Abstract
Biological systems are organized into well-ordered structures and can evolve new patterns when perturbed. To identify principles underlying biological order, we turned to C. elegans for its simple anatomy and powerful genetics. We developed a method to quantify the arrangement of three dendrites in the main sensory nerve bundle, and found that they exhibit a stereotyped arrangement throughout larval growth. Dendrite order does not require prominent features including sensory cilia and glial junctions. In contrast, loss of the cell adhesion molecule (CAM) CDH-4/Fat-like cadherin causes dendrites to be ordered randomly, despite remaining bundled. Loss of the CAMs PTP-3/LAR or SAX-7/L1CAM causes dendrites to adopt an altered order, which becomes increasingly random as animals grow. Misexpression of SAX-7 leads to subtle but reproducible changes in dendrite order. Our results suggest that combinations of CAMs allow dendrites to self-organize into a stereotyped arrangement and can produce altered patterns when perturbed.
Highlights
Biological systems reflect a remarkable hierarchy of structural organization: proteins assemble into nanometer-scale machines, that in turn build cells, that are organized and patterned to form structures as complex as the human brain
We found that loss of either sax-7 or ptp-3 causes amphid dendrites to initially take on a non-random arrangement that is distinct from wild type
We found that amphid dendrites are ordered within the bundle, and this order is maintained over time
Summary
Biological systems reflect a remarkable hierarchy of structural organization: proteins assemble into nanometer-scale machines, that in turn build cells, that are organized and patterned to form structures as complex as the human brain. How do these pieces come together in predictable ways? One can imagine a top-down deterministic approach in which the shape, position, and connections of each biological part are specified, similar to an electrical wiring diagram or an architectural blueprint While this approach is reasonable for simple systems, it breaks down quickly in the face of the complexity we encounter in biology. This concept was first demonstrated in 1955 by Townes and Holtfreter, who dissociated different germ layers of embryonic amphibian cells, mixed them together, and found that these cells re-aggregated and
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