Abstract
One of the central questions of developmental biology is how cells of equivalent potential—an equivalence group—come to adopt specific cellular fates. In this study we have used a combination of live imaging, single cell lineage analyses, and perturbation of specific signaling pathways to dissect the specification of the adaxial cells of the zebrafish embryo. We show that the adaxial cells are myogenic precursors that form a cell fate equivalence group of approximately 20 cells that consequently give rise to two distinct sub-types of muscle fibers: the superficial slow muscle fibers (SSFs) and muscle pioneer cells (MPs), distinguished by specific gene expression and cell behaviors. Using a combination of live imaging, retrospective and indicative fate mapping, and genetic studies, we show that MP and SSF precursors segregate at the beginning of segmentation and that they arise from distinct regions along the anterior-posterior (AP) and dorsal-ventral (DV) axes of the adaxial cell compartment. FGF signaling restricts MP cell fate in the anterior-most adaxial cells in each somite, while BMP signaling restricts this fate to the middle of the DV axis. Thus our results reveal that the synergistic actions of HH, FGF, and BMP signaling independently create a three-dimensional (3D) signaling milieu that coordinates cell fate within the adaxial cell equivalence group.
Highlights
The mechanisms that are utilised to generate individual cell types from a set of equivalently fated set of precursors remains a central experimental focus of developmental biology
In this study we use lineage tracing live imaging and the manipulation of distinct genetic pathways to demonstrate that the adaxial cells form a cell fate ‘‘equivalence group’’ that is specified using separate signaling pathways that operating in distinct dimensions
There, the slow muscle fibers (SSFs) precursors complete their differentiation to form a monolayer of approximately 20 slow twitch muscle fibers
Summary
The mechanisms that are utilised to generate individual cell types from a set of equivalently fated set of precursors remains a central experimental focus of developmental biology. Studies from invertebrate systems have defined the concept of an equivalence group, where small clusters of lineage related cells are determined by a combination of inductive and intrinsic signals to adopt individual fates [1,2,3,4,5,6]. The early differentiating slow-muscle cells arise from a particular subset of presomitic mesodermal cells, termed the adaxial cells, which at the end of gastrulation align medially against the notochord [8] These precursors initially adopt a pseudo epithelial morphology but shortly after their incorporation within the formed somite, undergo stereotypic morphogenetic cell shape changes, moving from their columnar shape to flatten and interleave, adopting a triangular shape, that upon further differentiation results in single adaxial cells extending from one somite boundary to the other. These cells collectively flatten medio-laterally to form a set of elongated myocytes that span the somite, positioned against the notochord [9]
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