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. 2012 Nov 27:12:228.
doi: 10.1186/1471-2148-12-228.

East African cassava mosaic-like viruses from Africa to Indian ocean islands: molecular diversity, evolutionary history and geographical dissemination of a bipartite begomovirus

Alexandre De Bruyn  1 , Julie Villemot, Pierre Lefeuvre, Emilie Villar, Murielle Hoareau, Mireille Harimalala, Anli L Abdoul-Karime, Chadhouliati Abdou-Chakour, Bernard Reynaud, Gordon W Harkins, Arvind Varsani, Darren P Martin, Jean-Michel Lett
Affiliations

East African cassava mosaic-like viruses from Africa to Indian ocean islands: molecular diversity, evolutionary history and geographical dissemination of a bipartite begomovirus

Alexandre De Bruyn et al. BMC Evol Biol. .

Abstract

Background: Cassava (Manihot esculenta) is a major food source for over 200 million sub-Saharan Africans. Unfortunately, its cultivation is severely hampered by cassava mosaic disease (CMD). Caused by a complex of bipartite cassava mosaic geminiviruses (CMG) species (Family: Geminivirideae; Genus: Begomovirus) CMD has been widely described throughout Africa and it is apparent that CMG's are expanding their geographical distribution. Determining where and when CMG movements have occurred could help curtail its spread and reveal the ecological and anthropic factors associated with similar viral invasions. We applied Bayesian phylogeographic inference and recombination analyses to available and newly described CMG sequences to reconstruct a plausible history of CMG diversification and migration between Africa and South West Indian Ocean (SWIO) islands.

Results: The isolation and analysis of 114 DNA-A and 41 DNA-B sequences demonstrated the presence of three CMG species circulating in the Comoros and Seychelles archipelagos (East African cassava mosaic virus, EACMV; East African cassava mosaic Kenya virus, EACMKV; and East African cassava mosaic Cameroon virus, EACMCV). Phylogeographic analyses suggest that CMG's presence on these SWIO islands is probably the result of at least four independent introduction events from mainland Africa occurring between 1988 and 2009. Amongst the islands of the Comoros archipelago, two major migration pathways were inferred: One from Grande Comore to Mohéli and the second from Mayotte to Anjouan. While only two recombination events characteristic of SWIO islands isolates were identified, numerous re-assortments events were detected between EACMV and EACMKV, which seem to almost freely interchange their genome components.

Conclusions: Rapid and extensive virus spread within the SWIO islands was demonstrated for three CMG complex species. Strong evolutionary or ecological interaction between CMG species may explain both their propensity to exchange components and the absence of recombination with non-CMG begomoviruses. Our results suggest an important role of anthropic factors in CMGs spread as the principal axes of viral migration correspond with major routes of human movement and commercial trade. Finer-scale temporal analyses of CMGs to precisely scale the relative contributions of human and insect transmission to their movement dynamics will require further extensive sampling in the SWIO region.

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Figures

Figure 1
Figure 1
Repartition map of the seven African CMG’s in East Africa, the Comoros archipelago and the Seychelles archipelago. The map on the left describes the general repartition of the seven DNA-A species in the area. The map at the bottom right zooms in on the archipelagos with the number and composition of samples from each island represented with pie charts. The colour code is available on the top right of the figure with FS indicating full genome sequences and PS indicating partial genome sequences.
Figure 2
Figure 2
Maximum clade credibility trees constructed from the EACMV-like capsid protein (CP) dataset. Branches are coloured according to the most probable location state of the node on their right (i.e. the likely geographical location of the ancestral sequence represented by this node). The large black circle around one of the nodes indicates that the state probability at this node is less than 0.5 (i.e. there is less than 50% confidence in the indicated location being the actual place where this ancestral sequence existed). The time-scale of evolutionary changes represented in the tree is indicated by the scale bar below it. Whereas filled circles associated with nodes indicate > 95% posterior probability support for the branches to their left, open circles indicate nodes with > 70% posterior support for these branches. Nodes to the right of branches with < 70% support are left unlabelled. The bar graph on the left corner indicates location probabilities of the node at the root of the tree (which is the node representing the last common ancestor of all the sequences represented in the tree). Grey bars represent the probabilities obtained with randomisation of the tip locations. Probable introduction events from Africa to the SWIO islands are indicated with red arrows.
Figure 3
Figure 3
Maximum clade credibility trees constructed from the EACMV-like DNA-B Full genome (FG-B) dataset. Branches are coloured according to the most probable location state of their descendant nodes, with black circled nodes indicating nodes with state probabilities < 0.5. The time-scale of evolutionary changes represented in the tree is indicated by the scale bar below it. Whereas filled circles associated with nodes indicate > 95% posterior probability support for the branches to their left, open circles indicate nodes with > 70% posterior support for these branches. Nodes to the right of branches with < 70% support are left unlabelled. The bar graph on the left corner indicates the location probabilities of the node at the root of the tree that represents the most recent common ancestor of all the sequences represented in the tree. Grey bars represent the probabilities obtained with randomisation of the tip locations. Probable introduction events from Africa to the SWIO islands are indicated with red arrows.
Figure 4
Figure 4
CMG migrations from East Africa and between SWIO islands. CMG migration events inferred using the capsid protein (CP, in green); full genome DNA-A (FG-A, in red) and full genome DNA-B (FG-B, in blue) datasets. Arrow colours represent the dataset used to infer each migration event. The thickness of arrows is proportional to the number of independent movements inferred between islands.
Figure 5
Figure 5
Analysis of EACMV-like component re-assortments. Analysis of component re-assortment through counts of DNA-B component “migrations” between the DNA-A sequences of the major CMG lineages. In the analysis DNA-A sequences were classified into six discrete groups. Branches are coloured according to which of these six groups the DNA-B sequence represented by the node to their right was associated with. Black circled nodes indicate ancestral DNA-B sequences where there is less than a < 0.5 state probability for all six of DNA-A lineages (i.e. it is particularly uncertain which DNA-A these ancestral DNA-B sequences were associated with). Whereas filled circles associated with nodes to the right of branches indicate > 95% posterior probability support for these branches, open circles indicate branches with > 70% posterior support. Nodes to the right of branches with < 70% support are left unlabelled. DNA-B “migrations” between different DNA-A lineages that could be explained by genome re-assortment events inferred in an independent RDP3 analysis are indicated by the corresponding RDP3 event number listed in Table 2. The underlined event number (event 6) corresponds to a partial DNA-B”migration” that likely involved overprinting of part of the DNA-B CR with that of the DNA-A sequence that captured it.
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