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Caenorhabditis elegans dpy-14: an essential collagen gene with unique expression profile and physiological roles in early development

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Abstract

We describe the molecular characterisation of Caenorhabditis elegans dpy-14, a gene encoding an essential cuticular collagen annotated as col-59. Expression of dpy-14 starts at the 16 E cell stage, making it the earliest-expressing collagen reported to date. SAGE data and dpy-14 promoter::GFP reporter constructs indicate that the gene is transcribed mainly during embryogenesis, specifically in ciliated neurons and hypoderm. Water permeability assays and lectin staining showed that a mutation in the DPY-14 collagen results in defects in the channels of the amphids, which are a class of ciliated neuron, while the amphids appear morphologically normal by dye filling methods. Behavioural assays showed that the ciliated neurons expressing the gene are functional in dpy-14 mutants. All together, our data suggest that ciliated neurons and their hypodermal support cells collaborate in the transcription and synthesis of DPY-14, which then becomes a component of the amphid channels but not of the amphids proper. Interestingly, seam cells of dpy-14 mutants do not properly fuse to form a syncytium. This novel phenotype due to collagen mutations further stresses that dpy-14 plays a fundamental role in C. elegans physiology, since it is required for the proper development of the hypoderm.

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Acknowledgements

We thank Dr Oliver E. Blacque for insightful discussions on the structure and function of the C. elegans ciliated neurons and on the experimental approach to analyse them. Thanks also to Martin Jones and Dr Nigel O’Neal for important comments and discussions. Strains were obtained from the CGC. SAGE data were obtained from the Genome BC C. elegans Gene Expression Consortium (http://www.elegans.bcgsc.bc.ca/). These SAGE data were produced at the Michael Smith Genome Sciences Centre with funding from Genome Canada. Funding for the present study was provided by the Natural Sciences and Engineering Research Council (NSERC) of Canada to DLB and AMR.

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  1. Department of Molecular Biology and Biochemistry, Simon Fraser University, 8888 University Drive, V5A 1S6, Burnaby, BC, Canada

    Marco Gallo, Allan K. Mah, Robert C. Johnsen & David L. Baillie

  2. Department of Medical Genetics, University of British Columbia, V6T 1Z3, Vancouver, BC, Canada

    Ann M. Rose

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  1. Marco Gallo
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Correspondence to David L. Baillie.

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Communicated by S. Hohmann

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Gallo, M., Mah, A.K., Johnsen, R.C. et al. Caenorhabditis elegans dpy-14: an essential collagen gene with unique expression profile and physiological roles in early development. Mol Genet Genomics 275, 527–539 (2006). https://doi.org/10.1007/s00438-006-0110-3

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