Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast

Atkinson, Sophie; Marguerat, Samuel; Bitton, Danny A.; Rodríguez-López, Maria; Rallis, Charalampos; Lemay, Jean-François; Cotobal, Cristina; Małecki, Michał; Smialowski, Pawel; Mata, Juan; Korber, Philipp; Bachand, François; Bähler, Jürg

doi:10.1261/rna.065524.118

Cited by 54 publications

(95 citation statements)

References 133 publications

(242 reference statements)

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“…As previously reported in S. cerevisiae and S. pombe (Wery et al 2016;Atkinson et al 2018;Wery et al 2018b), many lncRNAs are targeted by both Rrp6 and Xrn1 in N. castellii ( Figure 1B).…”

Section: Aslncrnas Are Primarily Degraded By Rrp6 and Xrn1 In N Castsupporting

confidence: 84%

“…Only 10 DUTs accumulate in dcr1 cells, and they are also (even more) sensitive to Xrn1 ( Figure S1D). This is marginal in comparison to the 1392 DUTs annotated in fission yeast (Atkinson et al 2018), raising the question of the function of Dcr1 in N. castellii. DCR1 has been conserved in some budding yeast species (Drinnenberg et al 2009).…”

Section: Discussionmentioning

confidence: 95%

“…Both Rrp6 and Xrn1 are conserved across Eukaryotes (Houseley et al 2006;Nagarajan et al 2013). In this respect, CUTs and XUTs were recently identified in fission yeast (Atkinson et al 2018;Watts et al 2018;Wery et al 2018b), and they are also mainly antisense to protein-coding genes in this species. This indicates that the roles of the nuclear exosome and Xrn1 in restricting aslncRNAs levels have been conserved across the yeast clade.…”

Section: Introductionmentioning

confidence: 99%

“…This is probably explained by different subcellular localization, as Dicer is restricted to the nucleus in fission yeast, mainly contributing in heterochromatin formation at centromeric repeats (Woolcock and Buhler 2013). Yet, Dicer was shown to control a novel class of lncRNAs, referred to as Dicer-sensitive Unstable Transcripts (DUTs), which are also mainly antisense to protein-coding genes (Atkinson et al 2018). Thus, in fission yeast, Dicer contributes to the control of aslncRNAs levels.…”

Section: Introductionmentioning

confidence: 99%

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Endogenous RNAi pathway evolutionarily shapes the destiny of the antisense lncRNAs transcriptome

Szachnowski

Andus

Foretek

et al. 2019

Preprint

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Antisense (as)lncRNAs are extensively degraded by the nuclear exosome and the cytoplasmic exoribonuclease Xrn1 in the budding yeast Saccharomyces cerevisiae, lacking RNA interference (RNAi). Whether the ribonuclease III Dicer affects aslncRNAs in close RNAi-capable relatives remains unknown. Using genome-wide RNA profiling, here we show that aslncRNAs are primarily targeted by the exosome and Xrn1 in the RNAi-capable budding yeast Naumovozyma castellii, Dicer only affecting Xrn1-sensitive lncRNAs (XUTs) levels in Xrn1-deficient cells. The dcr1 and xrn1 mutants display synergic growth defects, indicating that Dicer becomes critical in the absence of Xrn1. Small RNA sequencing showed that Dicer processes aslncRNAs into small RNAs, with a preference for asXUTs. Consistently, Dicer localizes into the cytoplasm. Finally, we observed an expansion of the exosome-sensitive antisense transcriptome in N. castellii compared to S. cerevisiae, suggesting that the presence of cytoplasmic RNAi has reinforced the nuclear RNA surveillance machinery to temper aslncRNAs expression. Our data provide fundamental insights into aslncRNAs metabolism and open perspectives into the possible evolutionary contribution of RNAi in shaping the aslncRNAs transcriptome.

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“…As previously reported in S. cerevisiae and S. pombe (Wery et al 2016;Atkinson et al 2018;Wery et al 2018b), many lncRNAs are targeted by both Rrp6 and Xrn1 in N. castellii ( Figure 1B).…”

Section: Aslncrnas Are Primarily Degraded By Rrp6 and Xrn1 In N Castsupporting

confidence: 84%

Section: Discussionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Endogenous RNAi pathway evolutionarily shapes the destiny of the antisense lncRNAs transcriptome

Szachnowski

Andus

Foretek

et al. 2019

Preprint

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“…represents sense transcripts, as antisense transcripts of the H3.c1 gene was~1% of sense transcripts 16 .…”

Section: Resultsmentioning

confidence: 99%

Time-lapse single-cell transcriptomics reveals modulation of histone H3 for dormancy breaking in fission yeast

et al. 2020

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How quiescent cells break dormancy is a key issue in eukaryotic cells including cancer. Fungal spores, for example, remain quiescent for long periods until nourished, although the mechanisms by which dormancy is broken remain enigmatic. Transcriptome analysis could provide a clue, but methods to synchronously germinate large numbers of spores are lacking, and thus it remains a challenge to analyse gene expression upon germination. Hence, we develop methods to assemble transcriptomes from individual, asynchronous spore cells of fission yeast undergoing germination to assess transcriptomic changes over time. The virtual time-lapse analyses highlights one of three copies of histone H3 genes whose transcription fluctuates during the initial stage of germination. Disruption of this temporal fluctuation causes defects in spore germination despite no visible defects in other stages of the life cycle. We conclude that modulation of histone H3 expression is a crucial 'wake-up' trigger at dormancy breaking.

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Shaping the chromatin landscape at rRNA and tRNA genes, an emerging new role for RNA polymerase II transcription?

Yague‐Sanz

2023

Yeast

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Eukaryotic genes must be condensed into chromatin while remaining accessible to the transcriptional machinery to support gene expression. Among the three eukaryotic RNA polymerases (RNAP), RNAPII is unique, partly because of the C‐terminal domain (CTD) of its largest subunit, Rpb1. Rpb1 CTD can be extensively modified during the transcription cycle, allowing for the co‐transcriptional recruitment of specific interacting proteins. These include chromatin remodeling factors that control the opening or closing of chromatin. How the CTD‐less RNAPI and RNAPIII deal with chromatin at rRNA and tRNA genes is less understood. Here, we review recent advances in our understanding of how the chromatin at tRNA genes and rRNA genes can be remodeled in response to environmental cues in yeast, with a particular focus on the role of local RNAPII transcription in recruiting chromatin remodelers at these loci. In fission yeast, RNAPII transcription at tRNA genes is important to re‐establish a chromatin environment permissive to tRNA transcription, which supports growth from stationary phase. In contrast, local RNAPII transcription at rRNA genes correlates with the closing of the chromatin in starvation in budding and fission yeast, suggesting a role in establishing silent chromatin. These opposite roles might support a general model where RNAPII transcription recruits chromatin remodelers to tRNA and rRNA genes to promote the closing and reopening of chromatin in response to the environment.

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Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast

Cited by 54 publications

References 133 publications

Endogenous RNAi pathway evolutionarily shapes the destiny of the antisense lncRNAs transcriptome

Endogenous RNAi pathway evolutionarily shapes the destiny of the antisense lncRNAs transcriptome

Time-lapse single-cell transcriptomics reveals modulation of histone H3 for dormancy breaking in fission yeast

Shaping the chromatin landscape at rRNA and tRNA genes, an emerging new role for RNA polymerase II transcription?

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