Convergent origination of a Drosophila-like dosage compensation mechanism in a reptile lineage
- Ray Marin1,2,11,
- Diego Cortez3,11,
- Francesco Lamanna4,11,
- Madapura M. Pradeepa5,11,
- Evgeny Leushkin4,
- Philippe Julien6,
- Angélica Liechti1,
- Jean Halbert1,
- Thoomke Brüning4,
- Katharina Mössinger4,
- Timo Trefzer7,
- Christian Conrad7,
- Halie N. Kerver8,
- Juli Wade8,9,
- Patrick Tschopp10 and
- Henrik Kaessmann4
- 1Center for Integrative Genomics, University of Lausanne, CH-1015 Lausanne, Switzerland;
- 2Swiss Institute of Bioinformatics, CH-1015 Lausanne, Switzerland;
- 3Center for Genomic Sciences, UNAM, CP62210 Cuernavaca, Mexico;
- 4Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany;
- 5School of Biological Sciences, University of Essex, Colchester CO4 3SQ, United Kingdom;
- 6EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation, 08003 Barcelona, Spain;
- 7Department of Theoretical Bioinformatics, German Cancer Research Center/BioQuant, D-69120 Heidelberg, Germany;
- 8Neuroscience Program, Michigan State University, East Lansing, Michigan 48824, USA;
- 9Department of Psychology, Michigan State University, East Lansing, Michigan 48824, USA;
- 10Institute of Zoology, University of Basel, 4051 Basel, Switzerland
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↵11 These authors contributed equally to this work.
Abstract
Sex chromosomes differentiated from different ancestral autosomes in various vertebrate lineages. Here, we trace the functional evolution of the XY Chromosomes of the green anole lizard (Anolis carolinensis), on the basis of extensive high-throughput genome, transcriptome and histone modification sequencing data and revisit dosage compensation evolution in representative mammals and birds with substantial new expression data. Our analyses show that Anolis sex chromosomes represent an ancient XY system that originated at least ≈160 million years ago in the ancestor of Iguania lizards, shortly after the separation from the snake lineage. The age of this system approximately coincides with the ages of the avian and two mammalian sex chromosomes systems. To compensate for the almost complete Y Chromosome degeneration, X-linked genes have become twofold up-regulated, restoring ancestral expression levels. The highly efficient dosage compensation mechanism of Anolis represents the only vertebrate case identified so far to fully support Ohno's original dosage compensation hypothesis. Further analyses reveal that X up-regulation occurs only in males and is mediated by a male-specific chromatin machinery that leads to global hyperacetylation of histone H4 at lysine 16 specifically on the X Chromosome. The green anole dosage compensation mechanism is highly reminiscent of that of the fruit fly, Drosophila melanogaster. Altogether, our work unveils the convergent emergence of a Drosophila-like dosage compensation mechanism in an ancient reptilian sex chromosome system and highlights that the evolutionary pressures imposed by sex chromosome dosage reductions in different amniotes were resolved in fundamentally different ways.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.223727.117.
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Freely available online through the Genome Research Open Access option.
- Received April 7, 2017.
- Accepted October 23, 2017.
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/.
