, tomato yellow leaf curl virus, tomato yellow leaf curl Sardinia virus, and okra yellow mosaic Mexico virus. These studies brought out two perspectives of seed-borne nature of begomoviruses: (i) the presence of begomovirus in the seed tissues derived from the infected plants but no expression of disease symptoms in the progeny seedlings and (ii) the seed infection successfully transmitted the virus to cause disease to the progeny seedlings. It seems that the seed transmission of begomovirus is a feature of a specific combination of host-genotype and virus strain, rather than a universal phenomenon. This review comprehensively describes the seed transmitted begomoviruses reported in the last 9 years and the possible mechanism of seed transmission. An emphasis is placed on the experimental results that proved the seed transmission of various begomoviruses, factors affecting seed transmission and impact of begomovirus seed transmission on virus circulation, outbreak of the disease, and management strategies.
... The endoplasmic reticulum is a primary target for plant RNA viruses, but they frequently remodel additional cellular compartments, such as chloroplasts and peroxisomes (Richardson, 2019). Begomoviruses constitute a remarkably successful group of emerging viruses and carry a monopartite or bipartite single-strand (ss) DNA genome (Fiallo-Olivéand Navas-Castillo, 2023). Their replication does not require a drastic host endomembrane remodeling and takes place in the nucleus. ...
The plant endomembrane system is an elaborate collection of membrane-bound compartments that perform distinct tasks in plant growth and development, and in responses to abiotic and biotic stresses. Most plant viruses are positive-strand RNA viruses that remodel the host endomembrane system to establish intricate replication compartments. Their fundamental role is to create optimal conditions for viral replication, and to protect replication complexes and the cell-to-cell movement machinery from host defenses. In addition to the intracellular antiviral defense, represented mainly by RNA interference and effector-triggered immunity, recent findings indicate that plant antiviral immunity also includes membrane-localized receptor-like kinases that detect viral molecular patterns and trigger immune responses, which are similar to those observed for bacterial and fungal pathogens. Another recently identified part of plant antiviral defenses is executed by selective autophagy that mediates a specific degradation of viral proteins, resulting in an infection arrest. In a perpetual tug-of-war, certain host autophagy components may be exploited by viral proteins to support or protect an effective viral replication. In this review, we present recent advances in the understanding of the molecular interplay between viral components and plant endomembrane-associated pathways.
... among its 2,556 protein-coding genes, and less than half of the genes consistently present in large dsDNA viruses (i.e., 'core' genes) (Philippe et al., 2013). In addition, viruses can undergo for example genetic recombination, pseudo-recombination, and hybridization, typical for example in the begomoviruses, a family of highly successful plant viruses (Chakraborty and Kumar, 2021;Fiallo-Olivé and Navas-Castillo, 2023). Such genomic divergence can further complicate virus classification. ...
Taxonomical classification has preceded evolutionary understanding. For that reason, taxonomy has become a battleground fueled by knowledge gaps, technical limitations, and a priorism . Here we assess the current state of the challenging field, focusing on fallacies that are common in viral classification. We emphasize that viruses are crucial contributors to the genomic and functional makeup of holobionts, organismal communities that behave as units of biological organization. Consequently, viruses cannot be considered taxonomic units because they challenge crucial concepts of organismality and individuality. Instead, they should be considered processes that integrate virions and their hosts into life cycles. Viruses harbor phylogenetic signatures of genetic transfer that compromise monophyly and the validity of deep taxonomic ranks. A focus on building phylogenetic networks using alignment-free methodologies and molecular structure can help mitigate the impasse, at least in part. Finally, structural phylogenomic analysis challenges the polyphyletic scenario of multiple viral origins adopted by virus taxonomy, defeating a polyphyletic origin and supporting instead an ancient cellular origin of viruses. We therefore, prompt abandoning deep ranks and urgently reevaluating the validity of taxonomic units and principles of virus classification.
... The members of this genus have singlestranded (ss) covalently closed circular (ccc) DNA genomes. The genome may be either monopartite (contains one component only) or bipartite (having two components namely DNA-A and DNA-B), and are found in both Old World (both genome types) and New World (mostly bipartite genomes)" [9]. "Majority of the begomoviruses have been found to be associated with satellites that cause symptom severity, and are dependent upon the helper begomovirus for their replication and/or encapsidation" [10]. ...
Bitter gourd (Momordica charantia) is an economically important vegetable and medicinal plant that gets infected by a number of viruses. A survey was conducted in and around Jalandhar region of Punjab, India to study viral symptoms in the bitter gourd fields. The plants showed reduced fruit size, upward leaf curling and mosaic symptoms, indicating begomovirus infection. DNA was isolated from the symptomatic leaves and tested for begomovirus infection using group-specific PCR primers. Amplified products were cloned into pMD20-T vector and sequenced. Based on the obtained sequence, new sets of primers were designed and used for amplification of complete DNA-A and DNA-B. Complete DNA-A and DNA-B were cloned in pMD20-T and sequenced. Sequence analysis of the present DNA-A and DNA-B showed their highest identity with Tomato leaf curl New Delhi virus (ToLCNDV). The associated Tomato leaf curl New Delhi alphasatellite was amplified using universal primers, cloned and sequenced. In phylogenetic analysis, the present DNA-A and DNA-B grouped with ToLCNDV isolates and other begomoviruses reported from bitter gourd. Phylogenetic analysis of the present alphasatellite showed its closet identity with Tomato leaf curl New Delhi alphasatellite. Recombination analysis of the DNA-A sequence showed that the present bitter gourd isolate might be a recombinant of Squash leaf curl China virus (SLCChV) as a major parent and Chilli leaf curl virus as a minor parent. Analysis of the DNA-B suggested it to be a recombinant of SLCChV as a major parent and Chyaote enation yellow mosaic virus as a minor parent. The present alphasatellite might be a recombinant of Tomato yellow spot alphasatellite as a major parent and Croton yellow mosaic alphasatellite as a minor parent. The percent identities of the nucleotide and amino acid sequences validate and support the results of the phylogenetic and recombination analyses.
Chilli, an important vegetable cum spice crop in India, is affected by various biotic and abiotic factors, which leads to a significant reduction in the growth and yield of the chilli crop. One of the most prominent biotic factors posing threat to chilli production in southern parts of India especially, in Tamil Nadu is begomoviruses (Family Geminiviridae). Begomoviruses are transmitted by the insect vector, whitefly (Bemisia tabaci) and they cause curling, yellowing, puckering, and reduction in the size of the leaf in the infected chilli plants. In this study, molecular (PCR) diagnostics were used to detect the presence of begomovirus, betasatellite, and six begomovirus species viz tomato leaf curl New Delhi virus (ToLCNDV), tomato leaf curl Bangalore virus (ToLCBV), tomato leaf curl Palampur virus (ToLCPalV), tomato leaf curl Gujarat virus (ToLCGV), tomato leaf curl Joydebpur virus (ToLCJoV) and chilli leaf curl virus (ChiLCV), in the chilli samples collected from the major chilli growing areas of all the five agro-climatic zones of Tamil Nadu state of India. A total number of 833 samples collected from different locations in Tamil Nadu during the period of 2018-2022 were analysed by generic as well as species-specific PCR. The PCR results of 833 samples showed positive amplification of 20.5% for generic, 13.4% for beta satellite, 42.1% for ChiLCV, 17.8% (ToLCNDV), 16.6% (ToLCGV), 6.7% (ToLCBV), 2.2% (ToLCPalV), and 0.7% for ToLCJoV specific primers respectively. The percentage of mixed infection of two or more than two begomoviruses among the total samples is 39.2. Our study has shown that the ChiLCV and multiple tomato-infecting begomoviruses were prevalent in the major chilli-growing areas of Tamil Nadu. The present study also showed that species of begomovirus infecting chilli plants in Northern and Southern India have a differential distribution.
Bemisia tabaci transmits begomoviruses that cause the most devastating disease of Capsicum chinense in tropical regions. Here we first evaluated the incidence and severity of Begomovirus symptoms on habanero pepper landraces H-224 and H-241 and commercial cultivar Jaguar that were naturally infested with B. tabaci in the field. Then we treated H-241 in the greenhouse with different botanical insecticides and assessed the Begomovirus symptoms. In the field, the mean area under the disease progress curve for incidence and severity did not differ significantly (P > 0.05) among the peppers tested; however, the final incidence of symptoms was significantly lower on Jaguar pepper than on the two landraces. Jaguar and H-241 had higher fruit yield than H-224. In the greenhouse experiment, the botanical insecticides protected H-241 against viral symptoms similarly to the treatment with only chemical insecticides. The fruit yield did not differ significantly between plants treated with the botanical insecticide combinations (2.1–2.5 kg plant−1) and those treated with only chemical insecticides (2.3 kg plant−1). The use of botanical insecticides holds promise as an environmental-friendly option to manage B. tabaci-transmitted begomoviruses in habanero pepper.
Aim: To study the disease incidence and diversity of Begomovirus infection and crop loss due to spread of virus across different districts of North Bengal. Methodology: Several fields in different districts of North Bengal were surveyed and potential begomoviral-infected samples were collected for further analysis. Total DNA extraction, PCR analysis, sequencing and phylogenetic analysis were conducted. Results: During 2019-2021, ten fields of each district were surveyed and begomoviral occurrence was observed in almost every field. The disease incidence in different districts varied from 15-45%. The highest disease (42.5%) incidence of was observed in the Darjeeling district while the lowest (15%) was recorded from Alipurduar district. The maximum crop loss due to Begomovirus was 64-100% in bitter gourd, 40-80% in cucumber and 20-30% in wax gourd. 153 samples from 6 different cucurbits were collected and analysed. PCR using AV494/AC1048 primers that amplified coat protein region (~550bp) showed 74% of the samples as positive. Upon sequencing and BLAST analysis, ToLCNDV, SLCCV and BGYVV were detected. In phylogenetic analysis, the isolates clustered in three separate clades based on Begomovirus species irrespective of the hosts. Present isolates showed more closeness to Indian and Bangladesh isolates. Interpretation: The documentation of disease severity caused by Begomovirus is of extreme importance for food security of the people. Present study revealed that Begomovirus is present in all the crop field studied. The results indicated an urgent need for the management of the viruses to save crops. Key words: Begomovirus, Cucurbitaceous crops, Disease incidence, North Bengal
Plants face constant threats from insect herbivores, which limit plant distribution and abundance in nature and crop productivity in agricultural ecosystems. In recent decades, the whitefly Bemisia tabaci, a group of phloem-feeding insects, has emerged as pests of global significance. In this article, we summarize current knowledge on plant defenses against whitefly and approaches to engineer plant resistance to whitefly. Physically, plants deploy trichome and acylsugar-based strategies to restrain nutrient extraction by whitefly. Chemically, toxic secondary metabolites such as terpenoids confer resistance against whitefly in plants. Moreover, the jasmonate (JA) signaling pathway seems to be the major regulator of whitefly resistance in many plants. We next review advances in interfering with whitefly-plant interface by engineering of plant resistance using conventional and biotechnology-based breeding. These breeding programs have yielded many plant lines with high resistance against whitefly, which hold promises for whitefly control in the field. Finally, we conclude with an outlook on several issues of particular relevance to the nature and engineering of plant resistance against whitefly.
Chilli leaf curl virus disease caused by begomoviruses, has emerged as a major threat to global chilli production, causing severe yield losses and economic harm. Begomoviruses are a highly successful and emerging group of plant viruses that are primarily transmitted by whiteflies belonging to the Bemisia tabaci complex. The most effective method for mitigating chilli leaf curl virus disease losses is breeding for host resistance to Begomovirus. This review highlights the current situation of chilli leaf curl virus disease and associated begomoviruses in chilli production, stressing the significant issues that breeders and growers confront. In addition, the various breeding methods used to generate begomovirus resistant chilli cultivars, and also the complicated connections between the host plant, vector and the virus are discussed. This review highlights the importance of resistance breeding, emphasising the importance of multidisciplinary approaches that combine the best of traditional breeding with cutting-edge genomic technologies. subsequently, the article highlights the challenges that must be overcome in order to effectively deploy begomovirus resistant chilli varieties across diverse agroecological zones and farming systems, as well as understanding the pathogen thus providing the opportunities for improving the sustainability and profitability of chilli production.
Bell pepper plant leaves showing typical begomovirus-like symptoms (crumpling, mosaic, and stunting) were collected from Jalandhar region of Punjab, India. Total DNA was isolated from symptomatic plant leaves, and species-specific primers were used to amplify and detect begomovirus. The full-length genome was amplified using the rolling circle amplification method, cloned into the pBluescript II KS (+) vector, and sequenced. A BLAST search of the current DNA-A isolate revealed the highest percentage of identity (98.83%) with other isolates. Betasatellite sequences on BLAST search showed a close similarity of 98.10% with other isolates. Phylogenetic analysis with other distinct begomovirus species revealed that the virus’s current DNA-A was closely related to the Papaya leaf crumple virus and the Chenopodium leaf distortion virus. For the present isolates of DNA-A and betasatellite, no major recombination event was found. In the present study, molecular identification and characterization of the Papaya leaf crumple virus with Papaya leaf curl betasatellite adds another host, and to the best of our knowledge, this is the first report of the present virus infecting the bell pepper plant worldwide.
Due to their stagnation, plants are frequently exposed to a variety of stresses, including both abiotic and biotic factors. Biotic stress in plants is due to many microbes that include viruses, fungi, bacteria, and parasitic organisms as plant pathogens. Plant viruses are one of those pathogens that frequently evolve and lower global agricultural productivity. Geminiviruses are the most damaging type of plant viruses. Tomato Leaf Curl New Delhi Virus (ToLCNDV) is a begomovirus belonging to the family Geminiviridae. This is a ssDNA virus having a bipartite genome with genomic length ranging between 2.6-2.7 kb. This virus was originally discovered in India in 1995 from tomato (Lycopersicon esculentum). It mostly infects solanaceous and cucurbitaceous crops and is a whitefly-transmitted, circulative and persistent virus. Its prominent symptoms are severe upward leaf curling, enations, stunting, puckering, yellow spots and yellow mosaic. This virus has devastating effects on the yield of different crops with yield losses ranging between 17.6-99.4 % depending upon the disease-causing factors. ToLCNDV-ES and ToLCNDV-OM are the most devastating strains of this virus. This comprehensive review will provide basic information on the characteristic features of ToLCNDV. The evolutionary mechanism of this virus is studied to know about the strain’s evolution with the passage of time on different host plants cultivated in several regions of the world. This review also covers the genome characteristics, geographical distribution, host range, transmission methods, genetic diversity, different molecular & serological assays, yield losses, and the management of this virus.
Horizontal transfer of genetic material (HT) is the passage of DNA between organisms by means other than reproduction. Increasing numbers of HT are reported in insects, with bacteria, fungi, plants and insects acting as the main sources of these transfers. Here, we provide a detailed account of plant-to-insect HT events. At least 14 insect species belonging to 6 orders are known to have received plant genetic material through HT. One of them, the whitefly Bemisia tabaci (MEAM1), concentrates most of these transfers, with no less than 28 HT events yielding 55 plant-derived genes in this species. Several plant-to-insect HT events reported so far involve gene families known to play a role in plant-parasite interactions. We highlight methodological approaches that may further help characterize these transfers. We argue that plant-to-insect HT is likely more frequent than currently appreciated and that in-depth studies of these transfers will shed new light on plant-insect interactions.
Begomoviruses cause significant losses to a wide range of crops worldwide, and a great progress has been made in characterizing some noncanonical proteins encoded by begomoviruses. In the present study, a novel viral protein, C6, was detected in Nicotiana benthamiana plants infected with tomato leaf curl China virus (ToLCCNV). Sequence analyses revealed that the C6 ORF is on the complementary strand of approximately 36% reported begomovirus sequences with conserved amino acid sequence. ToLCCNV C6 specifically localizes to mitochondria. Analysis of deletion mutants showed that C6 possesses an internal mitochondrial targeting signal. Overall, these data uncover a novel begomovirus-encoded protein targeting distinct plant cell organelles.
Whitefly-transmitted begomoviruses infect and damage a wide range of food, feed, and fiber crops worldwide. Some of these viruses are associated with betasatellite molecules that are known to enhance viral pathogenesis. In this study, we investigated the function of a novel βV1 protein encoded by radish leaf curl betasatellite (RaLCB) by overexpressing the protein using potato virus X (PVX)-based virus vector in Nicotiana benthamiana. βV1 protein induced lesions on leaves, suggestive of hypersensitive response (HR), indicating cell death. The HR reaction induced by βV1 protein was accompanied by an increased accumulation of reactive oxygen species (ROS), free radicals, and HR-related transcripts. Subcellular localization through confocal microscopy revealed that βV1 protein localizes to the cellular periphery. βV1 was also found to interact with replication enhancer protein (AC3) of helper virus in the nucleus. The current findings suggest that βV1 functions as a protein elicitor and a pathogenicity determinant.
Tomato yellow leaf curl virus (TYLCV) is known to encode 6 canonical viral proteins. Our recent study revealed that TYLCV also encodes some additional small proteins with potential virulence functions. The fifth ORF of TYLCV in the complementary sense, which we name C5, is evolutionarily conserved, but little is known about its expression and function during viral infection. Here, we confirmed the expression of the TYLCV C5 by analyzing the promoter activity of its upstream sequences and by detecting the C5 protein in infected cells by using a specific custom-made antibody. Ectopic expression of C5 using a potato virus X (PVX) vector resulted in severe mosaic symptoms and higher virus accumulation levels followed by a burst of reactive oxygen species (ROS) in Nicotiana benthamiana plants. C5 was able to effectively suppress local and systemic post-transcriptional gene silencing (PTGS) induced by single-stranded GFP but not double-stranded GFP, and reversed the transcriptional gene silencing (TGS) of GFP. Furthermore, the mutation of C5 in TYLCV inhibited viral replication and the development of disease symptoms in infected plants. Transgenic overexpression of C5 could complement the virulence of a TYLCV infectious clone encoding a dysfunctional C5. Collectively, this study reveals that TYLCV C5 is a pathogenicity determinant and RNA silencing suppressor, hence expanding our knowledge of the functional repertoire of the TYLCV proteome.
The whitefly, B . tabaci is a major pest of agricultural crops which transmits begomovirus in a species-specific manner. Yellow vein mosaic disease (YVMD) and okra leaf curl disease (OLCD) caused by distinct begomovirus are a major limitation to production of okra in India. In this framework the present investigation reports, for the first time, comparative study of begomovirus species viz. yellow vein mosaic virus (YVMV) and okra enation leaf curl virus (OELCuV) ingested and egested by two cryptic species (Asia I and Asia II 5) of B . tabaci at different time interval using detached leaf assay. A gradual increase of both virus copies were observed with increased feeding exposure in Asia I and Asia II 5. Both the genetic groups of whitefly could acquire the viruses within just 5 minutes of active feeding however, a significant amount of variation was noted in virus uptake by the both. At 24 hours of active feeding Asia II 5 acquired more of YVMV whereas, Asia I ingested more OELCuV. Similarly, the genetic group acquiring higher titre of virus egested higher amount during inoculation period. On the whole, it can be presumed that Asia I is a more effective transmitter of OELCuV whereas, Asia II 5 of YVMV further suggesting increased risk of virus pandemics (both YVMV and OELCuV) in regions where Asia I and Asia II 5 is dominant.
DNA methylation is an epigenetic mechanism that plays important roles in gene regulation and transposon silencing. Active DNA demethylation has evolved to counterbalance DNA methylation at many endogenous loci. Here, we report that active DNA demethylation also targets viral DNAs, tomato yellow leaf curl China virus (TYLCCNV) and its satellite tomato yellow leaf curl China betasatellite (TYLCCNB), to promote their virulence. We demonstrate that the βC1 protein, encoded by TYLCCNB, interacts with a ROS1-like DNA glycosylase in Nicotiana benthamiana and with the DEMETER (DME) DNA glycosylase in Arabidopsis thaliana. The interaction between βC1 and DME facilitates the DNA glycosylase activity to decrease viral DNA methylation and promote viral virulence. These findings reveal that active DNA demethylation can be regulated by a viral protein to subvert DNA methylation-mediated defense.
In recent decades, a legion of monopartite begomoviruses transmitted by the whitefly Bemisia tabaci has emerged as serious threats to vegetable crops in Africa. Recent studies in Burkina Faso (West Africa) reported the predominance of pepper yellow vein Mali virus (PepYVMLV) and its frequent association with a previously unknown DNA-B component. To understand the role of this DNA-B component in the emergence of PepYVMLV, we assessed biological traits related to virulence, virus accumulation, location in the tissue and transmission. We demonstrate that the DNA-B component is not required for systemic movement and symptom development of PepYVMLV (non-strict association), but that its association produces more severe symptoms including growth arrest and plant death. The increased virulence is associated with a higher viral DNA accumulation in plant tissues, an increase in the number of contaminated nuclei of the phloem parenchyma and in the transmission rate by B. tabaci . Our results suggest that the association of a DNA-B component with the otherwise monopartite PepYVMLV is a key factor of its emergence.
The family Geminiviridae includes viruses with mono- or bipartite single-stranded, circular DNA genomes of 2.5–5.2 kb. They cause economically important diseases in most tropical and subtropical regions of the world. Geminiviruses infect dicot and monocot plants and are transmitted by insect vectors. DNA satellites are associated with some geminiviruses. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the family Geminiviridae which is available at ictv.global/report/geminiviridae .
Tomato yellow leaf curl virus (TYLCV) is one of the most important plant viruses belonging to the genus Begomovirus of the family Geminiviridae. To identify natural weed hosts that could act as reservoirs of TYLCV, 100 samples were collected at a TYLCV-affected tomato farm in Iksan from 2013 to 2014. The sample weeds were identified as belonging to 40 species from 18 families. TYLCV was detected in 57 samples belonging to 28 species through polymerase chain reaction using root samples including five species (Eleusine indica, Digitaria ciliaris, Echinochloa crus-galli, Panicum dichotomiflorum, and Setaria faberi) from the family Poaceae. Whitefly Bemisia tabaci-mediated TYLCV transmission from TYLCV-infected E. indica plants to healthy tomatoes was confirmed, and inoculated tomatoes showed typical symptoms, such as leaf curling and yellowing. In addition, TYLCV was detected in leaf and root samples of E. indica plants inoculated by both whitefly-mediated transmission using TYLCV-viruliferous whitefly and agro-inoculation using a TYLCV infectious clone. The majority of mastreviruses infect monocotyledonous plants, but there have also been reports of mastreviruses that can infect dicotyledonous plants, such as the chickpea chlorotic dwarf virus. No exception was reported among begomoviruses known as infecting dicots only. This is the first report of TYLCV as a member of the genus Begomovirus infecting monocotyledonous plants.
Begomoviruses and associated DNA satellites are involved in pathosystems that include many cultivated and wild dicot plants and the whitefly vector Bemisia tabaci. A survey of leguminous plants, both crops and wild species, was conducted in Venezuela, an understudied country, to determine the presence of begomoviruses. Molecular analysis identified the presence of bipartite begomoviruses in 37% of the collected plants. Four of the six begomoviruses identified constituted novel species, and two others had not been previously reported in Venezuela. In addition, a novel deltasatellite (cabbage leaf curl deltasatellite, CabLCD) was found to be associated with cabbage leaf curl virus (CabLCV) in several plant species. CabLCD was the first deltasatellite found to infect legumes and the first found in the New World to infect a crop plant. Agroinoculation experiments using Nicotiana benthamiana plants and infectious viral clones confirmed that CabLCV acts as a helper virus for CabLCD. The begomovirus–deltasatellite complex described here is also present in wild legume plants, suggesting the possible role of these plants in the emergence and establishment of begomoviral diseases in the main legume crops in the region. Pathological knowledge of these begomovirus–deltasatellite complexes is fundamental to develop control methods to protect leguminous crops from the diseases they cause.
Begomoviruses can be found in association with alphasatellites, which are capable of autonomous replication but are dependent on the helper begomovirus for systemic infection, encapsidation and vector transmission. Previous studies suggest that the presence of NW alphasatellites (genus Clecrusatellite) is associated with more severe symptoms. To better understand this interaction, we investigated the effects of two alphasatellites on infectivity, symptom development, viral DNA accumulation and vector transmission of three begomoviruses in three hosts. In tomato and Nicotiana benthamiana, all combinations were infectious. In Leonurus sibiricus, only the ToYSV/ToYSA combination was infectious. The presence of EuYMA increased symptom severity of EuYMV and ToYSV in N. benthamiana, and the presence of ToYSA was associated with more severe symptoms of ToYSV in N. benthamiana and L. sibiricus. EuYMA increased the accumulation of ToYSV in N. benthamiana but reduced the accumulation of EuYMV in tomato and of ToSRV in N. benthamiana. The presence of ToYSA decreased the accumulation of ToYSV in N. benthamiana and L. sibiricus. ToYSA negatively affected transmission of ToSRV by Bemisia tabaci MEAM1. Together, our results indicate that NW alphasatellites can interact with different begomoviruses, increasing symptom severity and interfering in the transmission of the helper begomovirus. Understanding this interaction is important as it may affect the emergence of diseases caused by begomovirus–alphasatellite complexes in the field.
Alphasatellites (family Alphasatellitidae) are circular, single-stranded DNA molecules (~1–1.4 kb) that encode a replication-associated protein and have commonly been associated with some members of the families Geminiviridae, Nanoviridae, and Metaxyviridae (recently established). Here, we provide a taxonomy update for the family Alphasatellitidae following the International Committee on Taxonomy of Viruses (ICTV) Ratification Vote held in March 2021. The taxonomic update includes the establishment of the new subfamily Petromoalphasatellitinae. This new subfamily includes three new genera as well as the genus Babusatellite, which previously belonged to the subfamily Nanoalphasatellitinae. Additionally, three new genera and 14 new species have been established in the subfamily Geminialphasatellitinae, as well as five new species in the subfamily Nanoalphasatellitinae.
Geminiviruses are plant viruses with limited coding capacity. Geminivirus-encoded proteins are traditionally identified by applying a 10-kDa arbitrary threshold; however, it is increasingly clear that small proteins play relevant roles in biological systems, which calls for the reconsideration of this criterion. Here, we show that geminiviral genomes contain additional ORFs. Using tomato yellow leaf curl virus, we demonstrate that some of these small ORFs are expressed during the infection, and that the encoded proteins display specific subcellular localizations. We prove that the largest of these additional ORFs, which we name V3, is required for full viral infection, and that the V3 protein localizes in the Golgi apparatus and functions as an RNA silencing suppressor. These results imply that the repertoire of geminiviral proteins can be expanded, and that getting a comprehensive overview of the molecular plant-geminivirus interactions will require the detailed study of small ORFs so far neglected.
Earlier reports have indicated that begomoviruses encode four proteins (AC1/C1, AC2/C2, AC3/C3, and AC4/C4 proteins) using complementary‐sense DNA as the template. In recent years, several reports have shown that some begomoviruses also encode an AC5/C5 protein from the complementary DNA strand, and these AC5/C5 proteins play different roles in virus infections. Here, we provide evidence showing that Ageratum leaf curl Sichuan virus (ALCScV), a monopartite begomovirus, also encodes a C5 protein that is important for disease symptom formation and can affect viral replication. Infection of Nicotiana benthamiana plants with a potato virus X (PVX)‐based vector carrying the ALCScV C5 gene resulted in more severe disease symptoms and higher virus accumulation levels. ALCScV C5 protein can be found in the cytoplasm and the nucleus. Furthermore, this protein is also a suppressor of posttranscriptional gene silencing. Mutational analysis showed that knockout of C5 gene expression significantly reduced ALCScV‐induced disease symptoms and virus accumulation, while expression of the C5 gene using the PVX‐based vector enhanced ALCScV accumulation in coinfected N. benthamiana plants. ALCScV C5 protein is a virulence factor and enhances the pathogenicity of PVX in Nicotiana benthamiana. Mutational analyses showed that C5 is important for disease symptom formation and affects ALCScV replication in infected plants.
Abstract: Seed transmission is an important factor in the epidemiology of plant pathogens. Geminiviruses are serious pests spread in tropical and subtropical regions. They are transmitted by hemipteran insects, but few cases of transmission though seeds were recently reported. Here, we investigated the tomato seed transmissibility of the begomovirus Tomato yellow leaf curl Sar-dinia virus (TYLCSV), one of the agents inducing the Tomato yellow leaf curl disease, heavily af-fecting tomato crops in the Mediterranean area. None of 180 seedlings originating from TY-LCSV-infected plants showed any phenotypic alteration typical of virus infection. Moreover, whole viral genomic molecules could not be detected in their cotyledons and true leaves, neither by membrane hybridization, nor by rolling-circle amplification followed by PCR, indicating that TYLCSV is not a seed transmissible pathogen for tomato. Examining the localization of TYLCSV DNA in progenitor plants, we detected the virus genome by PCR in all vegetative and reproductive tissues, but viral genomic and replicative forms were found only in leaves, flowers and fruit flesh, but not in seeds and embryos. Closer investigations allowed us to discover for the first time that these embryos were superficially contaminated by TYLCSV DNA but whole genomic molecules were not detectable. Therefore, the inability of TYLCSV genomic molecules to colonize tomato embryos during infection justifies the lack of seed transmissibility observed in this host.
Begomoviruses (family Geminiviridae , genus Begomovirus ) significantly hamper crop production and threaten food security around the world. The frequent emergence of new begomovirus genotypes is facilitated by high mutation frequencies and the propensity to recombine and reassort. Homologous recombination has been especially implicated in the emergence of novel cassava mosaic begomovirus (CMB) genotypes, which cause cassava mosaic disease (CMD). Cassava ( Manihot esculenta ) is a staple food crop throughout Africa, and an important industrial crop in Asia, two continents where production is severely constrained by CMD. The CMD species complex is comprised of 11 bipartite begomovirus species with ample distribution throughout Africa and the Indian subcontinent. While recombination is regarded as a frequent occurrence for CMBs, a revised, systematic assessment of recombination and its impact on CMB phylogeny is currently lacking. We assembled data sets of all publicly available, full-length DNA-A (n=880) and DNA-B (n=369) nucleotide sequences from the 11 recognized CMB species. Phylogenetic networks and complementary recombination detection methods revealed extensive recombination among the CMB sequences. Six out of the eleven species have descended from unique interspecies recombination events. Estimates of recombination and mutation rates revealed that all species experience mutation more frequently than recombination, but measures of population divergence indicate that recombination is largely responsible for the genetic differences between species. Our results support that recombination has significantly impacted the CMB phylogeny and has driven speciation in the CMD species complex.
IMPORTANCE
Cassava mosaic disease (CMD) is a significant threat to cassava production throughout Africa and Asia. CMD is caused by a complex comprised of 11 recognized virus species exhibiting accelerated rates of evolution, driven by high frequencies of mutation and genetic exchange. Here, we present a systematic analysis of the contribution of genetic exchange to cassava mosaic virus species-level diversity. Most of these species emerged as a result of genetic exchange. This is the first study to report the significant impact of genetic exchange on speciation in a group of viruses.
Cotton leaf curl Multan virus (CLCuMuV) and its associated satellites are a major part of the cotton leaf curl disease (CLCuD) caused by the begomovirus species complex. Despite the implementation of potential disease management strategies, the incessant resurgence of resistance-breaking variants of CLCuMuV imposes a continuous threat to cotton production. Here, we present a focused effort to map the geographical prevalence, genomic diversity and molecular evolutionary endpoints that enhance disease complexity by facilitating the successful adaptation of CLCuMuV populations to the diversified ecosystems. Our results demonstrate that CLCuMuV populations are predominantly distributed in China while the majority of alphasatellites and betasatellites exist in Pakistan. We demonstrate that together with frequent recombination, an uneven genetic variation mainly drives CLCuMuV and its satellite’s virulence and evolvability. However, the pattern and distribution of recombination breakpoints greatly vary among viral and satellite sequences. The CLCuMuV, Cotton leaf curl Multan alphasatellite (CLCuMuA) and Cotton leaf curl Multan betasatellite (CLCuMuB) populations arising from distinct regions exhibit high mutation rates. Though evolutionary linked, these populations are independently evolving under strong purifying selection. These findings will facilitate to comprehensively understand the standing genetic variability and evolutionary patterns existing among CLCuMuV populations across major cotton-producing regions of the world.
Sweepoviruses are begomoviruses (genus Begomovirus, family Geminiviridae) with ssDNA genomes infecting sweet potato and other species of the family Convolvulaceae. Deltasatellites (genus Deltasatellite, family Tolecusatellitidae) are small-size non-coding DNA satellites associated with begomoviruses. In this study, the genetic diversity of deltasatellites associated with sweepoviruses infecting Ipomoea indica plants was analyzed by further sampling the populations where the deltasatellite sweet potato leaf curl deltasatellite 1 (SPLCD1) was initially found, expanding the search to other geographical areas in southern continental Spain and the Canary Islands. The sweepoviruses present in the samples coinfected with deltasatellites were also fully characterized by sequencing in order to define the range of viruses that could act as helper viruses in nature. Additionally, experiments were performed to assess the ability of a number of geminivirids (the monopartite tomato leaf deformation virus and the bipartite NW begomovirus Sida golden yellow vein virus, the bipartite OW begomovirus tomato leaf curl New Delhi virus, and the curtovirus beet curly top virus) to transreplicate SPLCD1 in their natural plant hosts or the experimental host Nicotiana benthamiana. The results show that SPLCD1 can be transreplicated by all the geminivirids assayed in N. benthamiana and by tomato leaf curl New Delhi virus in zucchini. The presence of SPLCD1 did not affect the symptomatology caused by the helper viruses, and its effect on viral DNA accumulation depended on the helper virus–host plant combination.
Tomato yellow leaf curl disease (TYLCD) caused by tomato yellow leaf curl virus (TYLCV) and a group of related begomoviruses is an important disease which in recent years has caused serious economic problems in tomato (Solanum lycopersicum) production worldwide. Spreading of the vectors, whiteflies of the Bemisia tabaci complex, has been responsible for many TYLCD outbreaks. In this review, we summarize the current knowledge of TYLCV and TYLV-like begomoviruses and the driving forces of the increasing global significance through rapid evolution of begomovirus variants, mixed infection in the field, association with betasatellites and host range expansion. Breeding for host plant resistance is considered as one of the most promising and sustainable methods in controlling TYLCD. Resistance to TYLCD was found in several wild relatives of tomato from which six TYLCV resistance genes (Ty-1 to Ty-6) have been identified. Currently, Ty-1 and Ty-3 are the primary resistance genes widely used in tomato breeding programs. Ty-2 is also exploited commercially either alone or in combination with other Ty-genes (i.e., Ty-1, Ty-3 or ty-5). Additionally, screening of a large collection of wild tomato species has resulted in the identification of novel TYLCD resistance sources. In this review, we focus on genetic resources used to date in breeding for TYLCVD resistance. For future breeding strategies, we discuss several leads in order to make full use of the naturally occurring and engineered resistance to mount a broad-spectrum and sustainable begomovirus resistance.
Sweet potato leaf curl virus (SPLCV) threatens global sweet potato production. SPLCV is transmitted by Bemisia tabaci or via infected vegetative planting materials; however, SPLCV was suggested to be seed transmissible, which is a characteristic that is disputed for geminiviruses. The objective of this study was to revisit the validity of seed transmission of SPLCV in sweet potato. Using large-scale grow-out of sweet potato seedlings from SPLCV-contaminated seeds over 4 consecutive years, approximately 23,034 sweet potato seedlings of 118 genotype entries were evaluated. All seedlings germinating in a greenhouse under insect-proof conditions or in a growth chamber were free of SPLCV; however, a few seedlings grown in an open bench greenhouse lacking insect exclusion tested positive for SPLCV. Inspection of these seedlings revealed that B. tabaci had infiltrated the greenhouse. Therefore, transmission experiments were conducted using B. tabaci MEAM1, demonstrating successful vector transmission of SPLCV to sweet potato. Additionally, tests on contaminated seed coats and germinating cotyledons demonstrated that SPLCV contaminated a high percentage of seed coats collected from infected maternal plants, but SPLCV was never detected in emerging cotyledons. Based on the results of grow-out experiments, seed coat and cotyledon tests, and vector transmission experiments, we conclude that SPLCV is not seed transmitted in sweet potato.
Projected climate changes are thought to promote emerging infectious diseases, though to date, evidence linking climate changes and such diseases in plants has not been available. Cassava is perhaps the most important crop in Africa for smallholder farmers. Since the late 1990’s there have been reports from East and Central Africa of pandemics of begomoviruses in cassava linked to high abundances of whitefly species within the Bemisia tabaci complex. We used CLIMEX, a process-oriented climatic niche model, to explore if this pandemic was linked to recent historical climatic changes. The climatic niche model was corroborated with independent observed field abundance of B. tabaci in Uganda over a 13-year time-series, and with the probability of occurrence of B. tabaci over 2 years across the African study area. Throughout a 39-year climate time-series spanning the period during which the pandemics emerged, the modelled climatic conditions for B. tabaci improved significantly in the areas where the pandemics had been reported and were constant or decreased elsewhere. This is the first reported case where observed historical climate changes have been attributed to the increase in abundance of an insect pest, contributing to a crop disease pandemic.
The whitefly Bemisia tabaci is a closely related group of >35 cryptic species that feed on the phloem sap of a broad range of host plants. Species in the complex differ in their host‐range breadth, but the mechanisms involved remain poorly understood. We investigated, therefore, how six different B. tabaci species cope with the environmental unpredictability presented by a set of four common and novel host plants. Behavioral studies indicated large differences in performances on the four hosts and putative specialization of one of the species to cassava plants. Transcriptomic analyses revealed two main insights. First, a large set of genes involved in metabolism (>85%) showed differences in expression between the six species, and each species could be characterized by its own unique expression pattern of metabolic genes. However, within species, these genes were constitutively expressed, with a low level of environmental responsiveness (i.e., to host change). Second, within each species, sets of genes mainly associated with the super‐pathways “environmental information processing” and “organismal systems” responded to the host switching events. These included genes encoding for proteins involved in sugar homeostasis, signal transduction, membrane transport, and immune, endocrine, sensory and digestive responses. Our findings suggested that the six B. tabaci species can be divided into four performance/transcriptomic “Types” and that polyphagy can be achieved in multiple ways. However, polyphagy level is determined by the specific identity of the metabolic genes/pathways that are enriched and overexpressed in each species (the species' individual metabolic “tool kit”).
Virus disease pandemics and epidemics that occur in the world’s staple food crops pose a major threat to global food security, especially in developing countries with tropical or subtropical climates. Moreover, this threat is escalating rapidly due to increasing difficulties in controlling virus diseases as climate change accelerates and the need to feed the burgeoning global population escalates. One of the main causes of these pandemics and epidemics is the introduction to a new continent of food crops domesticated elsewhere, and their subsequent invasion by damaging virus diseases they never encountered before. This review focusses on providing historical and up-to-date information about pandemics and major epidemics initiated by spillover of indigenous viruses from infected alternative hosts into introduced crops. This spillover requires new encounters at the managed and natural vegetation interface. The principal virus disease pandemic examples described are two (cassava mosaic, cassava brown streak) that threaten food security in sub-Saharan Africa (SSA), and one (tomato yellow leaf curl) doing so globally. A further example describes a virus disease pandemic threatening a major plantation crop producing a vital food export for West Africa (cacao swollen shoot). Also described are two examples of major virus disease epidemics that threaten SSA’s food security (rice yellow mottle, groundnut rosette). In addition, brief accounts are provided of two major maize virus disease epidemics (maize streak in SSA, maize rough dwarf in Mediterranean and Middle Eastern regions), a major rice disease epidemic (rice hoja blanca in the Americas), and damaging tomato tospovirus and begomovirus disease epidemics of tomato that impair food security in different world regions. For each pandemic or major epidemic, the factors involved in driving its initial emergence, and its subsequent increase in importance and geographical distribution, are explained. Finally, clarification is provided over what needs to be done globally to achieve effective management of severe virus disease pandemics and epidemics initiated by spillover events.
The knowledge of genomic data of new plant viruses is increasing exponentially; however, some aspects of their biology, such as vectors and host range, remain mostly unknown. This information is crucial for the understanding of virus-plant interactions, control strategies, and mechanisms to prevent outbreaks. Typically, rhabdoviruses infect monocot and dicot plants and are vectored in nature by hemipteran sap-sucking insects, including aphids, leafhoppers, and planthoppers. However, several strains of a potentially whitefly-transmitted virus, papaya cytorhabdovirus, were recently described: (i) bean-associated cytorhabdovirus (BaCV) in Brazil, (ii) papaya virus E (PpVE) in Ecuador, and (iii) citrus-associated rhabdovirus (CiaRV) in China. Here, we examine the potential of the Bemisia tabaci Middle East-Asia Minor 1 (MEAM1) to transmit BaCV, its morphological and cytopathological characteristics, and assess the incidence of BaCV across bean producing areas in Brazil. Our results show that BaCV is efficiently transmitted, in experimental conditions, by B. tabaci MEAM1 to bean cultivars, and with lower efficiency to cowpea and soybean. Moreover, we detected BaCV RNA in viruliferous whiteflies but we were unable to visualize viral particles or viroplasm in the whitefly tissues. BaCV could not be singly isolated for pathogenicity tests, identification of the induced symptoms, and the transmission assay. BaCV was detected in five out of the seven states in Brazil included in our study, suggesting that it is widely distributed throughout bean producing areas in the country. This is the first report of a whitefly-transmitted rhabdovirus.
The genus Begomovirus (family Geminiviridae) is the largest genus in the entire virosphere, with more than 400 species recognized. Begomoviruses are single-stranded DNA plant viruses transmitted by whiteflies of the Bemisia tabaci complex and are considered one of the most important groups of emerging plant viruses in tropical and subtropical regions. Several types of DNA satellites have been described to be associated with begomoviruses: betasatellites, alphasatellites, and deltasatellites. Recently, a family of single-stranded DNA satellites associated with begomoviruses has been created, Tolecusatellitidae, including the genera Betasatellite and Deltasatellite. In this work, we analyzed the population of begomoviruses and associated DNA satellites present in Corchorus siliquosus, a malvaceous plant growing wild in Central America, southeastern North America and the Caribbean, collected in Cuba. The genomes of isolates of two New World begomoviruses [(Desmodium leaf distortion virus (DesLDV) and Corchorus yellow vein Cuba virus (CoYVCUV)] and two deltasatellites [tomato yellow leaf distortion deltasatellite 2 (TYLDD2) and Desmodium leaf distortion deltasatellite (DesLDD)] have been cloned and sequenced from plants showing yellow vein symptoms. Isolates of one of the begomoviruses, CoYVCUV, and one of the deltasatellites, DesLDD, represent novel species. Experiments with infectious clones showed the monopartite nature of CoYVCUV and that DesLDD utilizes the bipartite DesLDV as helper virus, but not the monopartite CoYVCUV. Also, CoYVCUV was shown to infect common bean in addition to Nicotiana benthamiana. This is the first time that (i) a monopartite New World begomovirus is found in a host other than tomato and (ii) deltasatellites have been found in C. siliquosus, thus extending the host and helper virus ranges of this recently recognized class of DNA satellites.
Significance
Viruses pose a great threat to animal and plant health worldwide. Whereas most plant viruses only replicate in plant hosts, some also replicate in their animal (insect) vector. A detailed knowledge of host expansion will give a better understanding of virus evolution, and identification of virus and host components involved in this process can lead to new strategies to combat virus spread. Here, we reveal that a plant DNA virus has evolved to induce and recruit insect DNA synthesis machinery to support its replication in vector salivary glands. Our study sheds light on the understanding of TYLCV–whitefly interactions and provides insights into how a plant virus may evolve to infect and replicate in an insect vector.
Tomato leaf curl New Delhi virus (ToLCNDV) is a bipartite begomovirus affecting tomato cultivation on the Indian subcontinent. Recently, however, a new strain of the virus, named ToLCNDV-ES, has spread to Mediterranean countries such as Spain, Italy, and Tunisia, and occurred in Cucurbita crops, causing economic damage. Although ToLCNDV is spread by the sweet potato whitefly (Bemisia tabaci), like other begomoviruses, it has not been clear how ToLCNDV suddenly spread from the Indian subcontinent to the Mediterranean region. In 2017, ToLCNDV was diagnosed in young seedlings germinated naturally from fruits fallen in the prior year on a farm located in Giugliano in Campania, Naples, Italy, suggesting a possible role of the seeds in vertical transmission of the virus. Because sweet potato whiteflies were widespread naturally in that region, it was necessary to verify that in an artificial insect vector-free condition. Seeds were harvested from two ToLCNDV-infected zucchini squash cultivars in Naples in 2017 and 2018 to examine whether ToLCNDV can be transmitted from zucchini squash seeds to young plants. Viral DNA was amplified from these seeds and 1- to 3-week-old seedlings germinated from them with a ToLCNDV-specific primer set. According to PCR results, viral contamination was confirmed from all harvested seeds and dissemination was proven from 61.36% of tested seedling samples. Mechanical transmission from seed-borne virus-infected seedlings to healthy zucchini squash plants was also succesful, demonstrating that seedlings from ToLCNDV-infected seeds did act as inoculum. This is the first report demonstrating that ToLCNDV is a seed-transmissible virus in zucchini squash plants in Italy.
Betasatellites are a group of circular, single-stranded DNA molecules that are frequently found to be associated with monopartite begomoviruses of the family Geminiviridae. Betasatellites require their helper viruses for replication, movement, and encapsidation and they are often essential for induction of typical disease symptoms. The βC1 protein encoded by betasatellites is multifunctional that participates in diverse cellular events. It interferes with several cellular processes like normal development, chloroplasts, and innate immune system of plants. Recent research has indicated βC1 protein interaction with cellular proteins and its involvement in modulation of the host’s cell cycle and symptom determination. This article focuses on the functional mechanisms of βC1 and its interactions with other viral and host proteins.
The begomoviruses are the largest and most economically important group of plant viruses transmitted exclusively by the whitefly Bemisia tabaci in a circulative, persistent manner. The circulation of the viruses within the insect vectors involves complex interactions between virus and vector components; however, the molecular mechanisms of these interactions remain largely unknown. Here we investigated the transcriptional response of the invasive B. tabaci Middle East-Asia Minor 1 species to Tomato yellow leaf curl China virus (TYLCCNV) using Illumina sequencing technology. Results showed that 1,606 genes involved in 157 biochemical pathways were differentially expressed in the viruliferous whiteflies. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicated that TYLCCNV can perturb the cell cycle and primary metabolism in the whitefly, which explains the negative effect of this virus on the longevity and fecundity of B. tabaci. Our data also demonstrated that TYLCCNV can activate whitefly immune responses, such as autophagy and antimicrobial peptide production, which might lead to a gradual decrease of viral particles within the body of the viruliferous whitefly. Furthermore, PCR results showed that TYLCCNV can invade the ovary and fat body tissues of the whitefly, and Lysotracker and Western blot analyses revealed that the invasion of TYLCCNV induced autophagy in both the ovary and fat body tissues. Surprisingly, TYLCCNV also suppressed the whitefly immune responses by downregulating the expression of genes involved in Toll-like signaling and mitogen-activated protein kinase (MAPK) pathways. Taken together, these results reveal the relationship of coevolved adaptations between begomoviruses and whiteflies and will provide a road map for future investigations into the complex interactions between plant viruses and their insect vectors.
Plant DNA viruses of the genus Begomovirus have been documented as the most genetically diverse in the family Geminiviridae and present a serious threat for global horticultural production, especially considering climate change. It is important to characterize naturally existing begomoviruses, since viral genetic diversity in non-cultivated plants could lead to future disease epidemics in crops. In this study, high-throughput sequencing (HTS) was employed to determine viral diversity of samples collected in a survey performed during 2012–2016 in seven states of Northern-Pacific Mexico, areas of diverse climatic conditions where different vegetable crops are subject to intensive farming. In total, 132 plant species, belonging to 34 families, were identified and sampled in the natural ecosystems surrounding cultivated areas (agro-ecological interface). HTS analysis and subsequent de novo assembly revealed a number of geminivirus-related DNA signatures with 80 to 100% DNA similarity with begomoviral sequences present in the genome databank. The analysis revealed DNA signatures corresponding to 52 crop-infecting and 35 non-cultivated-infecting geminiviruses that, interestingly, were present in different plant species. Such an analysis deepens our knowledge of geminiviral diversity and could help detecting emerging viruses affecting crops in different agro-climatic regions.
Many animal and plant viruses depend on arthropods for their transmission. Virus-vector interactions are highly specific and only one vector, or a group of vectors from the same family are able to transmit a given virus. Poleroviruses (Luteoviridae) are phloem-restricted RNA plant viruses, which are exclusively transmitted by aphids. Multiple aphid-transmitted polerovirus species commonly infect pepper, causing vein yellowing, leaf rolling and fruit discoloration. Despite low aphid populations, a recent outbreak with such severe symptoms in many bell pepper farms in Israel led to reinvestigation of the disease and its insect vector. Here we report that this outbreak was caused by a new whitefly ( Bemisia tabaci )-transmitted polerovirus, which we coined Pepper whitefly borne vein yellows virus (PeWBVYV). PeWBVYV is highly homologous (>95%) to Pepper vein yellows virus (PeVYV) from Israel and Greece on its 5′ end half, while it is homologous to African eggplant yellows virus (AeYV) on its 3′ half. Koch's postulates were proven by constructing a PeWBVYV infectious clone causing the pepper disease, which was in turn transmitted to test pepper plants by B. tabaci but not by aphids. PeWBVYV is the first report of a whitefly transmitted polerovirus.
Importance
High specificity of virus-vector interactions limits the possibility of a given virus to change vector. Our study reports a new virus from a family of viruses strictly transmitted by aphids, which is now transmitted by whiteflies ( Bemisia tabaci ) and not by aphids. This study constitutes the first report of a polerovirus transmission by whiteflies. Whiteflies are highly resistant to insecticides and disperse to long distances, carrying virus inoculum. Thus, the report of such unusual polerovirus transmission by a super vector has deep implications on the epidemiology of the virus disease, with ramifications on international trade of agricultural commodities.
A collection of cultivated and non-cultivated species of cotton (Gossypium spp.) has been maintained for the last four decades in Multan, Pakistan. This geographical location has been observed as a hotspot for the evolution of begomoviruses and satellites associated with cotton leaf curl disease (CLCuD). Recent studies showed that begomoviruses responsible for the CLCuD epidemic in the 1990s, and that almost disappeared from the CLCuD complex in 2000s, have been observed again in CLCuD-infected cotton fields. To identify host species that acted as probable reservoirs for these viruses, we characterized begomoviruses and satellites in non-cultivated cotton species G. raimondii, G. thurberi and G. mustelinum and identified several species of CLCuD associated begomoviruses and satellites. Further, phylogenetic analysis indicated that the identified begomoviruses and beta/alphasatellites are closely related to the ones associated with the most recent CLCuD complex. qPCR indicated that the comparative level of virus significantly decreased in the presence of alphasatellites. Our results indicated that non-cultivated cotton species have been continuously challenged by diverse begomoviruses and associated satellites and act as reservoirs for CLCuD associated begomoviruses. These results provide novel insights into understanding the spread of begomoviruses and associated satellites in New World cotton species introduced into the Old World.
Mutation, recombination and pseudo-recombination are the major forces driving the evolution of viruses by the generation of variants upon which natural selection, genetic drift and gene flow can act to shape the genetic structure of viral populations. Recombination between related virus genomes co-infecting the same cell usually occurs via template swapping during the replication process and produces a chimeric genome. The family Geminiviridae shows the highest evolutionary success among plant virus families, and the common presence of recombination signatures in their genomes reveals a key role in their evolution. This review describes the general characteristics of members of the family Geminiviridae and associated DNA satellites, as well as the extensive occurrence of recombination at all taxonomic levels, from strain to family. The review also presents an overview of the recombination patterns observed in nature that provide some clues regarding the mechanisms involved in the generation and emergence of recombinant genomes. Moreover, the results of experimental evolution studies that support some of the conclusions obtained in descriptive or in silico works are summarized. Finally, the review uses a number of case studies to illustrate those recombination events with evolutionary and pathological implications as well as recombination events in which DNA satellites are involved.
TYLCV-IS76, a unique recombinant between tomato yellow leaf curl virus (TYLCV) and tomato yellow leaf curl Sardinia virus (TYLCSV), has replaced its parental viruses in southern Morocco. To refine its emergence scenario, its fitness was monitored experimentally in conditions aiming at reproducing natural situations, i.e. superinfection of plants already infected with parental viruses and competition with other TYLCV/TYLCSV recombinants (LSRec) automatically generated in plants coinfected with TYLCV and TYLCSV. TYLCV-IS76 accumulated significantly more than parental viruses regardless of plant age and superinfection delay. Although TYLCV-IS76 and LSRec both accumulated more than parental viruses in laboratory conditions, LSRec were displaced by TYLCV-IS76 in nature like parental viruses were. TYLCV-IS76 did not exhibit any vector transmission advantage over LSRec and TYLCV the most competitive parental virus. Thus, it is apparently only in the plant compartment that the recombination event that generated TYLCV-IS76, induced the competitiveness advantage by which the last became first.
Seed transmission can be of considerable relevance to the dissemination of plant viruses in nature and for their prevalence and perpetuation. Long-distance spread of isolates of the begomovirus species Tomato leaf curl New Delhi virus (genus Begomovirus, family Geminiviridae) has recently occurred from Asia to the Middle East and the Mediterranean Basin. Here we investigated the possible transmission by melon (Cucumis melo L.) seeds of a tomato leaf curl New Delhi virus (ToLCNDV) isolate of the "Spain" strain widely distributed in the Mediterranean area as an alternative mechanism for long-distance spread. Polymerase chain reaction (PCR) amplification detection of ToLCNDV in floral parts and mature seeds of melon plants reveals that this virus is seed-borne. Seed-borne is defined as the ability of a virus to be carried through seeds, which does not necessarily lead to transmission to the next generation. Treatment with a chemical disinfectant significantly reduced the detectable virus associated with melon seeds, suggesting ToLCNDV contamination of the external portion of the seed coat. Also, when the internal fraction of the mature seed (seed cotyledons + embryo) was analyzed by quantitative PCR amplification, ToLCNDV was detectable at low levels, suggesting the potential for viral contamination or of infection of the internal portions of seed. However, grow-out studies conducted with melon progeny plants germinated from mature seeds collected from ToLCNDV-infected plants and evaluated at early (one leaf) or at late (20 leaf) growth stages did not support the transmission of ToLCNDV from seeds to offspring.
Tomato yellow leaf curl virus (TYLCV) is one of the most studied complexes of begomoviruses. Once ingested by the whitefly Bemisia tabaci during feeding, TYLCV follows an established path: ingestion, stylet, food canal, esophagus, filter chamber, midgut (MG), hemolymph, salivary glands, and egestion. Most of the virus is concentrated in the MGs. Until not long ago, TYLCV was defined as a circulative, nonpropagative begomovirus. The results accumulated during the last decade have questioned this paradigm. They have opened many questions. Among them: (1) Are TYLCVs replicating and transcribed in their B. tabaci vector? (2) Are TYLCVs transovarially transmitted to the next generation of B. tabaci? (3) If TYLCVs replicate and are transmitted to progeny, then why only TYLCVs? To review these questions, we found it necessary to describe in broad lines the experimental conditions used by the authors to obtain their results and derive their interpretation. Indeed, different protocols may lead to contradictory results. Much of the recent results discussed here need to be repeated and confirmed, while opening new avenues of research.
Plant viruses with densely packed genomes employ non-canonical translational strategies to increase the coding capacity for viral function. However, the diverse translational strategies used make it challenging to define the full set of viral genes. Here, using tomato yellow leaf curl Thailand virus (TYLCTHV, genus Begomovirus) as a model system, we identified genes beyond the annotated gene sets by experimentally profiling in vivo translation initiation sites (TISs). We found that unanticipated AUG TISs were prevalent and determined that their usage involves alternative transcriptional and/or translational start sites and is associated with flanking mRNA sequences. Specifically, two downstream in-frame TISs were identified in the viral gene AV2. These TISs were conserved in the begomovirus lineage and led to the translation of different protein isoforms localized to cytoplasmic puncta and at the cell periphery, respectively. In addition, we found translational evidence of an unexplored gene, BV2. BV2 is conserved among TYLCTHV isolates and localizes to the endoplasmic reticulum and plasmodesmata. Mutations of AV2 isoforms and BV2 significantly attenuated disease symptoms in tomato (Solanum lycopersicum). In conclusion, our study pinpointing in vivo TISs untangles the coding complexity of a plant viral genome and, more importantly, illustrates the biological significance of the hidden open reading frames encoding viral factors for pathogenicity.
Cotton leaf curl disease (CLCuD) is the most devastating disorder of cotton caused by begomoviruses (family Geminiviridae) and betasatellite complex transmitted exclusively by whiteflies (Bemisia tabaci). This disease is endemic in the Indian sub-continent and sporadically occurs in Africa. Affected plants show the distinct symptoms such as vein thickening, downward or upward leaf curling, enation formation…etc. In the Indian subcontinent, CLCuD passed through two major epidemics. In the first epidemic begomoviruses members of several species including Cotton leaf curl Kokhran virus (CLCKokV), Cotton leaf curl Multan virus (CLCMulV), Cotton leaf curl Alabad virus (CLCAlaV) and Papaya leaf curl virus (PLCV) were associated with the disease. Only a single species of betasatellite viz. Cotton leaf curl Multan betasatellite (CLCMulB) was associated with the disease. In the late of 1990s cotton production was restored by adopting some resistant varieties but soon resistance was broken in 2001 by a recombinant begomovirus viz. CLCKokV-Burewala strain. It was also associated with a recombinant CLCMulB-Bur. The spread of this disease complex caused the second epidemic of CLCuD and remained dominant in the field till 2014. Although in this period some bipartite begomoviruses were identified in cultivated cotton in Pakistan and recently also from Africa, but their role in the disease is not fully established but some evidence suggests that these bipartite begomoviruses may work synergistically with the complex monopartite begomovirus and betasatellite CLCMulB. In the year 2015, multiple begomoviruses which were associated with the first epidemic, reappeared in Pakistan and CLCMulV was also exclusively detected in India and CLCKokV-Bur was no longer a predominant strain in the field. At this time, no commercial cotton variety is resistant to CLCuD, but a new source of resistance has been identified which has been introgressed into commercial cotton. Efforts are under way to understand the genes involved in compatible interactions as well host defense response in resistance sources in order to precisely design the strategies to develop durable and broad-spectrum resistant cultivars of cotton.
Tomato leaf curl New Delhi virus (ToLCNDV) the causal agent of tomato leaf curl disease (ToLCD) has a very devastating impact on the growth and productivity of several agro-economically important plant families such as Solanaceae, Cucurbitaceae, Malvaceae, and several other crops around the world. ToLCNDV belongs to the single-stranded plant DNA Begomovirus genus of the family Geminiviridae and is transmitted by the insect vector whitefly (Bemisia tabaci Genn.). ToLCNDV induces typical symptoms of both upward and downward leaf curling, distortion of leaves, and stunted plant growth. Molecular techniques such as PCR and nanoparticle-based biosensors can be used as an effective diagnosis approach. Strategic control of ToLCNDV epidemic requires methods like marker-assisted screening, population control of viruliferous whiteflies, identification of defense-related resistance host genes, and transgenic as well as non-transgenic genetic approaches.
Cassava mosaic geminiviruses (CMGs) are a group of single-stranded DNA viruses that cause disease in cassava throughout cassava-growing regions of sub-Saharan Africa, as well as in South and South-East Asia. There are currently nine species recorded from Africa and two from Asia. All are transmitted in a persistent manner by the whitefly Bemisia tabaci, but they are also widely propagated through infected stem cuttings. Principal control efforts comprise the production and dissemination of virus-free planting material of conventionally-bred resistant varieties. RNAi and gene editing are being investigated in efforts to further strengthen control.
Tomato yellow leaf curl virus (TYLCV) is one of the most studied plant viral pathogens because it is the most damaging virus for global tomato production. In order to combat this global threat, it is important that we understand the biology of TYLCV and devise management approaches. The prime objective of this review is to highlight management strategies for efficiently tackling TYLCV epidemics and global spread. For that purpose, we focus on the impact TYLCV has on worldwide agriculture and the role of recent advances for our understanding of TYLCV interaction with its host and vector. Another important focus is the role of recombination and mutations in shaping the evolution of TYLCV genome and geographical distribution.
The severe yellowing disease (‘Amarelão’) on melon plants is a serious problem in Brazil, although the causative agent remained unknown for a long time. Recently, recombinant isolates of cucurbit aphid‐borne yellows virus (CABYV) were reported as the possible causative agents of the severe yellowing disease on melon plants. Although aphids are known to be the vectors of the common type of CABYV isolates, almost no aphid colony was observed in the major melon fields in Brazil with high incidence of the severe yellowing disease. In contrast, whiteflies are often abundant. Based on this observation, the hypothesis of the transmission of recombinant CABYV by whiteflies was evaluated. After thorough transmission experiments, we found out that this recombinant CABYV isolate was transmitted by the whitefly Bemisia tabaci MEAM1, but not by Aphis gossipii. Furthermore, the host response by whitefly‐based inoculation in cucurbits and other indicator plants showed differences in host range when compared to the common type of CABYV. Due to its transmissibility by the whitefly and the distant relationship of the P3/P5 protein to CABYV, the name “cucurbit whitefly‐borne yellows virus” is proposed for this recombinant CABYV. This is the second report of the polerovirus transmission by the whitefly B. tabaci, following the report of pepper whitefly‐borne vein yellows virus.
Recently, chili pepper (Capsicum annuum) plants in Indonesia have been devastated by a notorious bipartite begomovirus infection named Pepper yellow leaf curl Indonesia virus (PepYLCIV), which causes a distinct decrease in chili pepper production. Pepper yellow diseases have been known since early 2000; however, the spread of this virus thus far is distressing. These diseases can reduce chili yields by 20 to 100% in Indonesia. As previously known, begomovirus can be transmitted through whitefly to several host plants from the families Solanaceae, Compositae, and Leguminosae. In the field, a single plant was observed with severe symptoms of pepper yellow leaf curl disease, while other plants in the same field were asymptomatic and healthy. The observation leads to the possibility that the virus can be transmitted from previously infected chili pepper plants through seeds, as begomovirus transmission through seeds has been reported before. This study was conducted using seeds from chili peppers infected with viruses from different places in Indonesia. Whole seeds, embryos, and seedlings from PepYLCIV infected seeds were investigated in this study by performing viral genome DNA extraction, uracil DNA glycosylase-PCR, and sequencing analysis. Results revealed that both DNA-A and DNA-B of PepYLCIV in seeds and embryos of infected chili pepper plants were detected. The results also showed that 25-67% of PepYLCIV DNA-A and 50-100% of DNA-B were detected from seedlings grown from infected chili pepper seed collected from different location, thus confirming PepYLCIV as a seed-transmissible virus in chili pepper plants.
Betasatellites (DNA β) are circular ssDNA molecules that are associated with monopartite geminiviruses and exert a positive effect on the viral infection. Betasatellites encode one protein, named βC1, on the complementary strand; βC1 functions as a pathogenicity factor and RNA silencing suppressor. In this report, we describe the identification of another betasatellite-encoded protein, βVl, which also contributes to symptom development. The βVl open reading frame can be found on the viral strand of approximately 40% of reported betasatellite sequences, and is conserved in position and sequence. The presence of the βVl transcript was observed in plants infected with Tomato yellow leaf curl China virus (TYTCCNV) along with its associated betasatellite Tomato yellow leaf curl China betasatellite (TYTCCNB). Mutant viruses unable to produce βVl showed reduced virulence and decreased viral load. Ectopic expression of the TYTCCNB-PV1 gene in Nicotiana benthamiana plants from a PVX-based vector resulted in leaf mosaic and chlorosis. We further demonstrated that the βVl protein could elicit hypersensitive response (HR)-type cell death in N. benthamiana leaves. Our results uncover a novel betasatellite-encoded protein that contributes to the virus infection, and this discover gives us a more complete view of the plant-geminivirus interaction landscape.
In West and Central Africa, as in many regions of the world, vegetables are severely affected by geminivirus diseases. In Burkina Faso, observation of various virus‐like symptoms, especially on tomato, suggests the involvement of several geminiviruses and underlines the pressing need for additional information on their diversity, distribution, prevalence and host plant reservoirs. Large‐scale surveys conducted in Burkina Faso confirmed the presence of tomato (yellow) leaf curl diseases (ToLCD‐TYLCD) and geminiviruses in all localities with mean prevalences of 25% and 45%, respectively. Five geminiviruses including four begomovirus pepper yellow vein Mali virus (PepYVMLV), tomato leaf curl Burkina Faso virus, tomato leaf curl Mali virus and tomato leaf curl Ghana virus, and a dicot‐infecting mastrevirus chickpea chlorotic dwarf virus were characterised on tomato. In addition, PepYVMLV and cotton leaf curl Gezira virus (CLCuGeV) were characterised on pepper and okra, respectively, in combination or not with alphasatellites and betasatellites for CLCuGeV. The most severe, prevalent and widely distributed virus on vegetables was PepYVMLV, which was characterised for the first time in combination with a genetically divergent DNA‐B component which may constitute a key factor of PepYVMLV pathogenicity. Of the eight weeds identified as potential reservoir hosts of begomoviruses, four host PepYVMLV. Our results confirm the importance of geminivirus diseases on vegetable crops in Burkina Faso and highlight the complex association of geminiviruses and satellites. The detection of begomoviruses in weeds growing close to crops points to the increasing necessity to consider reservoir plants and virus communities in the control of virus diseases.
Isolates of Tomato yellow leaf curl virus (TYLCV) species (genus Begomovirus, family Geminiviridae) infect tomato crops worldwide causing severe economic damage. Members of the whitefly Bemisia tabaci sibling species group are the vector of begomoviruses, including TYLCV. However, transmission of isolates of the type (Israel, IL) strain of TYLCV (TYLCV-IL) by tomato seeds has recently been reported based on infections occurring in Korea. Because of the consequences of this finding on the epidemiology and control of the disease caused by TYLCV and on the seed market, it was considered essential to revisit and expand those results to other tomato-growing areas. TYLCV DNA content was detected in tomato and Nicotiana benthamiana seeds collected from plants naturally or experimentally infected with TYLCV-IL supporting seed borne nature. The TYLCV-IL replication detected in tomato and N. benthamiana flower reproductive organs demonstrated close association of this virus with the seeds during maturation. However, the significant reduction of TYLCV DNA load after surface disinfections of tomato seeds suggests that most of the virus is located externally, as contaminant of the seed coat. Transmission assays, carried out with seven tomato genotypes and more than 3000 tomato plants revealed no evidence of seed transmission from "surface disinfected" or untreated seeds for two Mediterranean isolates of TYLCV-IL. Similar results were also obtained for seeds collected from TYLCV-IL-infected N. benthamiana plants. The results support that TYLCV-IL is seed-borne but is not seed-transmitted in tomato or N. benthamiana suggesting that transmission through seeds is not a general property of TYLCV.
Most plant viruses require a biological vector to spread from plant to plant in nature. Among biological vectors for plant viruses, hemipteroid insects are the most common, including phloem-feeding aphids, whiteflies, mealybugs, planthoppers and leafhoppers. Majority of the emerging diseases challenging agriculture worldwide are insect borne, with those transmitted by whiteflies (Hemiptera: Aleyrodidae) topping the list. Most damaging whitefly-transmitted viruses include begomoviruses (Geminiviridae), criniviruses (Closteroviridae), and torradoviruses (Secoviridae). Among the whitefly vectors, Bemisia tabaci, now recognized as a complex of cryptic species, is the most harmful in terms of virus transmission. Here we review the available information on the differential transmission efficiency of begomoviruses and other whitefly-borne viruses by different species of whiteflies, including the cryptic species of the B. tabaci complex. In addition, we summarize the factors affecting transmission of viruses by whiteflies and point out some future research prospects.
Viruses constitute the largest group of emerging pathogens, and geminiviruses (plant viruses with circular, single-stranded DNA genomes) are the major group of emerging plant viruses. With their high potential for genetic variation due to mutation and recombination, their efficient spread by vectors, and their wide host range as a group, including both wild and cultivated hosts, geminiviruses are attractive models for the study of the evolutionary and ecological factors driving virus emergence. The epidemiological features of geminivirus diseases have traditionally focused primarily on crop plants. Nevertheless, knowledge of geminivirus infection in wild plants, and especially at the interface between wild and cultivated plants, is necessary to provide a complete view of their ecology, evolution, and emergence. In this review, we address the most relevant aspects of geminivirus variability and evolution in wild and crop plants and geminiviruses’ potential to emerge in crops.
Expected final online publication date for the Annual Review of Virology Volume 6 is September 30, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.