The spread of tomato yellow leaf curl virus from the Middle East to the world

Abstract

The ongoing global spread of Tomato yellow leaf curl virus (TYLCV; Genus Begomovirus, Family Geminiviridae) represents a serious looming threat to tomato production in all temperate parts of the world. Whereas determining where and when TYLCV movements have occurred could help curtail its spread and prevent future movements of related viruses, determining the consequences of past TYLCV movements could reveal the ecological and economic risks associated with similar viral invasions. Towards this end we applied Bayesian phylogeographic inference and recombination analyses to available TYLCV sequences (including those of 15 new Iranian full TYLCV genomes) and reconstructed a plausible history of TYLCV's diversification and movements throughout the world. In agreement with historical accounts, our results suggest that the first TYLCVs most probably arose somewhere in the Middle East between the 1930s and 1950s (with 95% highest probability density intervals 1905-1972) and that the global spread of TYLCV only began in the 1980s after the evolution of the TYLCV-Mld and -IL strains. Despite the global distribution of TYLCV we found no convincing evidence anywhere other than the Middle East and the Western Mediterranean of epidemiologically relevant TYLCV variants arising through recombination. Although the region around Iran is both the center of present day TYLCV diversity and the site of the most intensive ongoing TYLCV evolution, the evidence indicates that the region is epidemiologically isolated, which suggests that novel TYLCV variants found there are probably not direct global threats. We instead identify the Mediterranean basin as the main launch-pad of global TYLCV movements.

Figure 1. Maximum likelihood phylogenetic tree (constructed with GTR+G₄ selected as the best fit model by RDP3 and rooted using a tomato yellow leaf curl Mali virus, or TYLCMV, isolate) depicting the relatedness of representative TYLCV full genome sequences.

While branches supported in >90% of bootstrap replicates are marked with filled circles, those supported in >70% of replicates are marked with open circles, and those supported in <50% of replicates have been collapsed. Twelve unique recombination events yielding ten different recombination patterns are presented to the right of the tree. Whereas green colours indicate TYLCV derived sequences all other colours indicate sequences derived from non-TYLCV sources. Recombination events are numbered according to Table 1.

Figure 2. Maximum clade credibility trees constructed from the TYLCV coat protein (CP) dataset.

Branches are coloured according to the most probable location state of their descendant nodes. The time-scale of evolutionary changes represented in the tree is indicated by the scale bar below it. Sequence accession numbers are coloured based on the TYLCV strains the sequences belong to. Sequences that are IL and Mld- like but which could not be confidently assigned to either strain because no corresponding full length sequences are available are coloured in black. Whereas filled circles associated with branches indicate >95% posterior probability support, open circles indicate branches with >50% posterior support. Branches with <50% support are unlabeled.

Figure 3. TYLCV migration events inferred using the coat protein (CP) and full genome (FG) datasets.

Sampling locations are indicated using circles that are coloured depending on the discreet sequence groupings they were assigned to during our phylogeography analyses (indicated by transparent coloured areas). Virus movements implied by location state transitions along the branches of the CP (see Figure 2) and FG MCC trees are indicated using arrows. Arrow colours depict the mean ages (in years) of the movements that they represent (inferred using the CP dataset and coloured according to the colour scale on the left of the figure). The thickness of arrows indicating movements between two locations indicate the over-all Bayes factor test support for epidemiological linkage between the locations. Whereas individual migration events inferred with both the CP and FG datasets are represented using solid arrows, events inferred with only the CP or the FG dataset are represented with dotted and dashed lines respectively.