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Genetic diversity and silencing suppression effects of Rice yellow mottle virus and the P1 protein.

ABSTRACT: BACKGROUND: PTGS (post-transcriptional gene silencing) is used to counter pathogenic invasions, particularly viruses. In return, many plant viruses produce proteins which suppress silencing directed against their RNA. The diversity of silencing suppression at the species level in natural hosts is unknown. RESULTS: We investigated the functional diversity of silencing suppression among isolates of the African RYMV (Rice yellow mottle virus) in rice. The RYMV-P1 protein is responsible for cell-to-cell movement and is a silencing suppressor. Transgenic gus-silencing rice lines were used to investigate intra-specific and serogroup silencing suppression diversity at two different levels: that of the virion and the P1 silencing suppressor protein. Our data provide evidence that silencing suppression is a universal phenomenon for RYMV species. However, we found considerable diversity in their ability to suppress silencing which was not linked to RYMV phylogeny, or pathogenicity. At the level of the silencing suppressor P1 alone, we found similar results to those previously found at the virion level. In addition, we showed that cell-to-cell movement of P1 was crucial for the efficiency of silencing suppression. Mutagenesis of P1 demonstrated a strong link between some amino acids and silencing suppression features with, one on the hand, the conserved amino acids C95 and C64 involved in cell-to-cell movement and the strength of suppression, respectively, and on the other hand, the non conserved F88 was involved in the strength of silencing suppression. CONCLUSION: We demonstrated that intra-species diversity of silencing suppression is highly variable and by mutagenesis of P1 we established the first link between silencing suppression and genetic diversity. These results are potentially important for understanding virus-host interactions.

SUBMITTER: Sire C

PROVIDER: S-EPMC2390521 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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Genetic diversity and silencing suppression effects of Rice yellow mottle virus and the P1 protein.

Siré Christelle C Bangratz-Reyser Martine M Fargette Denis D Brugidou Christophe C

Virology journal 20080430

<h4>Background</h4>PTGS (post-transcriptional gene silencing) is used to counter pathogenic invasions, particularly viruses. In return, many plant viruses produce proteins which suppress silencing directed against their RNA. The diversity of silencing suppression at the species level in natural hosts is unknown.<h4>Results</h4>We investigated the functional diversity of silencing suppression among isolates of the African RYMV (Rice yellow mottle virus) in rice. The RYMV-P1 protein is responsible ...[more]

PMID: 18447922

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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:To investigate the spread of Rice yellow mottle virus (RYMV) along the Niger River, regular sampling of virus isolates was conducted along 500 km of the Niger Valley in the Republic of Niger and was complemented by additional sampling in neighbouring countries in West Africa and Central Africa. The spread of RYMV into and within the Republic of Niger was inferred as a continuous process using a Bayesian statistical framework applied previously to reconstruct its dispersal history in West Africa, East Africa, and Madagascar. The spatial resolution along this section of the Niger River was the highest implemented for RYMV and possibly for any plant virus. We benefited from the results of early field surveys of the disease for the validation of the phylogeographic reconstruction and from the well-documented history of rice cultivation changes along the Niger River for their interpretation. As a prerequisite, the temporal signal of the RYMV data sets was revisited in the light of recent methodological advances. The role of the hydrographic network of the Niger Basin in RYMV spread was examined, and the link between virus population dynamics and the extent of irrigated rice was assessed. RYMV was introduced along the Niger River in the Republic of Niger in the early 1980s from areas to the southwest of the country where rice was increasingly grown. Viral spread was triggered by a major irrigation scheme made of a set of rice perimeters along the river valley. The subsequent spatial and temporal host continuity and the inoculum build-up allowed for a rapid spread of RYMV along the Niger River, upstream and downstream, over hundreds of kilometres, and led to the development of severe epidemics. There was no evidence of long-distance dissemination of the virus through natural water. Floating rice in the main meanders of the Middle Niger did not contribute to virus dispersal from West Africa to Central Africa. RYMV along the Niger River is an insightful example of how agricultural intensification favours pathogen emergence and spread.

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

Genetic diversity and silencing suppression effects of Rice yellow mottle virus and the P1 protein.

Publications

Genetic diversity and silencing suppression effects of Rice yellow mottle virus and the P1 protein.

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