Octopamine is a biogenic amine implicated in several invertebrate behaviors. Octopamine biosynthesis requires a tyrosine decarboxylase (TDC) to convert tyrosine to tyramine and a tyramine beta-hydroxylase (TBH) to convert tyramine to octopamine. We characterized a C. elegans tyrosine decarboxylase gene (
tdc-1 ) and a tyramine-beta-hydroxylase gene (
tbh-1 ). We showed that
tdc-1 deletion mutants lack tyramine and octopamine, whereas
tbh-1 deletion mutants lack only octopamine. This observation indicates that
tdc-1 is required for tyramine biosynthesis and that
tdc-1 and
tbh-1 are required for octopamine biosynthesis.
tdc-1 and
tbh-1 expression overlap in the RIC interneurons and the gonadal sheath cells.
tdc-1 , but not
tbh-1 , is expressed in the RIM motor neurons and four uterine cells. These expression patterns suggest that the RIC interneurons and gonadal sheath cells are octopaminergic and the RIM motor neurons and UV cells are tyraminergic.
tdc-1 mutants have several behavioral defects that are not shared by
tbh-1 mutants, suggesting a role for tyramine in the suppression of head oscillations upon anterior touch and in reversal behavior (Alkema et al . 14 IWM 2003).
tbh-1 and
tdc-1 mutants share several behavioral defects: they fail to properly inhibit egg laying and pharyngeal pumping in the absence of food and move more slowly than wild-type animals.
tbh-1 and
tdc-1 mutants are also hypersensitive to exogenous serotonin in assays of locomotion, pharyngeal pumping and egg laying. Our results indicate that endogenous octopamine inhibits pharyngeal pumping and egg laying and stimulates locomotion and thus acts antagonistically to serotonin in these behaviors. Mutations in
tdc-1 and
tbh-1 suppress the pharyngeal pumping defect but not the egg-laying defect of serotonin-deficient
tph-1 mutants. Food-deprived
tbh-1 and
tdc-1 mutants, much like food-deprived animals mutant for the serotonin-reuptake transporter MOD-5, become almost immobilized when they encounter a bacterial lawn.
tbh-1 deletions can suppress the resistance to exogenous serotonin in locomotion assays of animals mutant for the serotonin-gated chloride channel MOD-1. Furthermore,
mod-1 ;
tbh-1 double mutants display a hyperenhanced slowing response similar to that of the
tbh-1 single mutants. These data suggest that
tbh-1 acts downstream of or in parallel to
mod-1 in the modulation of locomotion.
mod-1 is expressed in a small number of motor neurons and interneurons, including the octopaminergic RIC neurons (Eric Miska, unpublished observation). This finding suggests that serotonin release can hyperpolarize the RIC interneurons and thereby inhibit octopamine signaling.