A Viable Hypomorphic Allele of the Essential IMP3 Gene Reveals Novel Protein Functions in Saccharomyces cerevisiae

Cosnier, Bruno; Kwapisz, Marta; Hatin, Isabelle; Namy, Olivier; Denmat, Sylvie Hermann‐Le; Morillon, Antonin; Rousset, Jean‐Pierre; Fabret, Céline

doi:10.1371/journal.pone.0019500

Cited by 5 publications

(6 citation statements)

References 45 publications

(64 reference statements)

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“…Consequences of readthrough include prevention of deadenylation increasing mRNA stability, ribosome stalling inducing mRNA degradation, or production of a protein with a C-terminal peptide extension. Two functional C-terminal extensions were previously identified in S. cerevisiae: Extension of the PDE2 gene decreases its stability, resulting in accumulation of cyclic AMP (Namy et al 2002); and readthrough of IMP3, involved in ribosomal biogenesis, destabilizes its interaction with the U3 snoRNA (Cosnier et al 2011). A recent systematic study of conserved protein-coding potential in candidate C-terminal extensions in eukaryotes failed to identify any candidates in yeasts (Jungreis et al 2011); however, the investigators required strong sequence conservation of the extension across five sensu stricto species.…”

Section: Identification Of Conserved C-terminal Peptide Extensionsmentioning

confidence: 99%

“…Combining direct translational evidence from the Ribo fraction with sequence conservation between the parental species, we identified 19 candidates for conserved C-terminal extensions (Table 2). However, in the majority of cases in which translation was detected in putative extensions, the peptide sequence was poorly conserved (62 cases) and/or speciesspecific (109 cases) (Supplemental Table S4), including the experimentally verified extension of IMP3 (Cosnier et al 2011).…”

Section: Conservation and Divergence Of C-terminal Peptide Extensionsmentioning

confidence: 99%

“…Both verified extensions in yeast exert their effects by destabilizing protein function and/or interactions (Namy et al 2002;Cosnier et al 2011). This may result from the addition of any unstructured component to the C ter-minus, which can lead to destabilization and degradation of the folded polypeptide (von der Haar and Tuite 2007).…”

Section: Conservation and Divergence Of C-terminal Peptide Extensionsmentioning

confidence: 99%

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Evolution at two levels of gene expression in yeast

2013

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Despite the greater functional importance of protein levels, our knowledge of gene expression evolution is based almost entirely on studies of mRNA levels. In contrast, our understanding of how translational regulation evolves has lagged far behind. Here we have applied ribosome profiling-which measures both global mRNA levels and their translation rates-to two species of Saccharomyces yeast and their interspecific hybrid in order to assess the relative contributions of changes in mRNA abundance and translation to regulatory evolution. We report that both cis-and trans-acting regulatory divergence in translation are abundant, affecting at least 35% of genes. The majority of translational divergence acts to buffer changes in mRNA abundance, suggesting a widespread role for stabilizing selection acting across regulatory levels. Nevertheless, we observe evidence of lineage-specific selection acting on several yeast functional modules, including instances of reinforcing selection acting at both levels of regulation. Finally, we also uncover multiple instances of stop-codon readthrough that are conserved between species. Our analysis reveals the underappreciated complexity of post-transcriptional regulatory divergence and indicates that partitioning the search for the locus of selection into the binary categories of

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Section: Identification Of Conserved C-terminal Peptide Extensionsmentioning

confidence: 99%

Section: Conservation and Divergence Of C-terminal Peptide Extensionsmentioning

confidence: 99%

Section: Conservation and Divergence Of C-terminal Peptide Extensionsmentioning

confidence: 99%

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Evolution at two levels of gene expression in yeast

2013

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“…Later, TR has also been described in bacteria 6 7 and eukaryotes 8 9 10 11 12 13 14 15 16 17 18 19 . Some TR-extended protein forms were shown to function differently from their non-extended counterparts, like PDE2 14 and IMP3 9 13 in yeast, the hdc (headcase) gene of D. melanogaster 16 17 or myelin protein zero (MPZ) 19 and vascular endothelial growth factor A (VEGFA) 20 in human. Functional difference may entail differential localization, into the peroxisomes 10 21 22 , or their production in a tissue-specific manner 15 .…”

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confidence: 96%

Computational analysis of translational readthrough proteins in Drosophila and yeast reveals parallels to alternative splicing

Pancsa

Macossay-Castillo

Kosol

et al. 2016

Sci Rep

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In translational readthrough (TR) the ribosome continues extending the nascent protein beyond the first in-frame termination codon. Due to the lack of dedicated analyses of eukaryotic TR cases, the associated functional-evolutionary advantages are still unclear. Here, based on a variety of computational methods, we describe the structural and functional properties of previously proposed D. melanogaster and S. cerevisiae TR proteins and extensions. We found that in D. melanogaster TR affects long proteins in mainly regulatory roles. Their TR-extensions are structurally disordered and rich in binding motifs, which, together with their cell-type- and developmental stage-dependent inclusion, suggest that similarly to alternatively spliced exons they rewire cellular interaction networks in a temporally and spatially controlled manner. In contrast, yeast TR proteins are rather short and fulfil mainly housekeeping functions, like translation. Yeast extensions usually lack disorder and linear motifs, which precludes elucidating their functional relevance with sufficient confidence. Therefore we propose that by being much more restricted and by lacking clear functional hallmarks in yeast as opposed to fruit fly, TR shows remarkable parallels with alternative splicing. Additionally, the lack of conservation of TR extensions among orthologous TR proteins suggests that TR-mediated functions may be generally specific to lower taxonomic levels.

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“…Telomere length was analyzed as described in [ 103 ]. Total DNA was isolated from cells grown overnight in YPD (OD 600 = 2.0).…”

Section: Methodsmentioning

confidence: 99%

Expression of Subtelomeric lncRNAs Links Telomeres Dynamics to RNA Decay in S. cerevisiae

Kwapisz

Ruault

Dijk

et al. 2015

ncRNA

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Long non-coding RNAs (lncRNAs) have been shown to regulate gene expression, chromatin domains and chromosome stability in eukaryotic cells. Recent observations have reported the existence of telomeric repeats containing long ncRNAs – TERRA in mammalian and yeast cells. However, their functions remain poorly characterized. Here, we report the existence in S. cerevisiae of several lncRNAs within Y′ subtelomeric regions. We have called them subTERRA. These belong to Cryptic Unstable Transcripts (CUTs) and Xrn1p-sensitive Unstable Transcripts (XUTs) family. subTERRA transcription, carried out mainly by RNAPII, is initiated within the subtelomeric Y’ element and occurs in both directions, towards telomeres as well as centromeres. We show that subTERRA are distinct from TERRA and are mainly degraded by the general cytoplasmic and nuclear 5′- and 3′- RNA decay pathways in a transcription-dependent manner. subTERRA accumulates preferentially during the G1/S transition and in C-terminal rap1 mutant but independently of Rap1p function in silencing. The accumulation of subTERRA in RNA decay mutants coincides with telomere misregulation: shortening of telomeres, loss of telomeric clustering in mitotic cells and changes in silencing of subtelomeric regions. Our data suggest that subtelomeric RNAs expression links telomere maintenance to RNA degradation pathways.

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A Viable Hypomorphic Allele of the Essential IMP3 Gene Reveals Novel Protein Functions in Saccharomyces cerevisiae

Cited by 5 publications

References 45 publications

Evolution at two levels of gene expression in yeast

Evolution at two levels of gene expression in yeast

Computational analysis of translational readthrough proteins in Drosophila and yeast reveals parallels to alternative splicing

Expression of Subtelomeric lncRNAs Links Telomeres Dynamics to RNA Decay in S. cerevisiae

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