Journal Article

Sox5 is involved in germ-cell regulation and sex determination in medaka following co-option of nested transposable elements

Wilhelm, Dagmar, Comprehensive Cancer Center Mainfranken ; University Clinic Würzburg, Guiguen, Yann, Physiological Chemistry, Biocenter ; Julius-Maximilians-Universität Würzburg = University of Würzburg (JMU), ANR-16-COFA-0004,AquaCrispr,Optimization of the CRISPR/Cas9 knock-in technology and application in salmon and trout, Universität Heidelberg [Heidelberg] = Heidelberg University, Department of Anatomy & Neuroscience [Melbourne] ; School of Biomedical Sciences [Melbourne] ; Faculty of Medicine, Dentistry and Health Sciences [Melbourne] ; University of Melbourne-University of Melbourne-Faculty of Medicine, Dentistry and Health Sciences [Melbourne] ; University of Melbourne-University of Melbourne, Centanin, Lazaro, Physiological Chemistry ; Julius-Maximilians-Universität Würzburg = University of Würzburg (JMU), Mourot, Brigitte, Schories, Susanne, Herpin, Amaury, Laboratoire de Physiologie et Génomique des Poissons (LPGP) ; Institut National de la Recherche Agronomique (INRA)-Structure Fédérative de Reche

2018

Overview

Background - Sex determination relies on a hierarchically structured network of genes, and is one of the most plastic processes in evolution. The evolution of sex-determining genes within a network, by neo- or sub-functionalization, also requires the regulatory landscape to be rewired to accommodate these novel gene functions. We previously showed that in medaka fish, the regulatory landscape of the master male-determining gene dmrt1bY underwent a profound rearrangement, concomitantly with acquiring a dominant position within the sex-determining network. This rewiring was brought about by the exaptation of a transposable element (TE) called Izanagi, which is co-opted to act as a silencer to turn off the dmrt1bY gene after it performed its function in sex determination. Results - We now show that a second TE, Rex1, has been incorporated into Izanagi. The insertion of Rex1 brought in a preformed regulatory element for the transcription factor Sox5, which here functions in establishing the temporal and cell-type-specific expression pattern of dmrt1bY. Mutant analysis demonstrates the importance of Sox5 in the gonadal development of medaka, and possibly in mice, in a dmrt1bY-independent manner. Moreover, Sox5 medaka mutants have complete female-to-male sex reversal. Conclusions - Our work reveals an unexpected complexity in TE-mediated transcriptional rewiring, with the exaptation of a second TE into a network already rewired by a TE. We also show a dual role for Sox5 during sex determination: first, as an evolutionarily conserved regulator of germ-cell number in medaka, and second, by de novo regulation of dmrt1 transcriptional activity during primary sex determination due to exaptation of the Rex1 transposable element.

• Publisher: HAL CCSD,BioMed Central,BioMed Central Ltd,BMC
• Subject: Analysis / Animals / Animals, Genetically Modified / Biomedical and Life Sciences / Cellular control mechanisms / Computer Science / Dmrt1bY / DNA Transposable Elements - physiology / Exaptation / Female / Germ Cells - metabolism / In the Light of Evolution / Life Sciences / Male / Master sex-determining gene / Medaka / Oryzias / Research Article / Sex Chromosomes - genetics / Sex Chromosomes - metabolism / Sex Determination Processes - physiology / Sex determination, Genetic / Sex recognition (Zoology) / Sox5 / SOXD Transcription Factors - biosynthesis / SOXD Transcription Factors - genetics / Transcriptional rewiring
• ISBN: 0004238248000