Abstract
Cell lineage, cell cycle, and cell fate are tightly associated in developmental processes, but in vivo studies at single-cell resolution showing the intricacies of these associations are rare due to technical limitations. In this study on the marine annelid Platynereis dumerilii, we investigated the lineage of the 4d micromere, using high-resolution long-term live imaging complemented with a live-cell cycle reporter. 4d is the origin of mesodermal lineages and the germline in many spiralians. We traced lineages at single-cell resolution within 4d and demonstrate that embryonic segmental mesoderm forms via teloblastic divisions, as in clitellate annelids. We also identified the precise cellular origins of the larval mesodermal posterior growth zone. We found that differentially-fated progeny of 4d (germline, segmental mesoderm, growth zone) display significantly different cell cycling. This work has evolutionary implications, sets up the foundation for functional studies in annelid stem cells, and presents newly established techniques for live imaging marine embryos.
Highlights
Development of a multicellular organism requires precise regulation of the cell cycle, which has crucial roles in cell lineage establishment, cell fate decisions, and maintenance of pluripotency
We show that a pair of mesoteloblasts (ML and MR), similar to what has been observed in clitellate annelids, are active during P. dumerilii embryogenesis and that they give rise to the mesodermal derivatives and putative PGCs (pPGCs) via asymmetric cell divisions
Establishment of a work flow for long time-lapse live imaging and cell lineage tracing in marine embryos and larvae
Summary
Development of a multicellular organism requires precise regulation of the cell cycle, which has crucial roles in cell lineage establishment, cell fate decisions, and maintenance of pluripotency. Cell cycle regulation defines the correct timing and pacing of divisions for generating the progenitor cells, as well as maintaining the potency of stem cells themselves (Ables and Drummond-Barbosa, 2013; Barker, 2014; Yasugi and Nishimura, 2016). Understanding the cell cycle characteristics of stem cells and the implications of cell cycle regulation requires a combined lineage tracing and live-cell cycle analysis approach at single-cell resolution. Such high-resolution lineage tracing has been challenging in many traditional and emerging animal model systems, due to a wide range of practical limitations that spans from the inaccessibility of embryos or tissues of interest, to the unavailability of tools and techniques (reviewed in Kretzschmar and Watt, 2012). In order to understand cycling behavior of stem cells and their progeny in vivo, studies are needed in organisms where continuous observations are feasible in intact individuals and tissues
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