Allelic diversification after transposable element exaptation promoted Gsdf as the master sex determining gene of sablefish
- Amaury HERPIN1,8,
- Manfred Schartl2,
- Alexandra Depince1,
- Yann Guiguen1,
- Julien Bobe1,
- Aurelie Hua-Van3,
- Edward S Hayman4,
- Anna Octavera5,
- Goro Yoshizaki5,
- Krista M Nichols6,
- Giles W Goetz7 and
- John A Luckenbach6
- 1 INRAE, LPGP;
- 2 University of Wuerzburg, Texas State University;
- 3 CNRS Université Paris-Saclay;
- 4 Ocean Associates Inc., Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration;
- 5 Tokyo University of Marine Science and Technology;
- 6 Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration;
- 7 University of Washington
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 (tgfbr1a) gene, gonadal soma-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.
- Received November 10, 2020.
- Accepted June 22, 2021.
- Published by Cold Spring Harbor Laboratory Press
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