Abstract
The sensory systems of multicellular organisms are designed to provide information about the environment and thus elicit appropriate changes in physiology and behavior. In the nematode Caenorhabditis elegans, sensory neurons affect the decision to arrest during development in a diapause state, the dauer larva, and modulate the lifespan of the animals in adulthood. However, the mechanisms underlying these effects are incompletely understood. Using whole-genome microarray analysis, we identified transcripts whose levels are altered by mutations in the intraflagellar transport protein daf-10, which result in impaired development and function of many sensory neurons in C. elegans. In agreement with existing genetic data, the expression of genes regulated by the transcription factor DAF-16/FOXO was affected by daf-10 mutations. In addition, we found altered expression of transcriptional targets of the DAF-12/nuclear hormone receptor in the daf-10 mutants and showed that this pathway influences specifically the dauer formation phenotype of these animals. Unexpectedly, pathogen-responsive genes were repressed in daf-10 mutant animals, and these sensory mutants exhibited altered susceptibility to and behavioral avoidance of bacterial pathogens. Moreover, we found that a solute transporter gene mct-1/2, which was induced by daf-10 mutations, was necessary and sufficient for longevity. Thus, sensory input seems to influence an extensive transcriptional network that modulates basic biological processes in C. elegans. This situation is reminiscent of the complex regulation of physiology by the mammalian hypothalamus, which also receives innervations from sensory systems, most notably the visual and olfactory systems.
Highlights
IntroductionBehavioral responses as well as physiological processes such as energy homeostasis, development and immune homeostasis need to be modulated depending on the environmental situation
Organisms are constantly interacting with their environment
In daf-10 mutant animals we find evidence of activation of DAF-16/FOXO, as expected, as well as activation of the nuclear hormone receptor (NHR) DAF-12, which we demonstrate is required for the increased dauer formation, but not for the extended longevity of sensory mutant animals
Summary
Behavioral responses as well as physiological processes such as energy homeostasis, development and immune homeostasis need to be modulated depending on the environmental situation. An animal’s feeding and development are crucial to survival in general, but may need to be reduced or delayed under certain environmental conditions to allow efficient allocation of resources for survival. To achieve such modulation, animals have developed complex sensory systems that acquire and integrate various sorts of information about their environment and their internal state. It is clear that the sensory system of C. elegans regulates physiological functions of the animals as well as its behavior.
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