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A phloem-limited fijivirus induces the formation of neoplastic phloem tissues that house virus multiplication in the host plant.

ABSTRACT: A number of phloem-limited viruses induce the development of tumours (enations) in the veins of host plants, but the relevance of tumour induction to the life cycle of those viruses is unclear. In this study, we performed molecular and structural analyses of tumours induced by rice black-streaked dwarf virus (RBSDV, genus Fijivirus) infection in maize plants. The transcript level of the maize cdc2 gene, which regulates the cell cycle, was highly elevated in tumour tissues. Two-dimensional electrophoresis identified 25 cellular proteins with altered accumulation in the tumour tissues. These proteins are involved in various metabolic pathways, including photosynthesis, redox, energy pathways and amino acid synthesis. Histological analysis indicated that the tumours predominantly originated from hyperplastic growth of phloem, but those neoplastic tissues have irregular structures and cell arrangements. Immunodetection assays and electron microscopy observations indicated that in the shoots, RBSDV is confined to phloem and tumour regions and that virus multiplication actively occurs in the tumour tissue, as indicated by the high accumulation of non-structural proteins and formation of viroplasms in the tumour cells. Thus, the induction of tumours by RBSDV infection provides a larger environment that is favourable for virus propagation in the host plant.

SUBMITTER: Shen J

PROVIDER: S-EPMC4949464 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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A phloem-limited fijivirus induces the formation of neoplastic phloem tissues that house virus multiplication in the host plant.

Shen Jiangfeng J Chen Xian X Chen Jianping J Sun Liying L

Scientific reports 20160719

A number of phloem-limited viruses induce the development of tumours (enations) in the veins of host plants, but the relevance of tumour induction to the life cycle of those viruses is unclear. In this study, we performed molecular and structural analyses of tumours induced by rice black-streaked dwarf virus (RBSDV, genus Fijivirus) infection in maize plants. The transcript level of the maize cdc2 gene, which regulates the cell cycle, was highly elevated in tumour tissues. Two-dimensional electr ...[more]

PMID: 27432466

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Project description:BackgroundVirulence does not represent any obvious advantage to parasites. Most models of virulence evolution assume that virulence is an unavoidable consequence of within-host multiplication of parasites, resulting in trade-offs between within-host multiplication and between-host transmission fitness components. Experimental support for the central assumption of this hypothesis, i.e., for a positive correlation between within-host multiplication rates and virulence, is limited for plant-parasite systems.Methodology/principal findingsWe have addressed this issue in the system Arabidopsis thaliana-Cucumber mosaic virus (CMV). Virus multiplication and the effect of infection on plant growth and on viable seed production were quantified for 21 Arabidopsis wild genotypes infected by 3 CMV isolates. The effect of infection on plant growth and seed production depended of plant architecture and length of postembryonic life cycle, two genetically-determined traits, as well as on the time of infection in the plant's life cycle. A relationship between virus multiplication and virulence was not a general feature of this host-parasite system. This could be explained by tolerance mechanisms determined by the host genotype and operating differently on two components of plant fitness, biomass production and resource allocation to seeds. However, a positive relationship between virus multiplication and virulence was detected for some accessions with short life cycle and high seed weight to biomass ratio, which show lower levels of tolerance to infection.Conclusions/significanceThese results show that genotype-specific tolerance mechanisms may lead to the absence of a clear relationship between parasite multiplication and virulence. Furthermore, a positive correlation between parasite multiplication and virulence may occur only in some genotypes and/or environmental conditions for a given host-parasite system. Thus, our results challenge the general validity of the trade-off hypothesis for virulence evolution, and stress the need of considering the effect of both the host and parasite genotypes in analyses of host-parasite interactions.

Project description:Although vertical transmission from parents to offspring through seeds is an important fitness component of many plant viruses, very little is known about the factors affecting this process. Viruses reach the seed by direct invasion of the embryo and/or by infection of the ovules or the pollen. Thus, it can be expected that the efficiency of seed transmission would be determined by (i) virus within-host multiplication and movement, (ii) the ability of the virus to invade gametic tissues, (iii) plant seed production upon infection, and (iv) seed survival in the presence of the virus. However, these predictions have seldom been experimentally tested. To address this question, we challenged 18 Arabidopsis thaliana accessions with Turnip mosaic virus and Cucumber mosaic virus Using these plant-virus interactions, we analyzed the relationship between the effect of virus infection on rosette and inflorescence weights; short-, medium-, and long-term seed survival; virulence; the number of seeds produced per plant; virus within-host speed of movement; virus accumulation in the rosette and inflorescence; and efficiency of seed transmission measured as a percentage and as the total number of infected seeds. Our results indicate that the best estimators of percent seed transmission are the within-host speed of movement and multiplication in the inflorescence. Together with these two infection traits, virulence and the number of seeds produced per infected plant were also associated with the number of infected seeds. Our results provide support for theoretical predictions and contribute to an understanding of the determinants of a process central to plant-virus interactions.IMPORTANCE One of the major factors contributing to plant virus long-distance dispersal is the global trade of seeds. This is because more than 25% of plant viruses can infect seeds, which are the main mode of germplasm exchange/storage, and start new epidemics in areas where they were not previously present. Despite the relevance of this process for virus epidemiology and disease emergence, the infection traits associated with the efficiency of virus seed transmission are largely unknown. Using turnip mosaic and cucumber mosaic viruses and their natural host Arabidopsis thaliana as model systems, we have identified the within-host speed of virus colonization and multiplication in the reproductive structures as the main determinants of the efficiency of seed transmission. These results contribute to shedding light on the mechanisms by which plant viruses disperse and optimize their fitness and may help in the design of more-efficient strategies to prevent seed infection.

Dataset Information

A phloem-limited fijivirus induces the formation of neoplastic phloem tissues that house virus multiplication in the host plant.

Publications

A phloem-limited fijivirus induces the formation of neoplastic phloem tissues that house virus multiplication in the host plant.

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