Identification of the Begomoviruses Squash Leaf Curl Virus and Watermelon Chlorotic Stunt Virus in Various Plant Samples in North America

Abstract

Geminiviruses are a group of plant-infecting viruses with single-stranded DNA genomes. Within this family, viruses in the genus Begomovirus are known to have a worldwide distribution causing a range of severe diseases in a multitude of dicotyledonous plant species. Begomoviruses are transmitted by the whitefly Bemisia tabaci, and their ssDNA genomes can be either monopartite or bipartite. As part of a viral survey, various plants including those in the families Alliaceae, Amaranthaceae, Apiaceae, Asteraceae, Brassicaceae, Cactaceae, Cucurbitaceae, Lamiaceae, Lauraceae, Malvaceae, Oleaceae and Solanaceae were sampled and screened for begomoviruses using both a high-throughput sequencing and a begomovirus-specific primer pair approach. Based on the sequences derived using these approaches, the full-length genome of various begomoviruses were amplified from plants using abutting primers. Squash leaf curl virus (SLCV) and watermelon chlorotic stunt virus (WCSV) were identified in Cactaceae (n = 25), Solanaceae (n = 7), Cucurbitaceae (n = 2) and Lamiaceae (n = 1) samples. WCSV is an Old World bipartite begomovirus that has only recently been discovered infecting watermelons in the Americas. Our discovery of WCSV in the USA is the first indication that it has reached this country and indicates that this virus might be widespread throughout North America. Phylogenetic analysis suggests WCSV was introduced to the New World twice. The detection of begomoviruses in cactus plants suggests possible spillover events from agricultural areas into native vegetation. Since WCSV and SLCV have previously been found in mixed infections, pseudo-recombination infection experiments were conducted. We demonstrate that WCSV DNA-B is successfully trans-replicated by SLCV DNA-A despite very low degree of similarity between the replication-associated iterative sequences present in their common region, an essential feature for binding of the replication associated protein. This study highlights the importance of viral surveys for the detection of spillover events into native vegetation, but also suggests the need for more surveillance of WCSV in the USA, as this virus is a serious threat to watermelon cultivation in the Middle East.

Reassortments in single-stranded DNA multipartite viruses: Confronting expectations based on molecular constraints with field observations

“…The sequence, number, and arrangement of iterons (relative position and spacing between them) can vary between genera and species ( Argüello-Astorga et al. 1994 ; Fontenele et al. 2021 ).…”

“…2008 ). Moreover, viable reassortants have been produced despite significant differences in iteron sequences or in iteron spatial arrangement ( Garrido-Ramirez, Sudarshana, and Gilbertson 2000 ; Fontenele et al. 2021 ).…”

“…Most of the related research focuses on experimental production of reassortants to evaluate the compatibility of isolates or species of interest in natural populations and anticipate potential agricultural threats ( Crespo-Bellido et al. 2021 ; Fontenele et al. 2021 ; Maliano et al.…”

Phylogeographic analysis ofBegomoviruscoat and replication-associated proteins

“…Regardless, geographically named clades may be of decreasing importance in begomovirology in upcoming decades. Several important plant host-virus pairs have resulted from 'new encounters' [77,[81][82][83], and the two large geographically defined lineages are no longer fully distinct, as evidenced by the recombinant origin of tomato latent virus [57] after the worldwide spread of TYLCV.…”

High-Throughput Sequencing Identified Distinct Bipartite and Monopartite Begomovirus Variants Associated with DNA-Satellites from Tomato and Muskmelon Plants in Saudi Arabia

“…Some of the recent examples include the spread of tomato yellow leaf curl virus (TYLCV) from the OW into the NW during the 1990s [ 12 ], the spread of NW squash leaf curl virus into the Middle East [ 13 ], and the spread of cotton leaf curl disease (CLCuD) from the Indo–Pak subcontinent into China [ 14 ]. A most recent example is the cross-continental spread of OW watermelon chlorotic stunt virus (WmCSV) into Mexico and the USA [ 15 , 16 ]. The discovery of tomato leaf curl Palampur virus (ToLCPMV) in cucurbits, tomato, and melon crops in Iran is another instance of long-distance begomovirus spread [ 17 ].…”