Allelic diversification after transposable element exaptation promoted gsdf as the master sex determining gene of sablefish
- Amaury Herpin1,2,12,
- Manfred Schartl3,4,12,
- Alexandra Depincé1,
- Yann Guiguen1,
- Julien Bobe1,
- Aurélie Hua-Van5,
- Edward S. Hayman6,
- Anna Octavera7,
- Goro Yoshizaki7,
- Krista M. Nichols8,
- Giles W. Goetz9 and
- J. Adam Luckenbach10,11
- 1INRAE, LPGP, 35000, Rennes, France;
- 2State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal University, Changsha, 410081, Hunan, P.R. China;
- 3University of Wuerzburg, Developmental Biochemistry, Biocenter, 97074 Wuerzburg, Germany;
- 4Xiphophorus Genetic Stock Center, Texas State University, San Marcos, Texas 78666, USA;
- 5Laboratoire Evolution, Génomes Comportement, Ecologie, CNRS Université Paris-Saclay, UMR 9191, IRD UMR 247, F-91198 Gif-sur-Yvette, France;
- 6Ocean Associates Incorporated, under contract to Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, Washington 98112, USA;
- 7Department of Marine Biosciences, Tokyo University of Marine Science and Technology, Tokyo 108-8477, Japan;
- 8Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, Washington 98112, USA;
- 9Cooperative Institutes for Climate, Ocean, and Environmental Sciences, University of Washington, Seattle, Washington 98112, USA;
- 10Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, Washington 98112, USA;
- 11Center for Reproductive Biology, Washington State University, Pullman, Washington 99164, USA
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↵12 These authors contributed equally to this work.
Abstract
Concepts of evolutionary biology suggest that morphological change may occur by rare punctual but rather large changes, or by more steady and gradual transformations. It can therefore be asked whether genetic changes underlying morphological, physiological, and/or behavioral innovations during evolution occur in a punctual manner, whereby a single mutational event has prominent phenotypic consequences, or if many consecutive alterations in the DNA over longer time periods lead to phenotypic divergence. In the marine teleost, sablefish (Anoplopoma fimbria), complementary genomic and genetic studies led to the identification of a sex locus on the Y Chromosome. Further characterization of this locus resulted in identification of the transforming growth factor, beta receptor 1a (tgfbr1a) gene, gonadal somatic cell derived factor (gsdf), as the main candidate for fulfilling the master sex determining (MSD) function. The presence of different X and Y Chromosome copies of this gene indicated that the male heterogametic (XY) system of sex determination in sablefish arose by allelic diversification. The gsdfY gene has a spatio-temporal expression profile characteristic of a male MSD gene. We provide experimental evidence demonstrating a pivotal role of a transposable element (TE) for the divergent function of gsdfY. By insertion within the gsdfY promoter region, this TE generated allelic diversification by bringing cis-regulatory modules that led to transcriptional rewiring and thus creation of a new MSD gene. This points out, for the first time in the scenario of MSD gene evolution by allelic diversification, a single, punctual molecular event in the appearance of a new trigger for male development.
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 https://www.genome.org/cgi/doi/10.1101/gr.274266.120.
- Received November 10, 2020.
- Accepted June 22, 2021.
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