Ordered arrangement of dendrites within a C. elegans sensory nerve bundle

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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.

Data availability

A browser (http://heimanlab.com/ibb) has been developed to provide access to the extensive underlying dataset (475 fasciculated dendrite bundles consisting of three pairwise distance measurements and corresponding p-value rankings at 100 positions per bundle). Code used for data analysis is available at http://github.com/zcandiceyip/dendrite_fasciculation.

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Author details

Zhiqi Candice Yip

Division of Genetics, Boston Children's Hospital, Boston, United States

Competing interests
The authors declare that no competing interests exist.
Maxwell G Heiman

Department of Genetics, Boston Children's Hospital, Boston, United States

For correspondence
heiman@genetics.med.harvard.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2557-6490

Funding

National Institutes of Health (R01GM108754)

Maxwell G Heiman

National Science Foundation (Graduate Student Research Fellowship)

Zhiqi Candice Yip

Harvard University (Milton Fund)

Maxwell G Heiman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.