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Development, Vol 119, Issue 1 155-167, Copyright © 1993 by Company of Biologists
JOURNAL ARTICLES |
CA Ettensohn and KM Malinda
Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213.
The formation of the skeleton is a central event in sea urchin morphogenesis. The skeleton serves as a framework for the larval body and is the primary determinant of its shape. Previous studies have shown that the size of the skeleton is invariant despite wide experimentally induced variations in the number of skeleton-forming primary mesenchyme cells (PMCs). In the present study, we have used PMC transplantation, fluorescent cell markers and confocal laser scanning microscopy to analyze cellular aspects of skeletal patterning. Labeling of embryos with 5-bromodeoxyuridine demonstrates that the entire embryonic phase of skeletal morphogenesis occurs in the absence of PMC division. During embryogenesis, skeletal rods elongate by one of two mechanisms; either preceded by a cluster (plug) of PMCs or by extending along an existing PMC filopodial cable. Elongation of skeletal rods occurs exclusively by the addition of new material at the rod tips, although radial growth (increase in rod thickness) occurs along the length of the rods. Photoablation of a distinctive region of ectoderm cells at the arm tip results in an inhibition of skeletal rod elongation, indicating that a local ectoderm-PMC interaction is required for skeletal growth. The regulation of skeletal patterning was also examined in embryos that had been microinjected with additional PMCs and in half-sized larvae derived from blastomeres isolated at the 2-cell stage. Microinjection of 50-100 PMCs into the blastocoel at the mesenchyme blastula stage leads to an increase in the numbers of PMCs along all skeletal rods and a two-fold increase in the number of cells in the plugs, yet no increase in the length of the skeletal rods. The length of the anal rods can, however, be increased by microinjecting developmentally 'young' PMCs into the arm tips of late stage embryos. We find that the rate of skeletal rod elongation is independent of both the mode of rod growth (chain or plug) and the number of PMCs in the plug at the growing rod tip. Instead, the rate of elongation appears to be strictly regulated by the quantity of ectodermal tissue present in the embryo. These studies provide new information concerning normal mechanisms of skeletal growth and patterning and lead us to propose a model for the regulation of skeleton size based upon an intrinsic PMC 'clock' and an ectoderm-derived signal that regulates the rate of skeletal rod elongation.
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