Natural polymorphism of the plasmid double-stranded RNA of the Saccharomyces yeasts

Наумов, Г. И.; Ivannikova, Yu. V.; Chernov, I. Yu.; Наумова, Е. С.

doi:10.1134/s0026261709020118

“…Secondly, virus infection of pathogenic fungi can also cause hypovirulence (a reduction in fungal pathogenesis), an outcome that is being exploited to treat agricultural disease [74][75][76][77]. Thirdly, many wild and domesticated strains of S. cerevisiae are free of totiviruses (and therefore also of killer), suggesting that there is selection against the ongoing maintenance of these viruses [20,28,71]. Fourthly, the continued maintenance of RNAi systems in fungi also correlates with the loss of the killer phenotype and is known to antagonize fungal viruses [71,78].…”

Section: Discussionmentioning

confidence: 99%

“…Further, all yeast viruses are unable to escape their host cell, and instead are transmitted through mating or during mitotic cell division. Almost all described species of Saccharomyces yeasts play host to doublestranded RNA (dsRNA) viruses of the family Totiviridae [20,21]. In fact, most commonly used S. cerevisiae laboratory strains are infected with a totivirus named L-A ( Fig 1A) [22].…”

Section: Introductionmentioning

confidence: 99%

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

Rowley

¹

,

Ho

²

,

Bushong

³

et al. 2016

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In eukaryotes, the degradation of cellular mRNAs is accomplished by Xrn1 and the cytoplasmic exosome. Because viral RNAs often lack canonical caps or poly-A tails, they can also be vulnerable to degradation by these host exonucleases. Yeast lack sophisticated mechanisms of innate and adaptive immunity, but do use RNA degradation as an antiviral defense mechanism. We find a highly refined, species-specific relationship between Xrn1p and the “L-A” totiviruses of different Saccharomyces yeast species. We show that the gene XRN1 has evolved rapidly under positive natural selection in Saccharomyces yeast, resulting in high levels of Xrn1p protein sequence divergence from one yeast species to the next. We also show that these sequence differences translate to differential interactions with the L-A virus, where Xrn1p from S. cerevisiae is most efficient at controlling the L-A virus that chronically infects S. cerevisiae, and Xrn1p from S. kudriavzevii is most efficient at controlling the L-A-like virus that we have discovered within S. kudriavzevii. All Xrn1p orthologs are equivalent in their interaction with another virus-like parasite, the Ty1 retrotransposon. Thus, Xrn1p appears to co-evolve with totiviruses to maintain its potent antiviral activity and limit viral propagation in Saccharomyces yeasts. We demonstrate that Xrn1p physically interacts with the Gag protein encoded by the L-A virus, suggesting a host-virus interaction that is more complicated than just Xrn1p-mediated nucleolytic digestion of viral RNAs.

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“…Secondly, virus infection of pathogenic fungi can also cause hypovirulence (a reduction in fungal pathogenesis), an outcome that is being exploited to treat agricultural disease [74][75][76][77]. Thirdly, many wild and domesticated strains of S. cerevisiae are free of totiviruses (and therefore also of killer), suggesting that there is selection against the ongoing maintenance of these viruses [20,28,71]. Fourthly, the continued maintenance of RNAi systems in fungi also correlates with the loss of the killer phenotype and is known to antagonize fungal viruses [71,78].…”

Section: Discussionmentioning

confidence: 99%

XRN1is a Species-Specific Virus Restriction Factor in Yeasts

Rowley

¹

,

Ho

²

,

Bushong

³

et al. 2016

Preprint

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In eukaryotes, the degradation of cellular mRNAs is accomplished by Xrn1 and the cytoplasmic exosome. Because viral RNAs often lack canonical caps or poly-A tails, they can also be vulnerable to degradation by these host exonucleases. Yeast lack sophisticated mechanisms of innate and adaptive immunity, but do use RNA degradation as an antiviral defense mechanism. We find a highly refined, species-specific relationship between Xrn1p and the "L-A" totiviruses of different Saccharomyces yeast species. We show that the gene XRN1 has evolved rapidly under positive natural selection in Saccharomyces yeast, resulting in high levels of Xrn1p protein sequence divergence from one yeast species to the next. We also show that these sequence differences translate to differential interactions with the L-A virus, where Xrn1p from S. cerevisiae is most efficient at controlling the L-A virus that chronically infects S. cerevisiae, and Xrn1p from S. kudriavzevii is most efficient at controlling the L-A-like virus that we have discovered within S. kudriavzevii. All Xrn1p orthologs are equivalent in their interaction with another virus-like parasite, the Ty1 retrotransposon. Thus, Xrn1p appears to co-evolve with totiviruses to maintain its potent antiviral activity and limit viral propagation in Saccharomyces yeasts. We demonstrate that Xrn1p physically interacts with the Gag protein encoded by the L-A virus, suggesting a host-virus interaction that is more complicated than just Xrn1p-mediated nucleolytic digestion of viral RNAs. Author SummaryLike other eukaryotes, Saccharomyces cerevisiae is chronically infected with viruses. It is fascinating to consider how S. cerevisiae deals with viral infection, because yeast have limited mechanisms of immunity. Our paper focuses on Xrn1p, an enzyme that is important for the destruction of irregular cellular RNAs in all eukaryotic cells. Xrn1p also degrades viral RNAs, owing to the fact that viral RNAs share biochemical characteristics with aberrant cellular mRNAs. Xrn1p was previously known to efficiently control the replication of a S. cerevisiae virus called "L-A. " We find that two different L-A viruses of Saccharomyces yeasts are best controlled by the Xrn1p from their own host species compared to the PLOS Pathogens |

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“…These include binding host transcription factors (Morillon et al , ), responding to extracellular mating pheromones (Bilanchone et al , ), interaction with Ty retrotransposon‐encoded antisense RNAs (Matsuda and Garfinkel, ) and dominant negative proteins (Nishida et al , ; Saha et al , ). Overall, regardless of the benign or beneficial influence of yeast nucleic acid elements on the physiology of their host, their prevalence and copy number are variable both within and between Saccharomyces species, which suggests that the gain and loss of viruses, retrotransposons and plasmids is ongoing in extant yeast populations (Xiao and Rank, ; López et al , ; Moore et al , ; Liti et al , ; Naumov et al , ; Chang et al , ; Strope et al , ). However, what determines these dynamic interactions is not yet completely understood.…”

Section: The Benefits Of Nucleic Acid Elements(?)mentioning

confidence: 99%

“…Their long-term persistence has probably enabled yeast nucleic acid elements to coevolve with their host over long periods of evolutionary time. Indeed, most extant Saccharomyces species harbor related nucleic acid elements (Liti et al, 2005;Naumov et al, 2009;Strope et al, 2015). This persistence may have allowed adaptation to their specific host cellular environment with little detriment to their host cell (Falcon et al, 2005;Futcher and Cox, 1983;McBride et al, 2013;Vega et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

The frenemies within: viruses, retrotransposons and plasmids that naturally infectSaccharomycesyeasts

Rowley

¹

2017

Yeast

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Viruses are a major focus of current research efforts because of their detrimental impact on humanity and their ubiquity within the environment. Bacteriophages have long been used to study host-virus interactions within microbes, but it is often forgotten that the single-celled eukaryote Saccharomyces cerevisiae and related species are infected with double-stranded RNA viruses, single-stranded RNA viruses, LTR-retrotransposons and double-stranded DNA plasmids. These intracellular nucleic acid elements have some similarities to higher eukaryotic viruses, i.e. yeast retrotransposons have an analogous lifecycle to retroviruses, the particle structure of yeast totiviruses resembles the capsid of reoviruses and segregation of yeast plasmids is analogous to segregation strategies used by viral episomes. The powerful experimental tools available to study the genetics, cell biology and evolution of S. cerevisiae are well suited to further our understanding of how cellular processes are hijacked by eukaryotic viruses, retrotransposons and plasmids. This article has been written to briefly introduce viruses, retrotransposons and plasmids that infect Saccharomyces yeasts, emphasize some important cellular proteins and machineries with which they interact, and suggest the evolutionary consequences of these interactions. Copyright © 2017 John Wiley & Sons, Ltd.

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Natural polymorphism of the plasmid double-stranded RNA of the Saccharomyces yeasts

Cited by 7 publications

References 10 publications

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

XRN1is a Species-Specific Virus Restriction Factor in Yeasts

The frenemies within: viruses, retrotransposons and plasmids that naturally infectSaccharomycesyeasts

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