A guanosine to adenosine transition in the 3′ terminal extracistronic region of bacteriophage Qβ RNA leading to loss of infectivity

Sabo, Donna L.; Domingo, Esteban; Bandle, E.; Weissmann, Charles

doi:10.1016/s0022-2836(77)80141-1

Cited by 36 publications

(12 citation statements)

References 25 publications

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“…Another, not mutually exclusive but mechanistic proposal, is that genome segmentation may ensue from the selection of shorter RNA molecules whose replication is completed in a shorter time than replication of the corresponding full length genome [3], [6]. Evidence supporting selection for deleted RNA was obtained in experiments involving in vitro replication of Qβ RNA, without the requirement to express viral proteins or to produce infectious particles [11], [12]. In the case of FMDV there is no evidence of an advantage of the segmented over ST genome at the stage of RNA genome replication, protein expression or production of infectious virus, in agreement with previous descriptions for positive strand defective viruses [13], [14].…”

Section: Discussionmentioning

confidence: 99%

Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

et al. 2011

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The evolutionary benefit of viral genome segmentation is a classical, yet unsolved question in evolutionary biology and RNA genetics. Theoretical studies anticipated that replication of shorter RNA segments could provide a replicative advantage over standard size genomes. However, this question has remained elusive to experimentalists because of the lack of a proper viral model system. Here we present a study with a stable segmented bipartite RNA virus and its ancestor non-segmented counterpart, in an identical genomic nucleotide sequence context. Results of RNA replication, protein expression, competition experiments, and inactivation of infectious particles point to a non-replicative trait, the particle stability, as the main driver of fitness gain of segmented genomes. Accordingly, measurements of the volume occupation of the genome inside viral capsids indicate that packaging shorter genomes involves a relaxation of the packaging density that is energetically favourable. The empirical observations are used to design a computational model that predicts the existence of a critical multiplicity of infection for domination of segmented over standard types. Our experiments suggest that viral segmented genomes may have arisen as a molecular solution for the trade-off between genome length and particle stability. Genome segmentation allows maximizing the genetic content without the detrimental effect in stability derived from incresing genome length.

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Section: Discussionmentioning

confidence: 99%

Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

et al. 2011

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“…Another proposal is that segmentation could result from selection of shorter RNA molecules that replicate faster than the corresponding parental genome, favored at high MOIs to ensure efficient complementation (25,40). Deleted forms of viral RNAs have indeed been shown to have a selective replicative advantage over parental full-length genomes in vitro (24,34). A difference of replication capacity or of tolerance to mutations is now amenable to direct experimental testing with the segmented-unsegmented FMDV genome system, and such experiments are currently in progress.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Transition toward Defective RNAs That Are Infectious by Complementation

García-Arriaza

Manrubia

Toja

et al. 2004

J Virol

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152

201

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Passage of foot-and-mouth disease virus (FMDV) in cell culture resulted in the generation of defective RNAs that were infectious by complementation. Deletions (of nucleotides 417, 999, and 1017) mapped in the L proteinase and capsid protein-coding regions. Cell killing followed two-hit kinetics, defective genomes were encapsidated into separate viral particles, and individual viral plaques contained defective genomes with no detectable standard FMDV RNA. Infection in the absence of standard FMDV RNA was achieved by cotransfection of susceptible cells with transcripts produced in vitro from plasmids encoding the defective genomes. These results document the first step of an evolutionary transition toward genome segmentation of an unsegmented RNA virus and provide an experimental system to compare rates of RNA progeny production and resistance to enhanced mutagenesis of a segmented genome versus its unsegmented counterpart.Mutation, recombination, and ensuing phenotypic modifications in response to selective pressures can be readily observed and quantitated with RNA viruses both in cell culture and in vivo within modest time periods. This has rendered viruses suitable experimental systems for studies of basic Darwinian processes of genetic modification, competition, and selection or random drift as agents of genome diversification and biological adaptation (reviewed in references 1, 8, and 12). However, some major evolutionary transitions such as RNA genome segmentation have never been observed in the laboratory, yet they have probably occurred, given the hundreds of animal, plant, bacterial, and fungal viruses with segmented RNA genomes that have been described, including picornavirus-like plant RNA viruses (43). We have carried out extensive studies on the population dynamics of the important animal picornavirus foot-and-mouth disease virus (FMDV), including that of phenotypic evolution upon long-term serial cytopathic infections of BHK-21 cells (2). Unexpectedly, after more than 200 serial infections of viral population C-S8c1 of FMDV (a clone of serotype C [reviewed in reference 33]), defective genomes became dominant in the population. Defective interfering (DI) particles are frequently produced upon passage of RNA viruses at a high multiplicity of infection (MOI). DI particles are deletion mutants that require the presence of helper virus for replication and can interfere with the replication of the standard infectious virus (14-16, 29, 32, 35). The results described here show that defective genomes which individually could not cause cytopathology could nevertheless complement each other to produce progeny and kill cells in the absence of standard virus. The results provide, to our knowledge, the first description of defective RNA genomes occurring during viral replication that can be stably maintained by complementation upon passage at a high MOI in the absence of standard infectious virus. Therefore, the results provide experimental evidence of the initial step of an evolutionary transition towards genome ...

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“…Thus, at 37°C, the ts defect of PCV110 may interfere with genome amplification early in the infectious cycle of the virus and would eventually lead to lower levels of viral-specific proteins and RNAs in infected cells. It has been previously shown that nucleotide changes in the 3' extracistronic region of bacteriophage Q, RNA produces changes in in vitro RNA replication (36) as well as in in vivo replication (37,38). A conditional mutation in the 3' noncoding region of poliovirus RNA has also been reported (39).…”

Section: Discussionmentioning

confidence: 99%

A chimeric plasmid from cDNA clones of poliovirus and coxsackievirus produces a recombinant virus that is temperature-sensitive.

Semler¹,

Johnson²,

Tracy³

1986

Proc. Natl. Acad. Sci. U.S.A.

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We have inserted a 405-nucleotide fragment from the 5' noncoding region of the coxsackievirus B3 genome into an infectious cDNA copy of the poliovirus RNA genome. Transfection of plasmid DNA containing this hybrid genome construct into cultured monkey cells produced infectious virus. Recombinant virus stocks displayed a temperature-sensitive phenotype for growth at 37C. We found that there is a dramatic reduction in the level of viral proteins and viral RNAs in HeLa cesll infected with the recombinant at 37C compared to that obtained at 33.50C. Thus, insertion of a portion of the coxsackievirus genome into the poliovirus genome produces a temperature-sensitive recombinant virus. That 'this substitution occurs in a region of the poliovirus genome that, to date, has not been shown to have any coding function suggests that RNA sequences involved in replicase recognition or ribosome binding may contribute to the temperature-senpitive phenotype of the recombinant virus.

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A guanosine to adenosine transition in the 3′ terminal extracistronic region of bacteriophage Qβ RNA leading to loss of infectivity

Cited by 36 publications

References 25 publications

Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

Evolutionary Transition toward Defective RNAs That Are Infectious by Complementation

A chimeric plasmid from cDNA clones of poliovirus and coxsackievirus produces a recombinant virus that is temperature-sensitive.

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