A long-term demasculinization of X-linked intergenic noncoding RNAs in Drosophila melanogaster

  1. Liping Wei1,10
  1. 1State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences and Center for Bioinformatics, Peking University, Beijing 100871, China;
  2. 2Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA;
  3. 3Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil 05508;
  4. 4Center of Developmental Biology and Genetics, College of Life Sciences, Peking University, Beijing 100871, China;
  5. 5Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China;
  6. 6Genome Facility, University of Chicago, Chicago, Illinois 60637, USA;
  7. 7Committee on Genetics, Genomics, and Systems Biology, University of Chicago, Chicago, Illinois 60637, USA
    1. 8 These authors contributed equally to this work.

    • 9 Present address: Department of Pathology and Laboratory Medicine, University of California at Los Angeles, Los Angeles, CA 90095, USA

    Abstract

    Recent studies have revealed key roles of noncoding RNAs in sex-related pathways, but little is known about the evolutionary forces acting on these noncoding RNAs. Profiling the transcriptome of Drosophila melanogaster with whole-genome tiling arrays found that 15% of male-biased transcribed fragments are intergenic noncoding RNAs (incRNAs), suggesting a potentially important role for incRNAs in sex-related biological processes. Statistical analysis revealed a paucity of male-biased incRNAs and coding genes on the X chromosome, suggesting that similar evolutionary forces could be affecting the genomic organization of both coding and noncoding genes. Expression profiling across germline and somatic tissues further suggested that both male meiotic sex chromosome inactivation (MSCI) and sexual antagonism could contribute to the chromosomal distribution of male-biased incRNAs. Comparative sequence analysis showed that the evolutionary age of male-biased incRNAs is a significant predictor of their chromosomal locations. In addition to identifying abundant sex-biased incRNAs in the fly genome, our work unveils a global picture of the complex interplay between noncoding RNAs and sexual chromosome evolution.

    Footnotes

    • 10 Corresponding authors

      E-mail weilp{at}mail.cbi.pku.edu.cn

      E-mail mlong{at}uchicago.edu

    • [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.165837.113.

      Freely available online through the Genome Research Open Access option.

    • Received September 1, 2013.
    • Accepted December 28, 2013.

    This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.

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