C. elegans exhibits complex experience-dependent thermosensory behaviors on spatial thermal gradients. AFD has been identified as the major thermosensory neuron type, and AFD-ablated worms exhibit strong defects in thermotaxis behaviors. Measurements of temperature-evoked intracellular calcium dynamics and thermoreceptor current have shown that AFD responds to thermal variation at temperatures above a threshold temperature (T*) that is set by the animal’s cultivation temperature (Tc). Thermotransduction in AFD is mediated by cGMP signaling, and requires the functions of the receptor guanylyl cyclases (rGCs), GCY-8, GCY-18 and GCY-23, the cGMP-dependent phosphodiesterase PDE-2, and the TAX-2 and TAX-4 cGMP-gated channels. However, the molecular mechanisms by which AFD senses temperature are still unknown.
Previous studies have shown that many rGCs function as sensors for specific stimuli, suggesting that the AFD-expressed rGCs may themselves act as thermosensors. We found that misexpression of GCY-8, GCY-18 and GCY-23 in the non-thermosensory AWB and ASE chemosensory neurons is sufficient to confer warming-dependent changes in intracellular calcium (also see abstract by Yu, Takeishi et al). We further expressed each rGC singly or in combination in these neurons, and found that expression of GCY-23 alone confers temperature responses onto AWB and ASE in the physiological temperature range, whereas expression of GCY-18 confers responses to higher temperatures. Interestingly, in contrast to AFD, the T* of AWB and ASE misexpressing AFD-specific rGCs is not modulated by Tc, suggesting that the observed Tc -dependent plasticity in AFD thermosensory response threshold may be mediated by AFD-specific mechanisms. To ask whether misexpression in cell types lacking endogenous cGMP signaling pathways would also confer thermosensory responses, we next misexpressed the rGCs in vulval muscles. We found that vulval muscles misexpressing GCY-23 as well as TAX-2/TAX-4 also exhibit responses to temperature variation. Our results suggest that AFD-specific rGCs can confer thermosensory responses onto multiple neuronal and non-neuronal cell types, and raise the possibility that these proteins may be bona fide thermosensors in C. elegans.
* - equal contributions.
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