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Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses.

ABSTRACT: Whitefly-transmitted geminiviruses are major pathogens of the important crop cassava in Africa. The intensive sampling and sequencing of cassava mosaic disease-causing viruses that occurred in the wake of a severe outbreak in Central Africa (1997-2002) allowed us to estimate the rate of evolution of this virus. East African cassava mosaic virus and related species are obligately bipartite (DNA-A and DNA-B segments), and these two genome segments have different evolutionary histories. Despite these phylogenetic differences, we inferred high rates of nucleotide substitution in both segments: mean rates of 1.60x10(-3) and 1.33x10(-4) substitutions site(-1) year(-1) for DNA-A and DNA-B, respectively. While similarly high substitution rates were found in datasets free of detectable recombination, only that estimated for the coat protein gene (AV1), for which an additional DNA-A sequence isolated in 1995 was available, was statistically robust. These high substitution rates also confirm that those previously estimated for the monopartite tomato yellow leaf curl virus (TYLCV) are representative of multiple begomoviruses. We also validated our rate estimates by comparing them with those depicting the emergence of TYLCV in North America. These results further support the notion that geminiviruses evolve as rapidly as many RNA viruses.

SUBMITTER: Duffy S

PROVIDER: S-EPMC4091138 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses.

Duffy Siobain S Holmes Edward C EC

The Journal of general virology 20090304 Pt 6

Whitefly-transmitted geminiviruses are major pathogens of the important crop cassava in Africa. The intensive sampling and sequencing of cassava mosaic disease-causing viruses that occurred in the wake of a severe outbreak in Central Africa (1997-2002) allowed us to estimate the rate of evolution of this virus. East African cassava mosaic virus and related species are obligately bipartite (DNA-A and DNA-B segments), and these two genome segments have different evolutionary histories. Despite the ...[more]

PMID: 19264617

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Project description:BackgroundCassava mosaic disease (CMD) in Madagascar is caused by a complex of at least six African cassava mosaic geminivirus (CMG) species. This provides a rare opportunity for a comparative study of the evolutionary and epidemiological dynamics of distinct pathogenic crop-infecting viral species that coexist within the same environment. The genetic and spatial structure of CMG populations in Madagascar was studied and Bayesian phylogeographic modelling was applied to infer the origins of Madagascan CMG populations within the epidemiological context of related populations situated on mainland Africa and other south western Indian Ocean (SWIO) islands.ResultsThe isolation and analysis of 279 DNA-A and 117 DNA-B sequences revealed the presence in Madagascar of four prevalent CMG species (South African cassava mosaic virus, SACMV; African cassava mosaic virus, ACMV; East African cassava mosaic Kenya virus, EACMKV; and East African cassava mosaic Cameroon virus, EACMCV), and of numerous CMG recombinants that have, to date, only ever been detected on this island. SACMV and ACMV, the two most prevalent viruses, displayed low degrees of genetic diversity and have most likely been introduced to the island only once. By contrast, EACMV-like CMG populations (consisting of East African cassava mosaic virus, EAMCKV, EACMCV and complex recombinants of these) were more diverse, more spatially structured, and displayed evidence of at least three independent introductions from mainland Africa. Although there were no statistically supported virus movement events between Madagascar and the other SWIO islands, at least one mainland African ACMV variant likely originated in Madagascar.ConclusionsOur study highlights both the complexity of CMD in Madagascar, and the distinct evolutionary and spatial dynamics of the different viral species that collectively are associated with this disease. Given that more distinct CMG species and recombinants have been found in Madagascar than any other similarly sized region of the world, the risks of recombinant CMG variants emerging on this island are likely to be higher than elsewhere. Evidence of an epidemiological link between Madagascan and mainland African CMGs suggests that the consequences of such emergence events could reach far beyond the shores of this island.

Project description:Cassava is infected by numerous geminiviruses in Africa and India that cause devastating losses to poor farmers. We here describe the molecular diversity of seven representative cassava mosaic geminiviruses (CMGs) infecting cassava from multiple locations in Tanzania. We report for the first time the presence of two isolates in East Africa: (EACMCV-[TZ1] and EACMCV-[TZ7]) of the species East African cassava mosaic Cameroon virus, originally described in West Africa. The complete nucleotide sequence of EACMCV-[TZ1] DNA-A and DNA-B components shared a high overall sequence identity to EACMCV-[CM] components (92% and 84%). The EACMCV-[TZ1] and -[TZ7] genomic components have recombinations in the same genome regions reported in EACMCV-[CM], but they also have additional recombinations in both components. Evidence from sequence analysis suggests that the two strains have the same ancient origin and are not recent introductions. EACMCV-[TZ1] occurred widely in the southern part of the country. Four other CMG isolates were identified: two were close to the EACMV-Kenya strain (named EACMV-[KE/TZT] and EACMV-[KE/TZM] with 96% sequence identity); one isolate, TZ10, had 98% homology to EACMV-UG2Svr and was named EACMV-UG2 [TZ10]; and finally one isolate was 95% identical to EACMV-[TZ] and named EACMV-[TZ/YV]. One isolate of African cassava mosaic virus with 97% sequence identity with other isolates of ACMV was named ACMV-[TZ]. It represents the first ACMV isolate from Tanzania to be sequenced. The molecular variability of CMGs was also evaluated using partial B component nucleotide sequences of 13 EACMV isolates from Tanzania. Using the sequences of all CMGs currently available, we have shown the presence of a number of putative recombination fragments that are more prominent in all components of EACMV than in ACMV. This new knowledge about the molecular CMG diversity in East Africa, and in Tanzania in particular, has led us to hypothesize about the probable importance of this part of Africa as a source of diversity and evolutionary change both during the early stages of the relationship between CMGs and cassava and in more recent times. The existence of multiple CMG isolates with high DNA genome diversity in Tanzania and the molecular forces behind this diversity pose a threat to cassava production throughout the African continent.

Project description: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.

Project description:Growing cassava in Africa requires resistance against the viruses causing cassava mosaic disease (CMD) and the viruses causing cassava brown streak disease (CBSD). A dominant CMD2 resistance gene from a West African cassava landrace provides strong resistance against the cassava mosaic viruses. However, resistance against cassava brown streak viruses is limited to cassava varieties that show tolerance to the disease. A recently identified cassava germplasm that cannot be infected with cassava brown streak viruses provides a new source of the resistance required to protect cassava from CBSD. We present a synopsis of the status of virus resistance in cassava and report on the research to combine resistance against CBSD and CMD. We improve the lengthy and erratic screening for CBSD resistance by proposing a virus infection and screening protocol for the viruses causing CBSD and CMD, which allows a rapid and precise assessment of cassava resistance under controlled conditions. Using this approach, we classified the virus responses of cassava lines from Africa and South America and identified truly virus-resistant clones that cannot be infected with any of the known viruses causing CBSD even under the most stringent virus infections. A modification of this protocol was used to test seedlings from cassava crosses for resistance against both diseases. A broad-spectrum resistance was identified in a workflow that lasted 9 months from seed germination to the identification of virus resistance. The workflow we propose dramatically reduces the evaluation and selection time required in a classical breeding workflow to reach the advanced field trial stage in only 9 months by conducting selections for virus resistance and plant multiplication in parallel. However, it does not bypass field evaluations; cassava resistance assessment prior to the field limits the evaluation to candidates with virus resistance defined as the absence of symptoms and the absence of the virus. The transfer of our virus screening workflow to cassava breeding programs enhances the efficiency by which resistance against viruses can be selected. It provides a precise definition of the plant's resistance response and can be used as a model system to tackle resistance in cassava against other diseases.

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Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses.

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Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses.

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