Characterization of a New World Monopartite Begomovirus Causing Leaf Curl Disease of Tomato in Ecuador and Peru Reveals a New Direction in Geminivirus Evolution

Abstract

All characterized whitefly-transmitted geminiviruses (begomoviruses) with origins in the New World (NW) have bipartite genomes composed of a DNA-A and DNA-B component. Recently, an NW begomovirus lacking a DNA-B component was associated with tomato leaf curl disease (ToLCD) in Peru, and it was named Tomato leaf deformation virus (ToLDeV). Here, we show that isolates of ToLDeV associated with ToLCD in Ecuador and Peru have a single, genetically diverse genomic DNA that is most closely related to DNA-A components of NW bipartite begomoviruses. Agroinoculation of multimeric clones of the genomic DNA of three ToLDeV genotypes (two variants and a strain) resulted in the development of tomato leaf curl symptoms indistinguishable from those of ToLCD in Ecuador and Peru. Biological properties of these ToLDeV genotypes were similar to those of Old World (OW) monopartite tomato-infecting begomoviruses, including lack of sap transmissibility, phloem limitation, a resistance phenotype in tomato germplasm with the Ty-1 gene, and functional properties of the V1 (capsid protein) and C4 genes. Differences in symptom phenotypes induced by the ToLDeV genotypes in tomato and Nicotiana benthamiana plants were associated with a highly divergent left intergenic region and C4 gene. Together, these results establish that ToLDeV is an emergent NW monopartite begomovirus that is causing ToLCD in Ecuador and Peru. This is the first report of an indigenous NW monopartite begomovirus, and evidence is presented that it emerged from the DNA-A component of a NW bipartite progenitor via convergent evolution and recombination.

Complexity of begomovirus and betasatellite populations associated with chilli leaf curl disease in India

“…ChiLCD-associated begomoviruses possess higher genetic variability than observed in other begomoviruses (Melgarejo et al, 2013;Rocha et al, 2013;Silva et al, 2012). As described by Lima et al (2013), the nucleotide diversity in these begomoviruses was noticed to be non-uniformly distributed throughout the genome.…”

“…Begomoviruses are widely distributed geographically, are transmitted through the arthropod vector Bemisia tabaci, and are further classified as monopartite with a DNA-A-like component or as bipartite containing DNA-A and DNA-B (Brown et al, 2012). The majority of the monopartite begomoviruses have been reported from the 'Old World' while the begomoviruses of the 'New World' are mostly bipartite, along with a true monopartite begomovirus (Melgarejo et al, 2013;Nawaz-ulRehman & Fauquet, 2009). Generally, DNA-A encodes six ORFs necessary for virus replication, transcription activation and encapsidation, while the proteins encoded by the DNA-B component facilitate cell-cell and nucleocytoplasmic trafficking of the viral genome.…”

SnRK1 Phosphorylation of AL2 Delays Cabbage Leaf Curl Virus Infection in Arabidopsis

“…An AL2/C2 protein sequence from one isolate of each viral species in the begomovirus, curtovirus, and topocuvirus lists assembled previously (46) was selected. The C2 protein of the newly discovered monopartite New World begomovirus Tomato leaf deformation virus (ToLDeV) was included in the list (47). The selected AL2/C2 amino acid sequences were aligned by use of the CLUSTAL program and used to construct a phylogenetic tree by the neighbor-joining method with the software package MEGA (version 4.0).…”

Peptide Aptamers That Bind to Geminivirus Replication Proteins Confer a Resistance Phenotype to Tomato Yellow Leaf Curl Virus and Tomato Mottle Virus Infection in Tomato

“…We also quantified viral DNA accumulation in TYLCV-inoculated and mock-inoculated plants at 14,21, and 28 dpi using leaf disc prints hybridized with a 32 P-labeled TYLCV DNA probe (Fig. 3D).…”

“…Many geminiviruses associate with small satellite DNA molecules that carry genes encoding pathogenicity determinants that can also recombine and further contribute to genetic variability and rapid virus evolution in the field (13). All of these properties facilitate the emergence of new and morevirulent viruses (7,14). Given the complexity and dynamic nature of geminivirus disease complexes, it is essential to develop novel strategies that target multiple viruses and result in stable, broadbased disease resistance.…”