Michael Sars Centre, University of Bergen, Bergen, Norway.
Center for Developmental Genetics, Department of Biology, New York University, New York, NY, USA.
EMBO Rep. 2024 May;25(5):2188-2201. doi: 10.1038/s44319-024-00139-0. Epub 2024 Apr 22.
Transcription control is a major determinant of cell fate decisions in somatic tissues. By contrast, early germline fate specification in numerous vertebrate and invertebrate species relies extensively on RNA-level regulation, exerted on asymmetrically inherited maternal supplies, with little-to-no zygotic transcription. However delayed, a maternal-to-zygotic transition is nevertheless poised to complete the deployment of pre-gametic programs in the germline. Here, we focus on early germline specification in the tunicate Ciona to study zygotic genome activation. We first demonstrate that a peculiar cellular remodeling event excludes localized postplasmic Pem-1 mRNA, which encodes the general inhibitor of transcription. Subsequently, zygotic transcription begins in Pem-1-negative primordial germ cells (PGCs), as revealed by histochemical detection of elongating RNA Polymerase II, and nascent Mef2 transcripts. In addition, we uncover a provisional antagonism between JAK and MEK/BMPRI/GSK3 signaling, which controls the onset of zygotic gene expression, following cellular remodeling of PGCs. We propose a 2-step model for the onset of zygotic transcription in the Ciona germline and discuss the significance of germ plasm dislocation and remodeling in the context of developmental fate specification.
转录调控是体细胞组织中细胞命运决定的主要决定因素。相比之下，在许多脊椎动物和无脊椎动物物种中，早期生殖系命运的特化在很大程度上依赖于 RNA 水平的调控，这些调控作用于不对称遗传的母体供应物上，而合子转录的作用很小或没有。然而，尽管延迟了，母体到合子的转变仍然准备好在生殖系中完成预配子程序的部署。在这里，我们专注于研究被囊动物海鞘中的早期生殖系特化，以研究合子基因组激活。我们首先证明了一种特殊的细胞重塑事件排除了局部的后质体 Pem-1mRNA，该 mRNA 编码转录的一般抑制剂。随后，通过延伸 RNA 聚合酶 II 和新生 Mef2 转录物的组织化学检测，在 Pem-1 阴性原始生殖细胞 (PGC) 中开始合子转录。此外，我们揭示了 JAK 和 MEK/BMPRI/GSK3 信号之间的临时拮抗作用，该作用控制了 PGC 细胞重塑后合子基因表达的开始。我们提出了一个两步模型，用于解释被囊动物生殖系中合子转录的开始，并讨论了生殖质易位和重塑在发育命运特化中的意义。
