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Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing

Zexian Zhu, Kazumi Matsubara, Foyez Shams, Jason Dobry, Erik Wapstra, Tony Gamble, Stephen D. Sarre, Arthur Georges, Jennifer A. Marshall Graves, Qi Zhou, View ORCID ProfileTariq Ezaz
doi: https://doi.org/10.1101/2021.10.13.462063
Zexian Zhu
1MOE Laboratory of Biosystems Homeostasis and Protection and Zhejiang Provincial Key Laboratory for Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou, 310058, China
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Kazumi Matsubara
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
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Foyez Shams
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
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Jason Dobry
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
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Erik Wapstra
3School of Biological Sciences, University of Tasmania, Hobart, Tasmania 7001, Australia
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Tony Gamble
4Department of Biological Sciences, Marquette University, Milwaukee, Wisconsin, 52322, United States of America
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Stephen D. Sarre
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
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Arthur Georges
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
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Jennifer A. Marshall Graves
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
5School of Life Science, La Trobe University, Melbourne 3168 Australia
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Qi Zhou
1MOE Laboratory of Biosystems Homeostasis and Protection and Zhejiang Provincial Key Laboratory for Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou, 310058, China
7Department of Neuroscience and Developmental Biology, University of Vienna, Vienna, 1030, Austria
8Center for Reproductive Medicine, The 2nd Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China
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  • For correspondence: zhouqi1982@zju.edu.cn Tariq.Ezaz@canberra.edu.au
Tariq Ezaz
2Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, Australia
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  • ORCID record for Tariq Ezaz
  • For correspondence: zhouqi1982@zju.edu.cn Tariq.Ezaz@canberra.edu.au
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Abstract

Reptile sex determination is attracting much attention because the great diversity of sex-determination and dosage compensation mechanisms permits us to approach fundamental questions about sex chromosome turnover and evolution. However, reptile sex chromosome variation remains largely uncharacterized and no reptile master sex determination genes have yet been identified. Here we describe a powerful and cost-effective “chromosomics” approach, combining probes generated from the microdissected sex chromosomes with transcriptome sequencing to explore this diversity in non-model Australian reptiles with heteromorphic or cryptic sex chromosomes. We tested the pipeline on a turtle, a gecko, and a worm-lizard, and we also identified sequences located on sex chromosomes in a monitor lizard using linked-read sequencing. Genes identified on sex chromosomes were compared to the chicken genome to identify homologous regions among the four species. We identified candidate sex determining genes within these regions, including conserved vertebrate sex-determining genes pdgfa, pdgfra amh and wt1, and demonstrated their testis or ovary-specific expression. All four species showed gene-by-gene rather than chromosome-wide dosage compensation. Our results imply that reptile sex chromosomes originated by independent acquisition of sex-determining genes on different autosomes, as well as translocations between different ancestral macro- and micro-chromosomes. We discuss the evolutionary drivers of the slow differentiation, but rapid turnover, of reptile sex chromosomes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† Current affiliation: Department of Environmental Biology, College of Bioscience and Biotechnology, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi 487-8501, Japan

  • https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA737594

  • https://ngdc.cncb.ac.cn/gwh/Assembly/reviewer/FEwDjeeBfCJBRWmjKmltbTByfgnYNzdbUPMYDAdsouQsSXwAfYrRVofsBnyhPNnF

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 14, 2021.
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Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing
Zexian Zhu, Kazumi Matsubara, Foyez Shams, Jason Dobry, Erik Wapstra, Tony Gamble, Stephen D. Sarre, Arthur Georges, Jennifer A. Marshall Graves, Qi Zhou, Tariq Ezaz
bioRxiv 2021.10.13.462063; doi: https://doi.org/10.1101/2021.10.13.462063
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Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing
Zexian Zhu, Kazumi Matsubara, Foyez Shams, Jason Dobry, Erik Wapstra, Tony Gamble, Stephen D. Sarre, Arthur Georges, Jennifer A. Marshall Graves, Qi Zhou, Tariq Ezaz
bioRxiv 2021.10.13.462063; doi: https://doi.org/10.1101/2021.10.13.462063

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