Conservation of mRNA quality control factor Ski7 and its diversification through changes in alternative splicing and gene duplication

Marshall, Alexandra; Han, Jaeil; Kim, Min‐Seon; Hoof, Ambro van

doi:10.1073/pnas.1801997115

Cited by 14 publications

(26 citation statements)

References 41 publications

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“…Data 1). This is consistent with published data from other eukaryotes (Kowalinski et al, 2016;Kalisiak et al, 2016;Marshall et al, 2018). The zebrafish ski7specific exon (exon 5) contains the previously annotated Ski7-like motif and the most conserved region of Ski7, the so-called patch 4-like (P4) motif (Kowalinski et al, 2016;Brunkard & Baker, 2018) (Fig.…”

Section: Ski7 Mrna Is Highly Expressed During the Oocyte-to-embryo Trsupporting

confidence: 91%

“…In contrast to yeast, in which Ski7 is encoded by an independent gene locus (Marshall et al, 2013;, the recently identified Ski7 homolog in vertebrates (human HBS1LV3) is encoded by an alternative splice isoform of vertebrate hbs1l (Kowalinski et al, 2016;Marshall et al, 2018;Kalisiak et al, 2016). Vertebrate Ski7 shares the Ski and exosome complex interacting domains of yeast Ski7, yet it lacks the GTPase domain (Marshall et al, 2018;Brunkard & Baker, 2018;Kowalinski et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition

Quio

Schleiffer

Mechtler

et al. 2020

Preprint

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Post-transcriptional mechanisms are crucial for the regulation of gene expression.These mechanisms are particularly important during rapid developmental transitions such as the oocyte-to-embryo transition, which is characterized by dramatic changes to the developmental program in the absence of nuclear transcription. Under these conditions, changes to the RNA content are solely dependent on RNA degradation.Although several mechanisms that promote RNA decay during embryogenesis have been identified, it remains unclear which cellular machineries contribute to remodeling the maternal transcriptome during the oocyte-to-embryo transition. Here, we focused on the auxiliary 3'-to-5' degradation factor Ski7 in zebrafish as its mRNA peaks during this time frame. Homozygous ski7 mutant fish were viable and developed into morphologically normal adults, yet they had decreased fertility. Consistent with the idea that Ski7 participates in remodeling the transcriptome during the oocyte-toembryo transition, transcriptome profiling identified stage-specific mRNA targets of Ski7. Genes upregulated in ski7 mutants were generally lowly expressed in wild type, suggesting that Ski7 maintains low transcript levels for this subset of genes. GO enrichment analyses of genes mis-regulated in ski7 mutants implicated Ski7 in the regulation of redox processes. This was confirmed experimentally by an increased resistance of ski7 mutant embryos to reductive stress. Overall, our results provide first insights into the physiological role of vertebrate Ski7 as an important posttranscriptional regulator during the oocyte-to-embryo transition.

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Section: Ski7 Mrna Is Highly Expressed During the Oocyte-to-embryo Trsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition

Quio

Schleiffer

Mechtler

et al. 2020

Preprint

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“…Association of the Ski complex with the exosome core complex requires an additional protein, SKI7 36 . Recent data revealed the functional conservation of SKI7 across eukaryotes 37 . In mammals and plants, SKI7 is produced by alternative splicing from a single locus that encodes also the HBS1 protein 37–39 .…”

Section: Introductionmentioning

confidence: 99%

“…Recent data revealed the functional conservation of SKI7 across eukaryotes 37 . In mammals and plants, SKI7 is produced by alternative splicing from a single locus that encodes also the HBS1 protein 37–39 . HBS1 functions together with the G-protein Dom34/PELOTA in No-Stop decay by releasing ribosomes stalled on RNAs lacking a stop codon 40–43 .…”

Section: Introductionmentioning

confidence: 99%

RST1 and RIPR connect the cytosolic RNA exosome to the Ski complex in Arabidopsis

et al. 2019

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The RNA exosome is a key 3’−5’ exoribonuclease with an evolutionarily conserved structure and function. Its cytosolic functions require the co-factors SKI7 and the Ski complex. Here we demonstrate by co-purification experiments that the ARM-repeat protein RESURRECTION1 (RST1) and RST1 INTERACTING PROTEIN (RIPR) connect the cytosolic Arabidopsis RNA exosome to the Ski complex. rst1 and ripr mutants accumulate RNA quality control siRNAs (rqc-siRNAs) produced by the post-transcriptional gene silencing (PTGS) machinery when mRNA degradation is compromised. The small RNA populations observed in rst1 and ripr mutants are also detected in mutants lacking the RRP45B/CER7 core exosome subunit. Thus, molecular and genetic evidence supports a physical and functional link between RST1, RIPR and the RNA exosome. Our data reveal the existence of additional cytosolic exosome co-factors besides the known Ski subunits. RST1 is not restricted to plants, as homologues with a similar domain architecture but unknown function exist in animals, including humans.

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“…Hbs1 instead delivers Dom34 to stalled ribosomes, which allows Dom34 to recycle the ribosomal subunits for subsequent rounds of translation (Becker et al, 2011;Pisareva et al, 2011;Shoemaker et al, 2010). We further showed that this alternative splicing of SKI7/HBS1 is conserved in animals, fungi, and plants (Marshall et al, 2018;Marshall et al, 2013).…”

Section: Introductionmentioning

confidence: 57%

Origin, Conservation, and Loss of Alternative Splicing Events that Diversify the Proteome in Saccharomycotina Budding Yeasts

Hurtig

Kim

Orlando-Coronel

et al. 2020

Preprint

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Many eukaryotes use alternative splicing to express multiple proteins from the same gene. However, while the majority of mammalian genes are alternatively spliced, other eukaryotes use this process less frequently. The budding yeast Saccharomyces cerevisiae has been successfully used to study the mechanism of splicing and the splicing machinery, but alternative splicing in yeast is relatively rare and has not been extensively studied. We have recently shown that the alternative splicing of SKI7/HBS1 is widely conserved, but that yeast and a few other eukaryotes have replaced this one alternatively spliced gene with a pair of duplicated unspliced genes as part of a whole genome doubling (WGD). Here we show that other examples of alternative splicing that were previously found to have functional consequences are widely conserved within the Saccharomycotina. We also show that the most common mechanism by which alternative splicing has disappeared is by the replacement of an alternatively spliced gene with duplicate genes. Saccharomycetaceae that diverged before WGD use alternative splicing more frequently than S. cerevisiae. This suggests that the WGD is a major reason for the low frequency of alternative splicing in yeast. We anticipate that whole genome doublings in other lineages may have had the same effect.

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Conservation of mRNA quality control factor Ski7 and its diversification through changes in alternative splicing and gene duplication

Cited by 14 publications

References 41 publications

Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition

Zebrafish Ski7 tunes RNA levels during the oocyte-to-embryo transition

RST1 and RIPR connect the cytosolic RNA exosome to the Ski complex in Arabidopsis

Origin, Conservation, and Loss of Alternative Splicing Events that Diversify the Proteome in Saccharomycotina Budding Yeasts

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