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Published online 21 February 2006. doi:10.1083/jcb.200509115
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 172, Number 5, 663-669
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 Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans

James E. Evans1, Joshua J. Snow1, Amy L. Gunnarson1, Guangshuo Ou1, Henning Stahlberg1, Kent L. McDonald2, and Jonathan M. Scholey1

1 Section of Molecular and Cellular Biology, University of California, Davis, Davis, CA 95616
2 Electron Microscopy Laboratory, University of California, Berkeley, Berkeley, CA 94720

Correspondence to Jonathan M. Scholey: jmscholey{at}ucdavis.edu


Abstract
The diversity of sensory cilia on Caenorhabditis elegans neurons allows the animal to detect a variety of sensory stimuli. Sensory cilia are assembled by intraflagellar transport (IFT) kinesins, which transport ciliary precursors, bound to IFT particles, along the ciliary axoneme for incorporation into ciliary structures. Using fluorescence microscopy of living animals and serial section electron microscopy of high pressure–frozen, freeze-substituted IFT motor mutants, we found that two IFT kinesins, homodimeric OSM-3 kinesin and heterotrimeric kinesin II, function in a partially redundant manner to build full-length amphid channel cilia but are completely redundant for building full-length amphid wing (AWC) cilia. This difference reflects cilia-specific differences in OSM-3 activity, which serves to extend distal singlets in channel cilia but not in AWC cilia, which lack such singlets. Moreover, AWC-specific chemotaxis assays reveal novel sensory functions for kinesin II in these wing cilia. We propose that kinesin II is a "canonical" IFT motor, whereas OSM-3 is an "accessory" IFT motor, and that subtle changes in the deployment or actions of these IFT kinesins can contribute to differences in cilia morphology, cilia function, and sensory perception.

Abbreviations used in this paper: 3D, three-dimensional; AWC, amphid wing; IFT, intraflagellar transport; MT, microtubule; RFP, red fluorescent protein; TEM, transmission EM; WT, wild type.


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