Frequent migration of introduced cucurbit-infecting begomoviruses among Middle Eastern countries

Abstract

Background: In the early 2000s, two cucurbit-infecting begomoviruses were introduced into the eastern Mediterranean basin: the Old World Squash leaf curl virus (SLCV) and the New World Watermelon chlorotic stunt virus (WmCSV). These viruses have been emerging in parallel over the last decade in Egypt, Israel, Jordan, Lebanon and Palestine.

Methods: We explored this unique situation by assessing the diversity and biogeography of the DNA-A component of SLCV and WmCSV in these five countries.

Results: There was fairly low sequence variation in both begomovirus species (SLCV π = 0.0077; WmCSV π = 0.0066). Both viruses may have been introduced only once into the eastern Mediterranean basin, but once established, these viruses readily moved across country boundaries. SLCV has been introduced at least twice into each of all five countries based on the absence of monophyletic clades. Similarly, WmCSV has been introduced multiple times into Jordan, Israel and Palestine.

Conclusions: We predict that uncontrolled movement of whiteflies among countries in this region will continue to cause SLCV and WmCSV migration, preventing strong genetic differentiation of these viruses among these countries.

Figure 1

Sampling locations. Squash fields sampled are shown as circles, and watermelon fields as squares. Sites in Egypt are shown in shades of red, in Israel in shades of blue, Jordan in shades of green, Lebanon in shades of yellow and in Palestine in shades of purple. The background image is from primap.com, which grants unrestricted permission for noncommercial use.

Figure 2

Maximum likelihood unrooted phylogeny of SLCV DNA-A isolated in this study, created in PAUP* using a general time reversible nucleotide substitution model with a gamma distribution of site heterogeneity. Sequences from Egypt (EG) are shown in shades of red, from Israel (IL) in shades of blue, Jordan (JO) in shades of green, Lebanon (LB) in shades of yellow and the regions of Palestine governed by the Palestinian Authority (PA) in shades of purple. Sequences from a common site were shown in the same shade, up to four sites per country. Bootstrap support of ≥85% from both PAUP* and RaxML trees is shown by a solid circle; an open circle denotes ≥85% support from only RaxML.

Figure 3

Maximum likelihood unrooted phylogeny of WmCSV DNA-A isolated in this study, created in PAUP* using a transitional nucleotide substitution model with a gamma distribution of site heterogeneity. Sequences from Israel (IL) in shades of blue, Jordan (JO) in shades of green, and the regions of Palestine governed by the Palestinian Authority (PA) in shades of purple. No WmCSV samples were isolated in Egypt and Lebanon during this study. Sequences from a common site were shown in the same shade, up to three sites per country. Bootstrap support of ≥85% from both PAUP* and RaxML trees is shown by a solid circle; an open circle denotes ≥85% support from only RaxML.

Figure 4

Maximum likelihood midpoint-rooted phylogeny of SLCV DNA-A both isolated in this study and from GenBank, created in PAUP* using a Tamura-Nei nucleotide substitution model with a gamma distribution of site heterogeneity. The locations from which various GenBank sequences were isolated, where available, were obtained from the GenBank file or from the associated publications. Sequences from Egypt (EG) are shown in red, from Israel (IL) in blue, Jordan (JO) in green, Lebanon (LB) in yellow and the regions of Palestine governed by the Palestinian Authority (PA) in purple. Sequences from all other countries are shown in black, with their two-letter country code preceding the accession number. Bootstrap support of ≥85% from both PAUP* and RaxML trees is shown by a solid circle; an open circle denotes ≥85% support from only RaxML. The closely related Rhynchosia golden mosaic Sinaloa virus (RhMSV) is also included, and serves as an outgroup.

Figure 5

Maximum likelihood midpoint-rooted phylogeny of WmCSV DNA-A both isolated in this study and from GenBank, created in PAUP* using a Kimura two-parameter nucleotide substitution model with a gamma distribution of site heterogeneity and a parameter for the proportion of invariant sites. The locations from which various GenBank sequences were isolated, where available, were obtained from the GenBank file or from the associated publications. Sequences from Israel (IL) are shown in blue, Jordan (JO) in green, Lebanon (LB) in yellow and the regions of Palestine governed by the Palestinian Authority (PA) in purple. Sequences from all other countries are shown in black, with their two-letter country code preceding the accession number. Bootstrap support of ≥85% from both PAUP* and RaxML is shown by a solid circle.