Turnover of ribosome-associated transcripts from de novo ORFs produces gene-like characteristics available for de novo gene emergence in wild yeast populations

  1. Christian R. Landry1,2
  1. 1Institut de Biologie Intégrative et des Systèmes, Département de Biologie, PROTEO, Centre de Recherche en Données Massives de l'Université Laval, Pavillon Charles-Eugène-Marchand, Université Laval, G1V 0A6 Québec, Québec, Canada;
  2. 2Département de Biochimie, Microbiologie et Bio-informatique, Université Laval, G1V 0A6 Québec, Québec, Canada;
  3. 3Institut de Biologie Intégrative de la Cellule (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, 91190 Gif sur Yvette, France
  • 4 Present address: Université de Lille CNRS, UMR 8198-Evo-Eco-Paleo, F-59655 Lille, France

  • Corresponding author: eleonore.durand{at}univ-lille.fr
  • Abstract

    Little is known about the rate of emergence of de novo genes, what their initial properties are, and how they spread in populations. We examined wild yeast populations (Saccharomyces paradoxus) to characterize the diversity and turnover of intergenic ORFs over short evolutionary timescales. We find that hundreds of intergenic ORFs show translation signatures similar to canonical genes, and we experimentally confirmed the translation of many of these ORFs in laboratory conditions using a reporter assay. Compared with canonical genes, intergenic ORFs have lower translation efficiency, which could imply a lack of optimization for translation or a mechanism to reduce their production cost. Translated intergenic ORFs also tend to have sequence properties that are generally close to those of random intergenic sequences. However, some of the very recent translated intergenic ORFs, which appeared <110 kya, already show gene-like characteristics, suggesting that the raw material for functional innovations could appear over short evolutionary timescales.

    Footnotes

    • [Supplemental material is available for this article.]

    • Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.239822.118.

    • Freely available online through the Genome Research Open Access option.

    • Received May 25, 2018.
    • Accepted May 13, 2019.

    This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

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