{"title":"Embryonic Genome Activation (EGA) Occurred at 1-Cell Stage of Embryonic Development in the Mud Crab, Scylla paramamosain, Revealed by RNA-Seq","authors":"Li-Kun Xu, Chun-Yan Ma, Feng-Ying Zhang, Wei Wang, Ming Zhao, Xin Jin, Jin-Ju Yin, Ling-Bo Ma, Wei Chen, Jia-Yuan Xu, Ke-Yi Ma, Zhi-Qiang Liu","doi":"10.1007/s10126-024-10369-x","DOIUrl":null,"url":null,"abstract":"<div><p>As a prerequisite for the success of embryo development, embryonic genome activation (EGA) is an important biological event in which zygotic gene products in the embryo are activated to replace maternal-derived transcripts. Although EGA has been extensively studied in a large number of vertebrates and invertebrates, there is a lack of information regarding this event in crustacean crab. In this study, the timing of EGA was confirmed by examining a transcriptomic dataset of early embryonic development, including mature oocytes and embryos through six early developmental stages, and signaling pathways associated with EGA were identified in the mud crab, <i>S. paramamosain.</i> The comprehensive transcriptomic data identified a total of 53,915 transcripts from these sequencing samples. Notable transcriptomic change was evident at the 1-cell stage, indicated by a 36% transcript number shift and a reduction in transcript fragment length, compared to those present in the mature oocytes. Concurrently, a substantial increase in the expression of newly transcribed transcripts was observed, with gene counts reaching 3485 at the 1-cell stage, indicative of the onset of EGA. GO functional enrichment revealed key biological processes initiated at the 1-cell stage, such as protein complex formation, protein metabolism, and various biosynthetic processes. KEGG analysis identified several critical signaling pathways activated during EGA, including the “cell cycle,” “spliceosome,” “RNA degradation”, and “RNA polymerase”, pathways. Furthermore, transcription factor families, including zinc finger, T-box, Nrf1, and Tub were predominantly enriched at the 1-cell stage, suggesting their pivotal roles in regulating embryonic development through the targeting of specific DNA sequences during the EGA process. This groundbreaking study not only addresses a significant knowledge gap regarding the developmental biology of <i>S. paramamosain</i>, especially for the understanding of the mechanism underlying EGA, but also provides scientific data crucial for the research on the individual synchronization of seed breeding within <i>S. paramamosain</i> aquaculture. Additionally, it serves as a reference basis for the study of early embryonic development in other crustacean species.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 6","pages":"1246 - 1259"},"PeriodicalIF":2.6000,"publicationDate":"2024-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Marine Biotechnology","FirstCategoryId":"99","ListUrlMain":"https://link.springer.com/article/10.1007/s10126-024-10369-x","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
As a prerequisite for the success of embryo development, embryonic genome activation (EGA) is an important biological event in which zygotic gene products in the embryo are activated to replace maternal-derived transcripts. Although EGA has been extensively studied in a large number of vertebrates and invertebrates, there is a lack of information regarding this event in crustacean crab. In this study, the timing of EGA was confirmed by examining a transcriptomic dataset of early embryonic development, including mature oocytes and embryos through six early developmental stages, and signaling pathways associated with EGA were identified in the mud crab, S. paramamosain. The comprehensive transcriptomic data identified a total of 53,915 transcripts from these sequencing samples. Notable transcriptomic change was evident at the 1-cell stage, indicated by a 36% transcript number shift and a reduction in transcript fragment length, compared to those present in the mature oocytes. Concurrently, a substantial increase in the expression of newly transcribed transcripts was observed, with gene counts reaching 3485 at the 1-cell stage, indicative of the onset of EGA. GO functional enrichment revealed key biological processes initiated at the 1-cell stage, such as protein complex formation, protein metabolism, and various biosynthetic processes. KEGG analysis identified several critical signaling pathways activated during EGA, including the “cell cycle,” “spliceosome,” “RNA degradation”, and “RNA polymerase”, pathways. Furthermore, transcription factor families, including zinc finger, T-box, Nrf1, and Tub were predominantly enriched at the 1-cell stage, suggesting their pivotal roles in regulating embryonic development through the targeting of specific DNA sequences during the EGA process. This groundbreaking study not only addresses a significant knowledge gap regarding the developmental biology of S. paramamosain, especially for the understanding of the mechanism underlying EGA, but also provides scientific data crucial for the research on the individual synchronization of seed breeding within S. paramamosain aquaculture. Additionally, it serves as a reference basis for the study of early embryonic development in other crustacean species.
作为胚胎发育成功的先决条件,胚胎基因组激活(EGA)是胚胎中子代基因产物被激活以取代母源转录本的重要生物学事件。虽然 EGA 已在大量脊椎动物和无脊椎动物中得到广泛研究,但有关甲壳类蟹类中这一事件的信息还很缺乏。在这项研究中,通过研究早期胚胎发育的转录组数据集(包括成熟卵母细胞和胚胎的六个早期发育阶段),确认了 EGA 的时间,并确定了与泥蟹(S. paramamosain)EGA 相关的信号通路。从这些测序样本中,综合转录组数据共鉴定出 53,915 个转录本。与成熟卵母细胞中的转录本相比,1细胞阶段的转录本组变化明显,转录本数量变化了36%,转录本片段长度减少。与此同时,还观察到新转录的转录本表达量大幅增加,在 1 细胞阶段基因数量达到 3485 个,表明 EGA 开始。GO 功能富集揭示了在 1 细胞阶段启动的关键生物过程,如蛋白质复合物形成、蛋白质代谢和各种生物合成过程。KEGG 分析确定了 EGA 期间激活的几个关键信号通路,包括 "细胞周期"、"剪接体"、"RNA 降解 "和 "RNA 聚合酶 "等通路。此外,包括锌指、T-box、Nrf1 和 Tub 在内的转录因子家族主要在 1 细胞阶段富集,这表明它们在 EGA 过程中通过靶向特定 DNA 序列调控胚胎发育方面发挥着关键作用。这项开创性的研究不仅填补了副栉水母胚胎发育生物学方面的重大知识空白,特别是有助于理解 EGA 的内在机制,而且为副栉水母养殖过程中的个体同步育种研究提供了至关重要的科学数据。此外,它还是研究其他甲壳类物种早期胚胎发育的参考依据。
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.