Dataset Information

Tomato Twisted Leaf Virus: A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela.

ABSTRACT: Begomoviruses are one of the major groups of plant viruses with an important economic impact on crop production in tropical and subtropical regions. The global spread of its polyphagous vector, the whitefly Bemisia tabaci, has contributed to the emergence and diversification of species within this genus. In this study, we found a putative novel begomovirus infecting tomato plants in Venezuela without a cognate DNA-B component. This begomovirus was genetically characterized and compared with related species. Furthermore, its infectivity was demonstrated by agroinoculation of infectious clones in tomato (Solanum lycopersicum) and Nicotiana benthamiana plants. The name Tomato twisted leaf virus (ToTLV) is proposed. ToTLV showed the typical genome organization of the DNA-A component of New World bipartite begomoviruses. However, the single DNA component of ToTLV was able to develop systemic infection in tomato and N. benthamiana plants, suggesting a monopartite nature of its genome. Interestingly, an additional open reading frame ORF was observed in ToTLV encompassing the intergenic region and the coat protein gene, which is not present in other closely related begomoviruses. A putative transcript from this region was amplified by strand-specific reverse transcription-PCR. Along with recent studies, our results showed that the diversity of monopartite begomoviruses from the New World is greater than previously thought.

SUBMITTER: Romay G

PROVIDER: S-EPMC6521247 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Tomato Twisted Leaf Virus: A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela.

Romay Gustavo G Geraud-Pouey Francis F Chirinos Dorys T DT Mahillon Mathieu M Gillis Annika A Mahillon Jacques J Bragard Claude C

Viruses 20190404 4

Begomoviruses are one of the major groups of plant viruses with an important economic impact on crop production in tropical and subtropical regions. The global spread of its polyphagous vector, the whitefly <i>Bemisia tabaci</i>, has contributed to the emergence and diversification of species within this genus. In this study, we found a putative novel begomovirus infecting tomato plants in Venezuela without a cognate DNA-B component. This begomovirus was genetically characterized and compared wi ...[more]

PMID: 30987360

Similar Datasets

Project description:Begomoviruses are members of the family Geminiviridae, a large and diverse group of plant viruses characterized by a small circular single-stranded DNA genome encapsidated in twinned quasi-icosahedral virions. Cultivated tomato (Solanum lycopersicum L.) is particularly susceptible and is infected by >100 bipartite and monopartite begomoviruses worldwide. In Brazil, 25 tomato-infecting begomoviruses have been described, most of which are bipartite. Tomato mottle leaf curl virus (ToMoLCV) is one of the most important of these and was first described in the late 1990s but has not been fully characterized. Here, we show that ToMoLCV is a monopartite begomovirus with a genomic DNA similar in size and genome organization to those of DNA-A components of New World (NW) begomoviruses. Tomato plants agroinoculated with the cloned ToMoLCV genomic DNA developed typical tomato mottle leaf curl disease symptoms, thereby fulfilling Koch's postulates and confirming the monopartite nature of the ToMoLCV genome. We further show that ToMoLCV is transmitted by whiteflies, but not mechanically. Phylogenetic analyses placed ToMoLCV in a distinct and strongly supported clade with other begomoviruses from northeastern Brazil, designated the ToMoLCV lineage. Genetic analyses of the complete sequences of 87 ToMoLCV isolates revealed substantial genetic diversity, including five strain groups and seven subpopulations, consistent with a long evolutionary history. Phylogeographic models generated with partial or complete sequences predicted that the ToMoLCV emerged in northeastern Brazil >700 years ago, diversifying locally and then spreading widely in the country. Thus, ToMoLCV emerged well before the introduction of MEAM1 whiteflies, suggesting that the evolution of NW monopartite begomoviruses was facilitated by local whitefly populations and the highly susceptible tomato host. IMPORTANCE Worldwide, diseases of tomato caused by whitefly-transmitted geminiviruses (begomoviruses) cause substantial economic losses and a reliance on insecticides for management. Here, we describe the molecular and biological properties of tomato mottle leaf curl virus (ToMoLCV) from Brazil and establish that it is a NW monopartite begomovirus indigenous to northeastern Brazil. This answered a long-standing question regarding the genome of this virus, and it is part of an emerging group of these viruses in Latin America. This appears to be driven by widespread planting of the highly susceptible tomato and by local and exotic whiteflies. Our extensive phylogenetic studies placed ToMoLCV in a distinct strongly supported clade with other begomoviruses from northeastern Brazil and revealed new insights into the origin of Brazilian begomoviruses. The novel phylogeographic analysis indicated that ToMoLCV has had a long evolutionary history, emerging in northeastern Brazil >700 years ago. Finally, the tools used here (agroinoculation system and ToMoLCV-specific PCR test) and information on the biology of the virus (host range and whitefly transmission) will be useful in developing and implementing integrated pest management (IPM) programs targeting ToMoLCV.

Project description:Begomoviruses (Family Geminiviridae) are a major group of emerging plant viruses worldwide. The knowledge of begomoviruses is mostly restricted to crop plant systems. Nevertheless, it has been described that non-cultivated plants are important reservoirs and vessels of viral evolution that leads to the emergence of new diseases. High-throughput sequencing (HTS) has provided a powerful tool for speeding up the understanding of molecular ecology and epidemiology of plant virome and for discovery of new viral species. In this study, by performing earlier metagenomics library data mining, followed by geminivirus-related signature single plant searching and RCA-based full-length viral genome cloning, and based on phylogenetic analysis, genomes of two isolates of a novel monopartite begomovirus species tentatively named Galium leaf distortion virus (GLDV), which infects non-cultivated endemic plant Galium mexicanum, were identified in Colima, Mexico. Analysis of the genetic structure of both isolates (GLDV-1 and GLDV-2) revealed that the GLDV genome displays a DNA-A-like structure shared with the new world (NW) bipartite begomoviruses. Nonetheless, phylogenetic analysis using representative members of the main begomovirus American clades for tree construction grouped both GLDV isolates in a clade of the monopartite NW begomovirus, Tomato leaf deformation virus (ToLDeV). A comparative analysis of viral replication regulatory elements showed that the GLDV-1 isolate possesses an array and sequence conservation of iterons typical of NW begomovirus infecting the Solanaceae and Fabaceae families. Interestingly, GLDV-2 showed iteron sequences described only in monopartite begomovirus from OW belonging to a sweepovirus clade that infects plants of the Convolvulaceae family. In addition, the rep iteron related-domain (IRD) of both isolates display FRVQ or FRIS amino acid sequences corresponding to NW and sweepobegomovirus clades for GMV-1 and GMV-2, respectively. Finally, the lack of the GLDV DNA-B segment (tested by molecular detection and biological assays using GLDV-1/2 infectious clones) confirmed the monopartite nature of GLDV. This is the first time that a monopartite begomovirus is described in Mexican ecosystems, and "in silico" geometagenomics analysis indicates that it is restricted to a specific region. These data revealed additional complexity in monopartite begomovirus genetics and geographic distribution and highlighted the importance of metagenomic approaches in understanding global virome ecology and evolution.

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.

Dataset Information

Tomato Twisted Leaf Virus: A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela.

Publications

Tomato Twisted Leaf Virus: A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets