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Backmasking in the yeast genome: encoding overlapping information for protein-coding and RNA degradation.

ABSTRACT: Backmasking is a recording technique used to hide a sound or message in a music track in reverse, meaning that it is only audible when the record is played backwards. Analogously, the compact yeast genome encodes for diverse sources of information such as overlapping coding and non-coding transcripts, and protein-binding sites on the two complementary DNA strands. Examples are the consensus binding site sequences of the RNA-binding proteins Nrd1 and Nab3 that target non-coding transcripts for degradation. Here, by examining the overlap of stable (SUTs, stable unannotated transcripts) and unstable (CUTs, cryptic unstable transcripts) transcripts with protein-coding genes, we show that the predicted Nrd1 and Nab3-binding site sequences occur at differing frequencies. They are always depleted in the sense direction of protein-coding genes, thus avoiding degradation of the transcript. However in the antisense direction, predicted binding sites occur at high frequencies in genes with overlapping unstable ncRNAs (CUTs), so limiting the availability of non-functional transcripts. In contrast they are depleted in genes with overlapping stable ncRNAs (SUTs), presumably to avoid degrading the non-coding transcript. The protein-coding genes maintain similar amino-acid contents, but they display distinct codon usages so that Nrd1 and Nab3-binding sites can arise at differing frequencies in antisense depending on the overlapping transcript type. Our study demonstrates how yeast has evolved to encode multiple layers of information-protein-coding genes in one strand and the relative chance of degrading antisense RNA in the other strand-in the same regions of a compact genome.

SUBMITTER: Cakiroglu SA

PROVIDER: S-EPMC5041482 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Backmasking in the yeast genome: encoding overlapping information for protein-coding and RNA degradation.

Cakiroglu S Aylin SA Zaugg Judith B JB Luscombe Nicholas M NM

Nucleic acids research 20160804 17

Backmasking is a recording technique used to hide a sound or message in a music track in reverse, meaning that it is only audible when the record is played backwards. Analogously, the compact yeast genome encodes for diverse sources of information such as overlapping coding and non-coding transcripts, and protein-binding sites on the two complementary DNA strands. Examples are the consensus binding site sequences of the RNA-binding proteins Nrd1 and Nab3 that target non-coding transcripts for de ...[more]

PMID: 27492286

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Project description:BackgroundIn eukaryotic cells, each molecule of H/ACA small nucleolar RNA (snoRNA) assembles with four evolutionarily conserved core proteins to compose a specific ribonucleoprotein particle. One of the four core components has pseudouridine synthase activity and catalyzes the conversion of a selected uridine to pseudouridine. Members of the pseudouridine synthase family are highly conserved. In addition to catalyzing pseudouridylation of target RNAs, they carry out a variety of essential functions related to ribosome biogenesis and, in mammals, to telomere maintenance. To investigate further the molecular mechanisms underlying the expression of pseudouridine synthase genes, we analyzed the transcriptional activity of the Drosophila member of this family in great detail.ResultsThe Drosophila gene for pseudouridine synthase, minifly/Nop60b (mfl), encodes two novel mRNAs ending at a downstream poly(A) site. One species is characterized only by an extended 3'-untranslated region (3'UTR), while a minor mRNA encodes a variant protein that represents the first example of an alternative subform described for any member of the family to date. The rare spliced variant is detected mainly in females and is predicted to have distinct functional properties. We also report that a cluster comprising four isoforms of a C/D box snoRNA and two highly related copies of a small ncRNA gene of unknown function is intron-encoded at the gene-variable 3'UTRs. Because this arrangement, the alternative 3' ends allow mfl not only to produce two distinct protein subforms, but also to release different ncRNAs. Intriguingly, accumulation of all these intron-encoded RNAs was found to be sex-biased and quantitatively modulated throughout development and, within the ovaries, the ncRNAs of unknown function were found not ubiquitously expressed.ConclusionOur results expand the repertoire of coding/non-coding transcripts derived from the gene encoding Drosophila pseudouridine synthase. This gene exhibits a complex and interlaced organization, and its genetic information may be expressed as different protein subforms and/or ncRNAs that may potentially contribute to its biological functions.

Dataset Information

Backmasking in the yeast genome: encoding overlapping information for protein-coding and RNA degradation.

Publications

Backmasking in the yeast genome: encoding overlapping information for protein-coding and RNA degradation.

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