Editors' ChoiceOlfaction

Optimizing Population Dispersal

Sci. Signal.  28 Sep 2010:
Vol. 3, Issue 141, pp. ec297
DOI: 10.1126/scisignal.3141ec297

Nematodes show positive chemotaxis toward odorants that indicate food, such as benzaldehyde, but failure to reach food after prolonged exposure induces dispersal from the odorant, a phenomenon called olfactory plasticity. Dauer pheromone, which is a mixture of sugar derivatives secreted by all worms, is an environmental cue that indicates population density and influences developmental decisions; high concentrations of pheromones induce worms to develop as dauer larvae, which are nonreproductive and resistant to starvation. Yamada et al. noted that the strength of olfactory plasticity in Caenorhabditis elegans positively correlated with the number of animals in the population and that pheromone biosynthesis–defective daf-22 mutants showed reduced olfactory plasticity, a phenotype that was reversed by treating the animals with purified pheromones. A genetic screen identified nep-2, which encodes a homolog of the mammalian metalloprotease neprilysin, as required in the nervous system for olfactory plasticity in benzaldehyde-induced chemotaxis, suggesting that degradation of a peptide signal was required for olfactory plasticity. The authors identified the putative neuropeptide precursor suppressor of nep-2 (SNET-1) in a secondary screen for mutations that suppressed the nep-2 phenotype. Expression of snet-1 in several sensory and interneurons increased in daf-22 mutants as compared with wild type (WT), suggesting that sensory input regulated snet-1 expression. Importantly, snet-1 was not expressed in the ASI sensory neurons in WT but was expressed in these neurons in daf-22 mutants. ASI neurons regulate dauer formation, and the addition of dauer pheromone to the culture rescued the ectopic expression phenotype. A null mutation in snet-1 restored olfactory plasticity in daf-22 mutants. These results suggest that SNET-1 is a secreted neuropeptide that negatively regulates olfactory plasticity, is down-regulated by dauer pheromone, and is degraded by NEP-2. This model provides a mechanism whereby high population density enhances olfactory plasticity to induce dispersal of animals.

K. Yamada, T. Hirotsu, M. Matsuki, R. A. Butcher, M. Tomioka, T. Ishihara, J. Clardy, H. Kunitomo, Y. Iino, Olfactory plasticity is regulated by pheromonal signaling in Caenorhabditis elegans. Science 329, 1647–1650 (2010). [Abstract] [Full Text]