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The homeobox genelim-6 is required for distinct chemosensory representations inC. elegans

Naturevolume 410, pages694–698 (2001)Cite this article

AnErratum to this article was published on 01 August 2001

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Abstract

The ability to discriminate between different chemical stimuli is crucial for food detection, spatial orientation and other adaptive behaviours in animals. In the nematodeCaenorhabditis elegans, spatial orientation in gradients of soluble chemoattractants (chemotaxis) is controlled mainly by a single pair of chemosensory neurons1. These two neurons, ASEL and ASER, are left–right homologues in terms of the disposition of their somata and processes, morphology of specialized sensory endings, synaptic partners and expression profile of many genes2,3. However, recent gene-expression studies have revealed unexpected asymmetries between ASEL and ASER. ASEL expresses the putative receptor guanylyl cyclase genesgcy-6 andgcy-7, whereas ASER expressesgcy-5 (ref.4). In addition, only ASEL expresses the homeobox genelim-6, an orthologue of the humanLMX1 subfamily of homeobox genes5. Here we show, using laser ablation of neurons and whole-cell patch-clamp electrophysiology, that the asymmetries between ASEL and ASER extend to the functional level. ASEL is primarily sensitive to sodium, whereas ASER is primarily sensitive to chloride and potassium. Furthermore, we find thatlim-6 is required for this functional asymmetry and for the ability to distinguish sodium from chloride. Thus, a homeobox gene increases the representational capacity of the nervous system by establishing asymmetric functions in a bilaterally symmetrical neuron pair.

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Figure 1: Discrimination of sodium and chloride by wild-typeC. elegans.
Figure 2: Effect of ablations of ASEL and ASER on chemotaxis performance in chloride, sodium and potassium gradients.
Figure 3: Comparison of membrane currents in ASEL and ASER.
Figure 4: Discrimination of sodium and chloride inlim-6 mutants.

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References

  1. Bargmann, C. I. & Horvitz, H. R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals inC. elegans.Neuron7, 729–742 (1991).

    Article CAS  Google Scholar 

  2. Ward, S., Thompson, N., White, J. & Brenner, S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematodeCaenorhabditis elegans.J. Comp. Neurol.160, 313–338 (1975).

    Article CAS  Google Scholar 

  3. White, J., Southgate, E., Thompson, J. & Brenner, S. The structure of the nervous system of the nematodeCaenorhabditis elegans.Phil. Trans. R. Soc. Lond. B314, 1–340 (1986).

    Article ADS CAS  Google Scholar 

  4. Yu, S., Avery, L., Baude, E. & Garbers, D. L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors.Proc. Natl Acad. Sci. USA94, 3384–3387 (1997).

    Article ADS CAS  Google Scholar 

  5. Hobert, O., Tessmar, K. & Ruvkun, G. TheCaenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons.Development126, 1547–1562 (1999).

    CAS  Google Scholar 

  6. Pierce-Shimomura, J. T., Morse, T. M. & Lockery, S. R. The fundamental role of pirouettes inCaenorhabditis elegans chemotaxis.J. Neurosci.19, 9557–9569 (1999).

    Article CAS  Google Scholar 

  7. Ward, S. Chemotaxis by the nematodeCaenorhabditis elegans: identification of attractants and analysis of the response by use of mutants.Proc. Natl Acad. Sci. USA70, 817–821 (1973).

    Article ADS CAS  Google Scholar 

  8. Goodman, M. B., Hall, D. H., Avery, L. & Lockery, S. R. Active currents regulate sensitivity and dynamic range inC. elegans neurons.Neuron20, 763–772 (1998).

    Article CAS  Google Scholar 

  9. Troemel, E. R., Sagasti, A. & Bargmann, C. I. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression inC. elegans.Cell99, 387–398 (1999).

    Article CAS  Google Scholar 

  10. Bargmann, C. I., Thomas, J. H. & Horvitz, H. R. Chemosensory cell function in the behavior and development ofCaenorhabditis elegans.Cold Spring Harb. Symp. Quant. Biol.55, 529–538 (1990).

    Article CAS  Google Scholar 

  11. Bargmann, C. I. & Horvitz, H. R. Control of larval development by chemosensory neurons inCaenorhabditis elegans.Science251, 1243–1246 (1991).

    Article ADS CAS  Google Scholar 

  12. Kaplan, J. M. & Horvitz, H. R. A dual mechanosensory and chemosensory neuron inCaenorhabditis elegans.Proc. Natl Acad. Sci. USA90, 2227–2231 (1993).

    Article ADS CAS  Google Scholar 

  13. Dusenbery, D. B. Analysis of chemotaxis in the nematode by counter current separation.J. Exp. Zool.188, 41–47 (1974).

    Article CAS  Google Scholar 

  14. Bargmann, C. I., Hartwieg, E. & Horvitz, H. R. Odorant-selective genes and neurons mediate olfaction inC. elegans.Cell74, 515–527 (1993).

    Article CAS  Google Scholar 

  15. Wes, P. D. & Bargmann, C. I.C. elegans odour discrimination requires asymmetric diversity in olfactory neurons.Nature410, 698–701 (2001).

    Article ADS CAS  Google Scholar 

  16. Mori, K. & Yoshihara, Y. Molecular recognition and olfactory processing in the mammalian olfactory system.Prog. Neurobiol.45, 585–619 (1995).

    Article CAS  Google Scholar 

  17. Rubin, B. D. & Katz, L. C. Optical imaging of odorant representations in the mammalian olfactory bulb.Neuron23, 499–511 (1991).

    Article  Google Scholar 

  18. Bargmann, C. I. & Avery, L. Laser killing of cells inCaenorhabditis elegans.Methods Cell Biol.48, 225–250 (1995).

    Article CAS  Google Scholar 

  19. Sengupta, P., Chou, J. H. & Bargmann, C. I.odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl.Cell84, 899–909 (1996).

    Article CAS  Google Scholar 

  20. Lockery, S. R. & Goodman, M. B. Tight-seal whole-cell patch clamping ofC. elegans neurons.Methods Enzymol.295, 201–217 (1998).

    Article  Google Scholar 

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Acknowledgements

We thank C. Bargmann and P. Wes for discussions and sharing unpublished data; O. Hobert for suggesting study of thelim-6 mutant; J. H. Thomas for technical instruction; O. Hobert, D. Garbers and TheC. elegans Genetics Center for strains; M. Moravec and J. Cervantes for technical assistance; and J. Eisen, M. Goodman, T. Morse and M. Westerfield for discussion. This work was supported by the National Science Foundation; the National Institute of Mental Health; the National Heart, Lung, and Blood Institute; the Office of Naval Research; The Sloan Foundation; and The Searle Scholars Program.

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  1. Institute of Neuroscience, 1254 University of Oregon, Eugene, 97403, Oregon, USA

    Jonathan T. Pierce-Shimomura, Serge Faumont, Michelle R. Gaston, Bret J. Pearson & Shawn R. Lockery

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  1. Jonathan T. Pierce-Shimomura

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Pierce-Shimomura, J., Faumont, S., Gaston, M.et al. The homeobox genelim-6 is required for distinct chemosensory representations inC. elegans.Nature410, 694–698 (2001). https://doi.org/10.1038/35070575

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