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The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans

Nature volume 410, pages 694–698 (2001)Cite this article

An Erratum 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 nematode Caenorhabditis 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 genes gcy-6 and gcy-7, whereas ASER expresses gcy-5 (ref. 4). In addition, only ASEL expresses the homeobox gene lim-6, an orthologue of the human LMX1 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 that lim-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-type C. 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 in lim-6 mutants.

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Acknowledgements

We thank C. Bargmann and P. Wes for discussions and sharing unpublished data; O. Hobert for suggesting study of the lim-6 mutant; J. H. Thomas for technical instruction; O. Hobert, D. Garbers and The C. elegans Genetics Center for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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Pierce-Shimomura, J., Faumont, S., Gaston, M. et al. The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature 410, 694–698 (2001). https://doi.org/10.1038/35070575

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