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Biology and Interaction of the Natural Occurrence of Distinct Monopartite Begomoviruses Associated With Satellites in Capsicum annum From India.

ABSTRACT: Chili (Capsicum annuum L.) is an important vegetable and spice crop of tropical and sub-tropical regions. Chili plants showing upward leaf curling, leaf crinkling, and leaf yellowing symptoms, collected from Sikar district of Rajasthan, India, were found to be associated with begomovirus and satellite molecules. The presence of virus was confirmed by PCR using virus-specific primer. The full-length genomic DNA-A of three begomovirus (MM-1, CS-1 and RV-1) and two satellites (MM-2 and MM-3) were cloned which was identified from single symptomatic chili plant. The genome organization of isolated three viruses is similar to those of other Old World monopartite begomoviruses. The comparison of the sequences and closest phylogenetic relationships for the begomoviruses, betasatellite and alphasatellite DNAs revealed that MM-1 was designated as DNA-A of Chili leaf curl virus (ChiLCV), CS-1 is considered to be a new distinct species of Tomato leaf curl Gujrat virus (ToLCGV) whereas RV-1 as a new strain of Cotton leaf curl Multan virus (CLCuMuV). The DNA-A component of ChiLCV showed 8.6%, ToLCGV of 16.6% and CLCuMuV of 7.7% average evolutionary divergence, concomitantly, the betasatellite and alphasatellite molecule had 9.9% and 5.9% overall sequence divergence, respectively. Interestingly, most of the begomoviruses were found to be intra-species recombinants. The dN/dS ratio and Tajima D value of all viral DNA-A component and their associated betasatellite showed their selective control on evolutionary relationships. The nucleotide substitution rates were determined for the DNA-A genomes of ChiLCV (7.22 × 10-4 substitutions site-1 year-1), CLCuMuV (1.49 × 10-4 substitutions site-1 year-1), ToLCGV (7.47 × 10-4 substitutions site-1 year-1), the genome of associated ChiLCB (4.20 × 10-4 substitutions site-1 year-1) and CLCuMuA (1.49 × 10-4 substitutions site-1 year-1). Agro-inoculation studies indicate that the presence of DNA betasatellite induce severe symptoms in N. benthamiana and chili, suggesting prerequisite association for typical disease development.

SUBMITTER: Mishra M

PROVIDER: S-EPMC7575687 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Biology and Interaction of the Natural Occurrence of Distinct Monopartite Begomoviruses Associated With Satellites in <i>Capsicum annum</i> From India.

Mishra Megha M Verma Rakesh Kumar RK Marwal Avinash A Sharma Pradeep P Gaur R K RK

Frontiers in microbiology 20201007

Chili (<i>Capsicum annuum</i> L.) is an important vegetable and spice crop of tropical and sub-tropical regions. Chili plants showing upward leaf curling, leaf crinkling, and leaf yellowing symptoms, collected from Sikar district of Rajasthan, India, were found to be associated with begomovirus and satellite molecules. The presence of virus was confirmed by PCR using virus-specific primer. The full-length genomic DNA-A of three begomovirus (MM-1, CS-1 and RV-1) and two satellites (MM-2 and MM-3) ...[more]

PMID: 33117300

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Project description:BackgroundTomato leaf curl viruses, which are the members of the genus Begomovirus, have emerged as devastating pathogens worldwide causing huge economic losses and threatening production of crops like cassava, cotton, grain legumes and vegetables. Even though the ToLCV isolates from Northern India have been shown to possess bipartite genome (designated as DNA A and DNA B), those from Australia, Taiwan and Southern India have a single genomic component (DNA A). We describe here the genetic diversity of two isolates of monopartite Tomato leaf curl virus infecting tomato in two extreme regions (North and South) of Indian subcontinent.ResultsThe rolling circle amplification (RCA) products obtained from symptomatic samples were digested, cloned and sequenced. The complete DNA sequence of two Tomato leaf curl virus isolates identified as ToLCV-CTM (India, New Delhi, 2005) and ToLCVK3/K5 (India, Kerala, 2008) are reported here. These isolates had the characteristic features of Begomovirus genome organization with six conserved open reading frames (ORFs). The ToLCV-K3 and ToLCV-K5 isolates may be the strains of the same virus since they show sequence homology of 97% over their entire genome. This, according to the guidelines established by the ICTV Geminiviridae Study-Group is higher than threshold (92%) for delineation of different viral variants and hence single, average value has been assigned for all their analyses presented here. The ToLCV-CTM and ToLCV-K3/K5 viruses were found to be monopartite, as neither DNA-B component nor betasatellite associated with begomovirus species, were detected. The complete nucleotide sequence of DNA-A genome of CTM exhibited highest sequence homology (88%) to Croton yellow vein mosaic virus (AJ507777), and of isolates K3/K5 (88.5%) to Tomato leaf curl Pakistan virus (DQ116884). This is less than the threshold value for demarcation of species in the genus Begomovirus.ConclusionK3/K5 and CTM are considered to be novel isolates of Tomato leaf curl virus. Sequence analyses and phylogenetic study indicate that these two ToLCV isolates might have evolved by recombination between viruses related to two or more viral ancestors. The existence of different ToLCV isolates having high genome diversity in India poses a threat to the tomato production in the Asian continent.

Project description:BACKGROUND: Emerging whitefly transmitted begomoviruses are major pathogens of vegetable and fibre crops throughout the world, particularly in tropical and sub-tropical regions. Mutation, pseudorecombination and recombination are driving forces for the emergence and evolution of new crop-infecting begomoviruses. Leaf curl disease of field grown radish plants was noticed in Varanasi and Pataudi region of northern India. We have identified and characterized two distinct monopartite begomoviruses and associated beta satellite DNA causing leaf curl disease of radish (Raphanus sativus) in India. RESULTS: We demonstrate that RaLCD is caused by a complex of two Old World begomoviruses and their associated betasatellites. Radish leaf curl virus-Varanasi is identified as a new recombinant species, Radish leaf curl virus (RaLCV) sharing maximum nucleotide identity of 87.7% with Tomato leaf curl Bangladesh virus-[Bangladesh:2] (Accession number AF188481) while the virus causing radish leaf curl disease-Pataudi is an isolate of Croton yellow vein mosaic virus-[India] (CYVMV-IN) (Accession number AJ507777) sharing 95.8% nucleotide identity. Further, RDP analysis revealed that the RaLCV has a hybrid genome, a putative recombinant between Euphorbia leaf curl virus and Papaya leaf curl virus. Cloned DNA of either RaLCV or CYVMV induced mild leaf curl symptoms in radish plants. However, when these clones (RaLCV or CYVMV) were individually co-inoculated with their associated cloned DNA betasatellite, symptom severity and viral DNA levels were increased in radish plants and induced typical RaLCD symptoms. To further extend these studies, we carried out an investigation of the interaction of these radish-infecting begomoviruses and their associated satellite, with two tomato infecting begomoviruses (Tomato leaf curl Gujarat virus and Tomato leaf curl New Delhi virus). Both of the tomato-infecting begomoviruses showed a contrasting and differential interaction with DNA satellites, not only in the capacity to interact with these molecules but also in the modulation of symptom phenotypes by the satellites. CONCLUSION: This is the first report and experimental demonstration of Koch's postulate for begomoviruses associated with radish leaf curl disease. Further observations also provide direct evidence of lateral movement of weed infecting begomovirus in the cultivated crops and the present study also suggests that the exchange of betasatellites with other begomoviruses would create a new disease complex posing a serious threat to crop production.

Project description:The genus Begomovirus represents a group of multipartite viruses that significantly damage many agricultural crops, including papaya, and influence overall production. Papaya leaf curl disease (PaLCD) caused by the complex begomovirus species has several important implications and substantial losses in papaya production in many developing countries, including India. The increase in the number of begomovirus species poses a continuous threat to the overall production of papaya. Here, we attempted to map the genomic variation, mutation, evolution rate, and recombination to know the disease complexity and successful adaptation of PaLCD in India. For this, we retrieved 44 DNA-A and 26 betasatellite sequences from GenBank reported from India. An uneven distribution of evolutionary divergence has been observed using the maximum-likelihood algorithm across the branch length. Although there were phylogenetic differences, we found high rates of nucleotide substitution mutation in both viral and sub-viral genome datasets. We demonstrated frequent recombination of begomovirus species, with a maximum in intra-species recombinants. Furthermore, our results showed a high degree of genetic variability, demographic selection, and mean substitution rate acting on the population, supporting the emergence of a diverse and purifying selection of viruses and associated betasatellites. Moreover, variation in the genetic composition of all begomovirus datasets revealed a predominance of nucleotide diversity principally driven by mutation, which might further accelerate the advent of new strains and species and their adaption to various hosts with unique pathogenicity. Therefore, the finding of genetic variation and selection emphases on factors that contribute to the universal spread and evolution of Begomovirus and this unanticipated diversity may also provide guidelines toward future evolutionary trend analyses and the development of wide-ranging disease control strategies for begomoviruses associated with PaLCD.

Project description:The studies on the prevalence and genetic diversity of begomoviruses in Saudi Arabia are minimal. In this study, field-grown symptomatic tomato and muskmelon plants were collected, and initially, begomovirus infection was confirmed by the core coat protein sequences. Four tomato and two muskmelon plants with viral infections were further evaluated for Illumina MiSeq sequencing, and twelve sequences (2.7-2.8 kb) equivalent to the full-length DNA-A or DNA-B components of begomoviruses were obtained along with eight sequences (~1.3-1.4 kb) equivalent to the begomovirus-associated DNA-satellite components. Four begomovirus sequences obtained from tomato plants were variants of tomato yellow leaf curl virus (TYLCV) with nt sequence identities of 95.3-100%. Additionally, two tomato plants showed a mixed infection of TYLCV and cotton leaf curl Gezira virus (CLCuGeV), okra yellow crinkle Cameroon alphasatellite (OYCrCMA), and okra leaf curl Oman betasatellite (OLCuOMB). Meanwhile, from muskmelon plants, two sequences were closely related (99-99.6%) to the tomato leaf curl Palampur virus (ToLCPalV) DNA-A, whereas two other sequences showed 97.9-100% sequence identities to DNA-B of ToLCPalV, respectively. Complete genome sequences of CLCuGeV and associated DNA-satellites were also obtained from these muskmelon plants. The nt sequence identities of the CLCuGeV, OYCrCMA, and OLCuOMB isolates obtained were 98.3-100%, 99.5-100%, and 95.6-99.7% with their respective available variants. The recombination was only detected in TYLCV and OLCuOMB isolates. To our knowledge, this is the first identification of a mixed infection of bipartite and monopartite begomoviruses associated with DNA-satellites from tomato and muskmelon in Saudi Arabia. The begomovirus variants reported in this study were clustered with Iranian isolates of respective begomovirus components in the phylogenetic dendrogram. Thus, the Iranian agroecological route can be a possible introduction of these begomoviruses and/or their associated DNA-satellites into Saudi Arabia.

Project description:UnlabelledIn contrast to begomoviruses, mastreviruses have not previously been shown to interact with satellites. This study reports the first identification of the association of satellites with a mastrevirus in field-grown plants. Two alphasatellite species were detected in different field samples of wheat infected with Wheat Dwarf India Virus (WDIV), a Cotton leaf curl Multan alphasatellite (CLCuMA) and a Guar leaf curl alphasatellite (GLCuA). In addition to the alphasatellites, a betasatellite, Ageratum yellow leaf curl betasatellite (AYLCB), was also identified in the wheat samples. No begomovirus was detected in the wheat samples, thus establishing association of the above-named satellites with WDIV. Agrobacterium-mediated inoculation of WDIV in wheat, in the presence of either of the alphasatellites or the betasatellite, resulted in infections inducing more severe symptoms. WDIV efficiently maintained each of the alphasatellites and the betasatellite in wheat. The satellites enhanced the level of WDIV DNA in wheat. Inoculation of the satellites isolated from wheat with various begomoviruses into Nicotiana tabacum demonstrated that these remain capable of interacting with the viruses with which they were first identified. Virus-specific small RNAs accumulated in wheat upon infection with WDIV but were lower in abundance in plants coinfected with the satellites, suggesting that both the alphasatellites and the betasatellite suppress RNA silencing. These results suggest that the selective advantage for the maintenance of the alphasatellites and the betasatellite by WDIV in the field is in overcoming RNA silencing-mediated host defense.ImportanceWheat is the most widely cultivated cereal crop in the world. A number of viruses are important pathogens of wheat, including the viruses of the genus Mastrevirus, family Geminiviridae. This study reports the association of subgenomic components, called satellites (alpha- and betasatellites), with a mastrevirus, Wheat Dwarf India Virus (WDIV), isolated from two distant locations in India. This study reports the first identification of the satellites in a monocot plant. The satellites enhanced accumulation of WDIV and severity of disease symptoms. The satellites lowered the concentration of virus-specific small RNAs in wheat plants, indicating their silencing suppressor activity. The involvement of the satellites in symptom severity of the mastrevirus can have implications in the form of economic impact of the virus on crop yield. Understanding the role of the satellites in disease severity is important for developing disease management strategies.

Dataset Information

Biology and Interaction of the Natural Occurrence of Distinct Monopartite Begomoviruses Associated With Satellites in Capsicum annum From India.

Publications

Biology and Interaction of the Natural Occurrence of Distinct Monopartite Begomoviruses Associated With Satellites in <i>Capsicum annum</i> From India.

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