Activin Signaling Pathway Specialization During Embryonic and Skeletal Muscle Development in Rainbow Trout (Oncorhynchus mykiss)

IF 2.6 3区 生物学 Q3 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Marine Biotechnology Pub Date : 2024-07-25 DOI:10.1007/s10126-024-10345-5
Jasmine Richman, Michael Phelps
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Abstract

Activin signaling is essential for proper embryonic, skeletal muscle, and reproductive development. Duplication of the pathway in teleost fish has enabled diversification of gene function across the pathway but how gene duplication influences the function of activin signaling in non-mammalian species is poorly understood. Full characterization of activin receptor signaling pathway expression was performed across embryonic development and during early skeletal muscle growth in rainbow trout (RBT, Oncorhynchus mykiss). Rainbow trout are a model salmonid species that have undergone two additional rounds of whole genome duplication. A small number of genes were expressed early in development and most genes increased expression throughout development. There was limited expression of activin Ab in RBT embryos despite these genes exhibiting significantly elevated expression in post-hatch skeletal muscle. CRISPR editing of the activin Aa1 ohnolog and subsequent production of meiotic gynogenetic offspring revealed that biallelic disruption of activin Aa1 did not result in developmental defects, as occurs with knockout of activin A in mammals. The majority of gynogenetic offspring exhibited homozygous activin Aa1 genotypes (wild type, in-frame, or frameshift) derived from the mosaic founder female. The research identifies mechanisms of specialization among the duplicated activin ohnologs across embryonic development and during periods of high muscle growth in larval and juvenile fish. The knowledge gained provides insights into potential viable gene-targeting approaches for engineering the activin receptor signaling pathway and establishes the feasibility of employing meiotic gynogenesis as a tool for producing homozygous F1 genome-edited fish for species with long-generation times, such as salmonids.

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虹鳟(Oncorhynchus mykiss)胚胎和骨骼肌发育过程中的活化素信号通路特化。
激活素信号对于胚胎、骨骼肌和生殖系统的正常发育至关重要。远洋鱼类中该通路的复制使得整个通路中的基因功能多样化,但基因复制如何影响非哺乳动物物种中的激活素信号转导功能却鲜为人知。我们对虹鳟鱼(RBT,Oncorhynchus mykiss)胚胎发育和骨骼肌早期生长过程中的激活素受体信号通路表达进行了全面鉴定。虹鳟是一种经历了两轮全基因组复制的模式鲑科鱼类。少量基因在发育早期表达,大多数基因在整个发育过程中表达量增加。尽管这些基因在孵化后骨骼肌中的表达量显著增加,但活化素 Ab 在 RBT 胚胎中的表达量有限。对激活蛋白 Aa1 基因进行 CRISPR 编辑并随后产生减数分裂雌雄同体后代的结果表明,激活蛋白 Aa1 基因的双侧缺失不会导致发育缺陷,这与哺乳动物中激活蛋白 A 基因的敲除结果相同。大多数雌核发育后代表现出同源的激活蛋白 Aa1 基因型(野生型、框架内型或框架偏移型),这些基因型来自马赛克创始雌性。这项研究确定了在整个胚胎发育过程中以及在幼鱼和幼鱼肌肉生长旺盛时期,重复的活化因子同源物之间的特化机制。所获得的知识为设计激活素受体信号通路的潜在可行基因靶向方法提供了见解,并确定了利用减数分裂雌核发育作为一种工具,为鲑科鱼类等世代时间较长的物种生产同种F1基因组编辑鱼类的可行性。
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来源期刊
Marine Biotechnology
Marine Biotechnology 工程技术-海洋与淡水生物学
CiteScore
4.80
自引率
3.30%
发文量
95
审稿时长
2 months
期刊介绍: Marine Biotechnology welcomes high-quality research papers presenting novel data on the biotechnology of aquatic organisms. The journal publishes high quality papers in the areas of molecular biology, genomics, proteomics, cell biology, and biochemistry, and particularly encourages submissions of papers related to genome biology such as linkage mapping, large-scale gene discoveries, QTL analysis, physical mapping, and comparative and functional genome analysis. Papers on technological development and marine natural products should demonstrate innovation and novel applications.
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