INRAE, LPGP, Rennes 35000, France.
Physiological Chemistry, Biocenter, University of Wuerzburg, Wuerzburg 97074, Germany.
G3 (Bethesda). 2022 Feb 4;12(2). doi: 10.1093/g3journal/jkab451.
Many salmonids have a male heterogametic (XX/XY) sex determination system, and they are supposed to have a conserved master sex-determining gene (sdY) that interacts at the protein level with Foxl2 leading to the blockage of the synergistic induction of Foxl2 and Nr5a1 of the cyp19a1a promoter. However, this hypothesis of a conserved master sex-determining role of sdY in salmonids is challenged by a few exceptions, one of them being the presence of naturally occurring "apparent" XY Chinook salmon, Oncorhynchus tshawytscha, females. Here, we show that some XY Chinook salmon females have a sdY gene (sdY-N183), with 1 missense mutation leading to a substitution of a conserved isoleucine to an asparagine (I183N). In contrast, Chinook salmon males have both a nonmutated sdY-I183 gene and the missense mutation sdY-N183 gene. The 3-dimensional model of SdY-I183N predicts that the I183N hydrophobic to hydrophilic amino acid change leads to a modification in the SdY β-sandwich structure. Using in vitro cell transfection assays, we found that SdY-I183N, like the wild-type SdY, is preferentially localized in the cytoplasm. However, compared to wild-type SdY, SdY-I183N is more prone to degradation, its nuclear translocation by Foxl2 is reduced, and SdY-I183N is unable to significantly repress the synergistic Foxl2/Nr5a1 induction of the cyp19a1a promoter. Altogether, our results suggest that the sdY-N183 gene of XY Chinook females is nonfunctional and that SdY-I183N is no longer able to promote testicular differentiation by impairing the synthesis of estrogens in the early differentiating gonads of wild Chinook salmon XY females.
许多鲑鱼具有雄性异配子(XX/XY)性别决定系统,它们应该具有保守的主性别决定基因(sdY),该基因在蛋白质水平上与 Foxl2 相互作用,导致 Foxl2 和 Nr5a1 的协同诱导 Cyp19a1a 启动子的阻断。然而,sdY 在鲑鱼中具有保守的主性别决定作用的这一假设受到了一些例外的挑战,其中之一是存在自然发生的“明显”XY 奇努克鲑鱼 Oncorhynchus tshawytscha 雌性。在这里,我们表明,一些 XY 奇努克鲑鱼雌性具有 sdY 基因(sdY-N183),其中 1 个错义突变导致保守的异亮氨酸被天冬酰胺取代(I183N)。相比之下,奇努克鲑鱼雄性既有未突变的 sdY-I183 基因,也有错义突变的 sdY-N183 基因。SdY-I183N 的 3 维模型预测,I183N 疏水性到亲水性氨基酸的变化导致 SdY β-夹心结构的修饰。通过体外细胞转染实验,我们发现 SdY-I183N 与野生型 SdY 一样,优先定位于细胞质中。然而,与野生型 SdY 相比,SdY-I183N 更容易降解,其由 Foxl2 介导的核易位减少,并且 SdY-I183N 无法显著抑制 Cyp19a1a 启动子的协同 Foxl2/Nr5a1 诱导。总的来说,我们的结果表明,XY 奇努克鲑鱼雌性的 sdY-N183 基因是无功能的,并且 SdY-I183N 不再能够通过损害野生奇努克鲑鱼 XY 雌性早期分化性腺中雌激素的合成来促进睾丸分化。