Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Identification of genes expressed in C. elegans touch receptor neurons

Abstract

The extent of gene regulation in cell differentiation is poorly understood. We previously used saturation mutagenesis to identify 18 genes that are needed for the development and function of a single type of sensory neuron—the touch receptor neuron for gentle touch in Caenorhabditis elegans1,2. One of these genes, mec-3, encodes a transcription factor that controls touch receptor differentiation3,4. By culturing and isolating wild-type and mec-3 mutant cells from embryos and applying their amplified RNA to DNA microarrays, here we have identified genes that are known to be expressed in touch receptors, a previously uncloned gene (mec-17) that is needed for maintaining touch receptor differentiation2,5, and more than 50 previously unknown mec-3-dependent genes. These genes are randomly distributed in the genome and under-represented both for genes that are co-expressed in operons and for multiple members of gene families. Using regions 5′ of the start codon of the first 20 genes, we have also identified an over-represented heptanucleotide, AATGCAT, that is needed for the expression of touch receptor genes6.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Morphology and gene expression of cultured C. elegans cells.
Figure 3: Newly identified mec-3-dependent genes.
Figure 2: The MEC-3::UNC-86 binding site.

Similar content being viewed by others

References

  1. Chalfie, M. & Sulston, J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev. Biol. 82, 358–370 (1981)

    Article  CAS  PubMed  Google Scholar 

  2. Chalfie, M. & Au, M. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243, 1027–1033 (1989)

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Way, J. C. & Chalfie, M. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54, 5–16 (1988)

    Article  CAS  PubMed  Google Scholar 

  4. Way, J. C. & Chalfie, M. The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3, 1823–1833 (1989)

    Article  CAS  PubMed  Google Scholar 

  5. Mitani, S., Du, H., Hall, D. H., Driscoll, M. & Chalfie, M. Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans. Development 119, 773–783 (1993)

    CAS  PubMed  Google Scholar 

  6. Xue, D., Finney, M., Ruvkun, G. & Chalfie, M. Regulation of the mec-3 gene by the C. elegans homeoproteins UNC-86 and MEC-3. EMBO J. 11, 4969–4979 (1992)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Savage, C. et al. mec-7 is a β-tubulin gene required for the production of 15- protofilament microtubules in Caenorhabditis elegans. Genes Dev. 3, 870–881 (1989)

    Article  CAS  PubMed  Google Scholar 

  8. Gu, G., Caldwell, G. A. & Chalfie, M. Genetic interactions affecting touch sensitivity in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 93, 6577–6582 (1996)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jiang, M. et al. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 98, 218–223 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Fukushige, T. et al. MEC-12, an α-tubulin required for touch sensitivity in C. elegans. J. Cell Sci. 112, 395–403 (1999)

    CAS  PubMed  Google Scholar 

  11. Xue, D., Tu, Y. & Chalfie, M. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 261, 1324–1328 (1993)

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Duggan, A., Ma, C. & Chalfie, M. Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125, 4107–4119 (1998)

    CAS  PubMed  Google Scholar 

  13. Van Helden, J., Andre, B. & Collado-Vides, J. A website for the computational analysis of yeast regulatory sequences. Yeast 16, 177–187 (2000)

    Article  CAS  PubMed  Google Scholar 

  14. Blumenthal, T. et al. A global analysis of Caenorhabditis elegans operons. Nature 417, 851–854 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Huang, M. & Chalfie, M. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 367, 467–470 (1994)

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Barnes, T. M., Jin, Y., Horvitz, H. R., Ruvkun, G. & Hekimi, S. The Caenorhabditis elegans behavioural gene unc-24 encodes a novel bipartite protein similar to both erythrocyte band 7.2 (stomatin) and nonspecific lipid transfer protein. J. Neurochem. 67, 46–57 (1996)

    Article  CAS  PubMed  Google Scholar 

  17. Treinin, M. & Chalfie, M. A mutated acetylcholine receptor subunit causes neuronal degeneration in C. elegans. Neuron 14, 871–877 (1995)

    Article  CAS  PubMed  Google Scholar 

  18. Treinin, M., Gillo, B., Liebman, L. & Chalfie, M. Two functionally dependent acetylcholine subunits are encoded in a single Caenorhabditis elegans operon. Proc. Natl Acad. Sci. USA 95, 15492–15495 (1998)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  19. Rubin, G. M. et al. Comparative genomics of the eukaryotes. Science 287, 2204–2215 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chalfie, M. & Thomson, J. N. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J. Cell Biol. 93, 15–23 (1982)

    Article  CAS  PubMed  Google Scholar 

  21. Liang, P. & MacRae, T. H. Molecular chaperones and the cytoskeleton. J. Cell Sci. 110, 1431–1440 (1997)

    CAS  PubMed  Google Scholar 

  22. Lockhart, D. J. & Winzeler, E. A. Genomics, gene expression and DNA arrays. Nature 405, 827–836 (2000)

    Article  CAS  PubMed  Google Scholar 

  23. Reinke, V. et al. A global profile of germline gene expression in C. elegans. Mol. Cell. 6, 605–616 (2000)

    Article  CAS  PubMed  Google Scholar 

  24. Hill, A. A., Hunter, C. P., Tsung, B. T., Tucker-Kellogg, G. & Brown, E. L. Genomic analysis of gene expression in C. elegans. Science 290, 809–812 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Eberwine, J. et al. Analysis of gene expression in single live neurons. Proc. Natl Acad. Sci. USA 89, 3010–3014 (1992)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, E45–E45 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bailey, T. L. & Elkan, C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28–36 (1994)

    CAS  PubMed  Google Scholar 

  28. Mello, C. C., Kramer, J. M., Stinchcomb, D. & Ambros, V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959–3970 (1991)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Huang, L. S., Tzou, P. & Sternberg, P. W. The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. Mol. Biol. Cell 5, 395–411 (1994)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Han, M. & Sternberg, P. W. Analysis of dominant-negative mutations of the Caenorhabditis elegans let-60 ras gene. Genes Dev. 5, 2188–2198 (1991)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank X. Chen for help with analysis of the microarray data; M. Goodman for constructing the integrated mec-18::gfp strain; B. Tycko for the LightCycler; and E. Schwarz, J. Wang and J. Eberwine for discussion. This work was supported by a grant from the National Center for Research Resources to S.K.K. and a grant from the National Institutes of Health to M.C.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Chalfie.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Y., Ma, C., Delohery, T. et al. Identification of genes expressed in C. elegans touch receptor neurons. Nature 418, 331–335 (2002). https://doi.org/10.1038/nature00891

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature00891

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing