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Chromosome fusions shape an ancient UV sex chromosome system

View ORCID ProfileSarah B. Carey, Jerry Jenkins, Adam C. Payton, Shenqiang Shu, John T. Lovell, Florian Maumus, Avinash Sreedasyam, George P. Tiley, Noe Fernandez-Pozo, Kerrie Barry, Cindy Chen, Mei Wang, Anna Lipzen, Chris Daum, Christopher A. Saski, Jordan C. McBreen, Roth E. Conrad, Leslie M. Kollar, Sanna Olsson, Sanna Huttunen, Jacob B. Landis, J. Gordon Burleigh, Norman J. Wickett, Matthew G. Johnson, Stefan A. Rensing, Jane Grimwood, Jeremy Schmutz, View ORCID ProfileStuart F. McDaniel
doi: https://doi.org/10.1101/2020.07.03.163634
Sarah B. Carey
1Department of Biology, University of Florida, Gainesville, FL, USA
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Jerry Jenkins
2Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
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Adam C. Payton
1Department of Biology, University of Florida, Gainesville, FL, USA
3RAPiD Genomics, Gainesville, FL, USA
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Shenqiang Shu
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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John T. Lovell
2Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
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Florian Maumus
5Université Paris-Saclay, INRAE, URGI, 78026, Versailles, France
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Avinash Sreedasyam
2Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
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George P. Tiley
6Department of Biology, Duke University, Durham, NC, USA
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Noe Fernandez-Pozo
7Plant Cell Biology, University of Marburg, Marburg, Germany
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Kerrie Barry
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Cindy Chen
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Mei Wang
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Anna Lipzen
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Chris Daum
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Christopher A. Saski
8Department of Plant and Environmental Sciences, Clemson University, Clemson, SC, USA
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Jordan C. McBreen
1Department of Biology, University of Florida, Gainesville, FL, USA
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Roth E. Conrad
9School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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Leslie M. Kollar
1Department of Biology, University of Florida, Gainesville, FL, USA
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Sanna Olsson
10Department of Forest Ecology and Genetics, INIA-CIFOR, Madrid, Spain
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Sanna Huttunen
11Department of Biology & Biodiversity Unit, University of Turku, Finland
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Jacob B. Landis
12School of Integrative Plant Science, Section of Plant Biology and the L.H. Bailey Hortorium, Cornell University, Ithaca, NY, USA
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J. Gordon Burleigh
1Department of Biology, University of Florida, Gainesville, FL, USA
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Norman J. Wickett
13Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, Glencoe, IL, USA
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Matthew G. Johnson
14Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA
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Stefan A. Rensing
7Plant Cell Biology, University of Marburg, Marburg, Germany
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Jane Grimwood
2Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Jeremy Schmutz
2Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
4US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Stuart F. McDaniel
1Department of Biology, University of Florida, Gainesville, FL, USA
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  • ORCID record for Stuart F. McDaniel
  • For correspondence: stuartmcdaniel@ufl.edu
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Abstract

Sex chromosomes occur in diverse organisms, but their structural complexity has often prevented evolutionary analyses. Here we use two chromosome-scale reference genomes of the moss Ceratodon purpureus to trace the evolution of the sex chromosomes in bryophytes. Comparative analyses show the moss genome comprises seven remarkably stable ancestral chromosomal elements. An exception is the sex chromosomes, which share thousands of broadly-expressed genes but lack any synteny. We show the sex chromosomes evolved over 300 million years ago and expanded via at least two distinct chromosomal fusions. These results link suppressed recombination between the sex chromosomes with rapid structural change and the evolution of distinct transposable element compositions, and suggest haploid gene expression promotes the evolution of independent female and male gene-regulatory networks.

One Sentence Summary Moss sex chromosomes retain thousands of broadly-expressed genes despite millions of years of suppressed recombination.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Chromosome fusions shape an ancient UV sex chromosome system
Sarah B. Carey, Jerry Jenkins, Adam C. Payton, Shenqiang Shu, John T. Lovell, Florian Maumus, Avinash Sreedasyam, George P. Tiley, Noe Fernandez-Pozo, Kerrie Barry, Cindy Chen, Mei Wang, Anna Lipzen, Chris Daum, Christopher A. Saski, Jordan C. McBreen, Roth E. Conrad, Leslie M. Kollar, Sanna Olsson, Sanna Huttunen, Jacob B. Landis, J. Gordon Burleigh, Norman J. Wickett, Matthew G. Johnson, Stefan A. Rensing, Jane Grimwood, Jeremy Schmutz, Stuart F. McDaniel
bioRxiv 2020.07.03.163634; doi: https://doi.org/10.1101/2020.07.03.163634
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Chromosome fusions shape an ancient UV sex chromosome system
Sarah B. Carey, Jerry Jenkins, Adam C. Payton, Shenqiang Shu, John T. Lovell, Florian Maumus, Avinash Sreedasyam, George P. Tiley, Noe Fernandez-Pozo, Kerrie Barry, Cindy Chen, Mei Wang, Anna Lipzen, Chris Daum, Christopher A. Saski, Jordan C. McBreen, Roth E. Conrad, Leslie M. Kollar, Sanna Olsson, Sanna Huttunen, Jacob B. Landis, J. Gordon Burleigh, Norman J. Wickett, Matthew G. Johnson, Stefan A. Rensing, Jane Grimwood, Jeremy Schmutz, Stuart F. McDaniel
bioRxiv 2020.07.03.163634; doi: https://doi.org/10.1101/2020.07.03.163634

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