Abstract
Caenorhabditis elegans senses at least five attractive odours with a single pair of olfactory neurons, AWC, but can distinguish among these odours in behavioural assays1. The two AWC neurons are structurally and functionally similar, but the G-protein-coupled receptor STR-2 is randomly expressed in either the left or the right AWC neuron, never in both2. Here we describe the isolation of a mutant, ky542, with specific defects in odour discrimination and odour chemotaxis. ky542 is an allele of nsy-1, a neuronal symmetry, or Nsy, mutant in which STR-2 is expressed in both AWC neurons2. Other Nsy mutants exhibit discrimination and olfactory defects like those of nsy-1 mutants. Laser ablation of the AWC neuron that does not express STR-2 (AWCOFF) recapitulates the behavioural phenotype of Nsy mutants, whereas laser ablation of the STR-2-expressing AWC neuron (AWCON) causes different chemotaxis defects. We propose that odour discrimination can be achieved by segregating the detection of different odours into distinct olfactory neurons or into unique combinations of olfactory neurons.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bargmann, C. I., Hartwieg, E. & Horvitz, H. R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74, 515–527 (1993).
Troemel, E. R., Sagasti, A. & Bargmann, C. I. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99, 387–398 (1999).
Sengupta, P., Chou, J. H. & Bargmann, C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899–909 (1996).
Troemel, E. R., Chou, J. H., Dwyer, N. D., Colbert, H. A. & Bargmann, C. I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83, 207–218 (1995).
Troemel, E. R. Chemosensory Receptors in Caenorhabditis elegans. Ph.D. Thesis, Univ. California (1999).
L’Etoile, N. D. & Bargmann, C. I. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron 25, 575–586 (2000).
Komatsu, H., Mori, I., Rhee, J.-S., Akaike, N. & Ohshima, Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707–718 (1996).
Coburn, C. M. & Bargmann, C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695–706 (1996).
Roayaie, K., Crump, J. G., Sagasti, A. & Bargmann, C. I. The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20, 55–67 (1998).
Birnby, D. A., Link, E. M., Vowels, J. J., Tian, H., Colacurcio, P. L. & Thomas, J. H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155, 85–104 (2000).
Chou, J. H., Bargmann, C. I. & Sengupta, P. The Caenorhabditis elegans odr-2 gene encodes a novel Ly-6-related protein required for olfaction. Genetics 157, 211–224 (2001).
Weinshenker, D., Wei, A., Salkoff, L. & Thomas, J. H. Block of an ether-a-go-go-like K+ channel by imipramine rescues egl-2 excitation defects in Caenorhabditis elegans. J. Neurosci. 19, 9831–9840 (1999).
Sengupta, P., Colbert, H. A. & Bargmann, C. I. The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79, 971–980 (1994).
Pierce-Shimomura, J. T., Faumont, S., Gaston, M. R., Pearson, B. J. & Lockery, S. R. The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature 410, 694–698 (2001).
Troemel, E. R., Kimmel, B. E. & Bargmann, C. I. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91, 161–169 (1997).
Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
Bargmann, C. I. & Horvitz, H. R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729–742 (1991).
Acknowledgements
We thank A. Sagasti and N. L'Etoile for for discussions and insights into AWC asymmetry; H. Nguyen for technical assistance; S. Wicks and R. Plasterk for sharing unpublished data; C. Adler and S. Kirch for advice on microscopy; and A. Sagasti, S. Shaham, N. L’Etoile, J. Gray and C. Adler for comments on the manuscript. P.D.W. was supported by a postdoctoral fellowship from the Jane Coffin Childs Memorial Fund for Medical Research. C.I.B. is an Investigator of the Howard Hughes Medical Institute. This work was supported by a grant from the National Institutes of Health.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wes, P., Bargmann, C. C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410, 698–701 (2001). https://doi.org/10.1038/35070581
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/35070581
This article is cited by
-
Investigation into the communication between unheated and heat-stressed Caenorhabditis elegans via volatile stress signals
Scientific Reports (2023)
-
Dissecting the genetic landscape of GPCR signaling through phenotypic profiling in C. elegans
Nature Communications (2023)
-
Neuropeptidergic regulation of compulsive ethanol seeking in C. elegans
Scientific Reports (2022)
-
Serotonin and dopamine modulate aging in response to food odor and availability
Nature Communications (2022)
-
Lessons from behavioral lateralization in olfaction
Brain Structure and Function (2022)
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.