A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure.
The tax-2 and tax-4 genes of C. elegans encode two subunits of a cyclic nucleotide-gated channel that is required for chemosensation, thermosensation and normal axon outgrowth of some sensory neurons. Here we show that, in tax-2 and tax-4 mutants, young larvae have superficially normal axons, but axon outgrowth resumes in inappropriate regions in late larval stages. Using a temperature-sensitive mutation in tax-2, we find that tax-2 activity is required during the adult stage to preserve normal axon morphology. These results indicate that tax-2 and tax-4 are required for the maintenance of correct axon structure, and reveal an unexpected plasticity that allows C. elegans axons to be remodeled long after their initial connections have been established. TAX-2 and TAX-4 have been proposed to form a transduction channel for chemosensation and thermosensation, and tax-2 activity is required in the adult stage for normal chemotaxis to NaCl and odorants. Animals mutant for the daf-11 gene have axon phenotypes that are similar to those of tax-2 and tax 4 mutants; this axon phenotype also has a late time of action. daf-11 regulates a developmental process called dauer larva formation that is controlled by sensory stimuli, and tax-2 and tax-4 can either stimulate or inhibit dauer larva formation in different contexts.
Coburn
C M
CM
Howard Hughes Medical Institute, Program in Developmental Biology, Department of Anatomy, The University of California, San Francisco 94143-0452, USA.
Mori
I
I
Ohshima
Y
Y
Bargmann
C I
CI
D000818:Animals; D001369:Axons / Q000502:physiology*; D017173:Caenorhabditis elegans / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins; D002633:Chemotaxis; D017238:Genes, Helminth / Q000502:physiology; D007473:Ion Channels / Q000235:genetics / Q000502:physiology*; D007814:Larva; D009154:Mutation; D009475:Neurons, Afferent / Q000502:physiology*; D009712:Nucleotides, Cyclic / Q000502:physiology; D009812:Odorants; D011993:Recombinant Fusion Proteins; D012965:Sodium Chloride / Q000494:pharmacology; D013696:Temperature
D029742:Caenorhabditis elegans Proteins; D007473:Ion Channels; D009712:Nucleotides, Cyclic; D011993:Recombinant Fusion Proteins; C102183:tax-2 protein, C elegans; C102184:tax-4 protein, C elegans; D012965:Sodium Chloride