Abstract
BackgroundSex 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.ResultsWe 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.ConclusionsOur 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.
Highlights
Sex determination relies on a hierarchically structured network of genes, and is one of the most plastic processes in evolution
We previously showed that this evolutionary innovation, which required a complete rewiring of the regulatory network, was partly brought about by exaptation of a ready-to-use pre-existing cis-regulatory element contributed by a transposable element (TE), called Izanagi [17]
Our work reveals a dual role for sox5 during Sex determination (SD): (i) first being an evolutionarily conserved important regulator of germ-cell number in medaka and possibly beyond and (ii) second, de novo regulation of medaka dmrt1 transcriptional activity during primary SD after it has been recruited for transcriptional rewiring of the dmrt1 promoter due to exaptation of a TE
Summary
Sex determination relies on a hierarchically structured network of genes, and is one of the most plastic processes in evolution. New master SD genes evolved repeatedly and independently [3] This situation is obvious in fish, since closely related sister species can have different genetic SD systems or master SD genes [3,4,5,6,7]. Such a high turnover of genetic determinants can work only if the evolutionary innovations are accompanied by the ability of the respective genes to neofunctionalize or sub-functionalize quickly and efficiently [8, 9].
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
