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Diversification of rice yellow mottle virus and related viruses spans the history of agriculture from the neolithic to the present.

ABSTRACT: The mechanisms of evolution of plant viruses are being unraveled, yet the timescale of their evolution remains an enigma. To address this critical issue, the divergence time of plant viruses at the intra- and inter-specific levels was assessed. The time of the most recent common ancestor (TMRCA) of Rice yellow mottle virus (RYMV; genus Sobemovirus) was calculated by a Bayesian coalescent analysis of the coat protein sequences of 253 isolates collected between 1966 and 2006 from all over Africa. It is inferred that RYMV diversified approximately 200 years ago in Africa, i.e., centuries after rice was domesticated or introduced, and decades before epidemics were reported. The divergence time of sobemoviruses and viruses of related genera was subsequently assessed using the age of RYMV under a relaxed molecular clock for calibration. The divergence time between sobemoviruses and related viruses was estimated to be approximately 9,000 years, that between sobemoviruses and poleroviruses approximately 5,000 years, and that among sobemoviruses approximately 3,000 years. The TMRCA of closely related pairs of sobemoviruses, poleroviruses, and luteoviruses was approximately 500 years, which is a measure of the time associated with plant virus speciation. It is concluded that the diversification of RYMV and related viruses has spanned the history of agriculture, from the Neolithic age to the present.

SUBMITTER: Fargette D

PROVIDER: S-EPMC2495034 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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Diversification of rice yellow mottle virus and related viruses spans the history of agriculture from the neolithic to the present.

Fargette Denis D Pinel-Galzi Agnès A Sérémé Drissa D Lacombe Séverine S Hébrard Eugénie E Traoré Oumar O Konaté Gnissa G

PLoS pathogens 20080815 8

The mechanisms of evolution of plant viruses are being unraveled, yet the timescale of their evolution remains an enigma. To address this critical issue, the divergence time of plant viruses at the intra- and inter-specific levels was assessed. The time of the most recent common ancestor (TMRCA) of Rice yellow mottle virus (RYMV; genus Sobemovirus) was calculated by a Bayesian coalescent analysis of the coat protein sequences of 253 isolates collected between 1966 and 2006 from all over Africa. ...[more]

PMID: 18704169

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Project description:BACKGROUND:The effects of viral infection involve concomitant plant gene variations and cellular changes. A simple system is required to assess the complexity of host responses to viral infection. The genome of the Rice yellow mottle virus (RYMV) is a single-stranded RNA with a simple organisation. It is the most well-known monocotyledon virus model. Several studies on its biology, structure and phylogeography have provided a suitable background for further genetic studies. 12 rice chromosome sequences are now available and provide strong support for genomic studies, particularly physical mapping and gene identification. RESULTS:The present data, obtained through the cDNA-AFLP technique, demonstrate differential responses to RYMV of two different rice cultivars, i.e. susceptible IR64 (Oryza sativa indica), and partially resistant Azucena (O. s. japonica). This RNA profiling provides a new original dataset that will enable us to gain greater insight into the RYMV/rice interaction and the specificity of the host response. Using the SIM4 subroutine, we took the intron/exon structure of the gene into account and mapped 281 RYMV stress responsive (RSR) transcripts on 12 rice chromosomes corresponding to 234 RSR genes. We also mapped previously identified deregulated proteins and genes involved in partial resistance and thus constructed the first global physical map of the RYMV/rice interaction. RSR transcripts on rice chromosomes 4 and 10 were found to be not randomly distributed. Seven genes were identified in the susceptible and partially resistant cultivars, and transcripts were colocalized for these seven genes in both cultivars. During virus infection, many concomitant plant gene expression changes may be associated with host changes caused by the infection process, general stress or defence responses. We noted that some genes (e.g. ABC transporters) were regulated throughout the kinetics of infection and differentiated susceptible and partially resistant hosts. CONCLUSION:We enhanced the first RYMV/rice interaction map by combining information from the present study and previous studies on proteins and ESTs regulated during RYMV infection, thus providing a more comprehensive view on genes related to plant responses. This combined map provides a new tool for exploring molecular mechanisms underlying the RYMV/rice interaction.

Project description:Rice yellow mottle virus (RYMV) is one of the major diseases of rice in Africa. The high resistance of the Oryza glaberrima Tog7291 accession involves a null allele of the RYMV2 gene, whose ortholog in Arabidopsis, CPR5, is a transmembrane nucleoporin involved in effector-triggered immunity. To optimize field deployment of the RYMV2 gene and improve its durability, which is often a weak point in varietal resistance, we analyzed its efficiency toward RYMV isolates representing the genetic diversity of the virus and the molecular basis of resistance breakdown. Tog7291 resistance efficiency was highly variable depending on the isolate used, with infection rates ranging from 0 to 98% of plants. Back-inoculation experiments indicated that infection cases were not due to an incomplete resistance phenotype but to the emergence of resistance-breaking (RB) variants. Interestingly, the capacity of the virus to overcome Tog7291 resistance is associated with a polymorphism at amino-acid 49 of the VPg protein which also affects capacity to overcome the previously studied RYMV1 resistance gene. This polymorphism appeared to be a main determinant of the emergence of RB variants. It acts independently of the resistance gene and rather reflects inter-species adaptation with potential consequences for the durability of resistance. RB mutations were identified by full-length or partial sequencing of the RYMV genome in infected Tog7291 plants and were validated by directed mutagenesis of an infectious viral clone. We found that Tog7291 resistance breakdown involved mutations in the putative membrane anchor domain of the polyprotein P2a. Although the precise effect of these mutations on rice/RYMV interaction is still unknown, our results offer a new perspective for the understanding of RYMV2 mediated resistance mechanisms. Interestingly, in the susceptible IR64 variety, RB variants showed low infectivity and frequent reversion to the wild-type genotype, suggesting that Tog7291 resistance breakdown is associated with a major loss of viral fitness in normally susceptible O. sativa varieties. Despite the high frequency of resistance breakdown in controlled conditions, this loss of fitness is an encouraging element with regards to RYMV2 resistance durability.

Dataset Information

Diversification of rice yellow mottle virus and related viruses spans the history of agriculture from the neolithic to the present.

Publications

Diversification of rice yellow mottle virus and related viruses spans the history of agriculture from the neolithic to the present.

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