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

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<jats:title>Abstract</jats:title><jats:sec> <jats:title>Background</jats:title> <jats:p>Fishes are the one of the most diverse groups of animals with respect to their modes of sex determination, providing unique models for uncovering the evolutionary and molecular mechanisms underlying sex determination and reversal. Here, we have investigated how sex is determined in a species of both commercial and ecological importance, the Siamese fighting fish <jats:italic>Betta splendens</jats:italic>.</jats:p> </jats:sec><jats:sec> <jats:title>Results</jats:title> <jats:p>We conducted association mapping on four commercial and two wild populations of <jats:italic>B. splendens</jats:italic>. In three of the four commercial populations, the master sex determining (MSD) locus was found to be located in a region of ~ 80 kb on LG2 which harbours five protein coding genes, including <jats:italic>dmrt1</jats:italic>, a gene involved in male sex determination in different animal taxa. In these fish, <jats:italic>dmrt1</jats:italic> shows a male-biased gonadal expression from undifferentiated stages to adult organs and the knockout of this gene resulted in ovarian development in XY genotypes. Genome sequencing of XX and YY genotypes identified a transposon, <jats:italic>drbx1</jats:italic>, inserted into the fourth intron of the X-linked <jats:italic>dmrt1</jats:italic> allele. Methylation assays revealed that epigenetic changes induced by <jats:italic>drbx1</jats:italic> spread out to the promoter region of <jats:italic>dmrt1</jats:italic>. In addition, <jats:italic>drbx1</jats:italic> being inserted between two closely linked <jats:italic>cis</jats:italic>-regulatory elements reduced their enhancer activities. Thus, epigenetic changes, induced by <jats:italic>drbx1</jats:italic>, contribute to the reduced expression of the X-linked <jats:italic>dmrt1</jats:italic> allele, leading to female development. This represents a previously undescribed solution in animals relying on <jats:italic>dmrt1</jats:italic> function for sex determination. Differentiation between the X and Y chromosomes is limited to a small region of ~ 200 kb surrounding the MSD gene. Recombination suppression spread slightly out of the SD locus. However, this mechanism was not found in the fourth commercial stock we studied, or in the two wild populations analysed, suggesting that it originated recently during domestication.</jats:p> </jats:sec><jats:sec> <jats:title>Conclusions</jats:title> <jats:p>Taken together, our data provide novel insights into the role of epigenetic regulation of <jats:italic>dmrt1</jats:italic> in sex determination and turnover of SD systems and suggest that fighting fish are a suitable model to study the initial stages of sex chromosome evolution.</jats:p> </jats:sec>

収録刊行物

  • BMC Biology

    BMC Biology 20 (1), 5-, 2022-01-07

    Springer Science and Business Media LLC

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