Allelic diversification after transposable element exaptation promotedgsdfas the master sex determining gene of sablefish

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.

Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish

“…It is hypothesized that transposable elements (TEs) are not only involved in the rewiring of regulatory networks to adapt to rapid turnover of SD systems as cis -regulatory elements [ 53 – 55 ] but are also able to directly regulate the expression patterns of key SD players and drive the turnover of the SD systems [ 24 , 27 ]. It is reported that a transposon-induced methylation of the promoter of a transcription factor CmWIP1 suppresses expression and thereby brings about sex determination in a plant species, the melon (Cucumis melo L.) [ 27 ].…”

“…Besides this mechanism, transposons can also introduce novel transcription factor binding sites and mediate cis -regulation of gene expressions [ 53 , 58 , 59 ]. Previous studies in medaka and sablefish ( Anoplopoma fimbria ) have shown that transposons are involved in sex determination and act as regulatory elements by transcriptional rewiring of the SD regulatory network during the evolution of novel master SD genes [ 53 – 55 ]. Thus, transposons can play vital roles not only in driving differentiation between a pair of sex chromosomes [ 13 , 60 , 61 ] but also in the transitions of SD systems and turnover of sex chromosomes [ 27 ].…”

Homozygous Mutation of gsdf Causes Infertility in Female Nile Tilapia (Oreochromis niloticus)

“…In Philippine medaka ( Oryzias luzonensis ) and sablefish ( Anoplopoma fimbria ), the gsdfY that evolved from autosomal gsdf via allelic diversification is the male sex determination gene ( 3 , 4 ). Autosomal gsdf is required for testicular differentiation in Japanese medaka ( O. latipes ) and Nile tilapia ( Oreochromis niloticus ), as XY gsdf -/- individuals undergo sex reversal from male to female ( 5 – 7 ).…”

A chromosome-level genome assembly enables the identification of the follicle stimulating hormone receptor as the master sex determining gene in Solea senegalensis

“…Fish display highly diverse chromosome SD systems (Cioffi et al, 2017) and several master SD genes have been reported in this group (Martínez et al, 2014). Among them, classical transcription factors such as dmy (Matsuda et al, 2002; Wang et al, 2022), sox3 (Takehana et al, 2014) or sox2 (Martínez et al, 2021); transforming growth factor ß-related genes such as gsdf (Myosho et al, 2012; Herpin et al, 2021) or amh (Hattori et al, 2012; Pan et al, 2019) and its receptor amhr2 (Kamiya et al, 2012; Feron et al, 2020; Nakamoto et al, 2021; Wen et al, 2022); genes related to the steroidogenic pathway such as bcar1 (Bao et al, 2019) or hsd17b1 (Koyama et al, 2019); and finally, some unexpected SD genes, such as the interferon-related sdY in salmonids (Yano et al, 2013). The recent identification of several master SD genes in this group has been associated with the highly contiguous and reliable chromosome-level genome assemblies achieved via improvements in long-read sequencing technologies, scaffolding and bioinformatic approaches (Ramos and Antunes, 2022).…”