Ty3 Retrotransposon Hijacks Mating Yeast RNA Processing Bodies to Infect New Genomes

Bilanchone, Virginia; Clemens, Kristina; Kaake, Robyn M.; Dawson, Anthony R.; Matheos, Dina P.; Nagashima, Kunio; Sitlani, Parth; Patterson, Kurt; Chang, Irene; Huang, Lan; Sandmeyer, Suzanne

doi:10.1371/journal.pgen.1005528

Cited by 23 publications

(25 citation statements)

References 113 publications

(168 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Finally, the Ty1 retrotransposon is another intracellular virus that replicates within Saccharomyces species and often co-exists with L-A within the same cell. Interestingly, Xrn1p is not a restriction factor for Ty retrotransposons, but rather promotes their replication [43,47,48,[53][54][55][56][57]. We found no significant difference between the mean values for retrotransposition in the presence of Xrn1p from S. cerevisiae, S. mikatae, S. kudriavzevii, or S. bayanus (one-way ANOVA, F 3 , 8 = 0.36, p = 0.78), indicating that the evolutionary differences between divergent XRN1 genes do not affect the ability of Ty1 to replicate within S. cerevisiae ( Fig 4D).…”

Section: Xrn1p Cellular Function Has Been Conserved In Saccharomyces mentioning

confidence: 99%

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

Rowley

Bushong

et al. 2016

PLoS Pathog

View full text Add to dashboard Cite

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.

show abstract

Section: Xrn1p Cellular Function Has Been Conserved In Saccharomyces mentioning

confidence: 99%

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

Rowley

Bushong

et al. 2016

PLoS Pathog

View full text Add to dashboard Cite

show abstract

“…Ty3 transcription is strongly induced by exposure to mating pheromone [153,154]. Ty3 VLPs form and mature in cells arrested in G1 with α-factor, but cDNA is not detected and retrotransposition does not occur until cells are released/recover from arrest [155,156]. Inhibition of retrotransposition depends on cell cycle arrest itself, rather than other aspects of the mating response [156].…”

Section: Saccharomyces Cerevisiaeexample Host Factors Regulating Ty1mentioning

confidence: 99%

“…Ty3 retrotransposition frequently occurs in haploid cells of opposite mating types allowed to mate and form diploid cells [152]. Ty3 proteins and RNA form cytoplasmic foci in α-factor-treated cells and mating cells that likely represent sites of VLP assembly [155,157].…”

Section: Saccharomyces Cerevisiaeexample Host Factors Regulating Ty1mentioning

confidence: 99%

Diverse transposable element landscapes in pathogenic and nonpathogenic yeast models: the value of a comparative perspective

Maxwell

2020

Mobile DNA

View full text Add to dashboard Cite

Genomics and other large-scale analyses have drawn increasing attention to the potential impacts of transposable elements (TEs) on their host genomes. However, it remains challenging to transition from identifying potential roles to clearly demonstrating the level of impact TEs have on genome evolution and possible functions that they contribute to their host organisms. I summarize TE content and distribution in four well-characterized yeast model systems in this review: the pathogens Candida albicans and Cryptococcus neoformans, and the nonpathogenic species Saccharomyces cerevisiae and Schizosaccharomyces pombe. I compare and contrast their TE landscapes to their lifecycles, genomic features, as well as the presence and nature of RNA interference pathways in each species to highlight the valuable diversity represented by these models for functional studies of TEs. I then review the regulation and impacts of the Ty1 and Ty3 retrotransposons from Saccharomyces cerevisiae and Tf1 and Tf2 retrotransposons from Schizosaccharomyces pombe to emphasize parallels and distinctions between these wellstudied elements. I propose that further characterization of TEs in the pathogenic yeasts would enable this set of four yeast species to become an excellent set of models for comparative functional studies to address outstanding questions about TE-host relationships.

show abstract

“…These results suggest that Ty1 mRNA and Ty1i transcription responds differently to SPT3 , and raise the possibility that there is differential recognition of the Ty1 and Ty1i promoters by SAGA. Ty1i RNA levels also increase while Ty1 mRNA slightly decreases in cells lacking XRN1 , which encodes a 5′-3′ ribonuclease involved in RNA decay associated with P-bodies (Parker 2012), RNA transcription (Berretta, et al 2008, Haimovich, et al 2013), and assembly of functional Ty1 (Checkley, et al 2010, Dutko, et al 2010) and Ty3 (Beliakova-Bethell, et al 2006, Bilanchone, et al 2015) VLPs. Analyses of CNC − mutations within ( Δ238–353 , Δ238–281 ) or adjacent ( T399C ) to the 5′ LTR suggest that Ty1i and Ty1 mRNA utilize similar enhancer sequences for transcription (Curcio, et al 2015, Saha, et al 2015).…”

Section: Synthesis Of P22/p18mentioning

confidence: 99%

A self-encoded capsid derivative restricts Ty1 retrotransposition in Saccharomyces

Garfinkel¹,

Tucker²,

Saha³

et al. 2015

Curr Genet

View full text Add to dashboard Cite

Retrotransposons and retroviral insertions have molded the genomes of many eukaryotes. Since retroelements transpose via an RNA intermediate, the additive nature of the replication cycle can result in massive increases in copy number if left unchecked. Host organisms have countered with several defense systems, including domestication of retroelement genes that now act as restriction factors to minimize propagation. We discovered a novel truncated form of the Saccharomyces Ty1 retrotransposon capsid protein, dubbed p22 that inhibits virus-like particle (VLP) assembly and function. The p22 restriction factor expands the repertoire of defense proteins targeting the capsid and highlights a novel host-parasite strategy. Instead of inhibiting all transposition by domesticating the restriction gene as a distinct locus, Ty1 and budding yeast may have coevolved a relationship that allows high levels of transposition when Ty1 copy numbers are low and progressively less transposition as copy numbers rise. Here, we offer a perspective on p22 restriction, including its mode of expression, effect on VLP functions, interactions with its target, properties as a nucleic acid chaperone, similarities to other restriction factors, and future directions.

show abstract

Ty3 Retrotransposon Hijacks Mating Yeast RNA Processing Bodies to Infect New Genomes

Cited by 23 publications

References 113 publications

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts

Diverse transposable element landscapes in pathogenic and nonpathogenic yeast models: the value of a comparative perspective

A self-encoded capsid derivative restricts Ty1 retrotransposition in Saccharomyces

Contact Info

Product

Resources

About