The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila

Abstract

Animals rely on highly sensitive thermoreceptors to seek out optimal temperatures, but the molecular mechanisms of thermosensing are not well understood. The Dorsal Organ Cool Cells (DOCCs) of the Drosophila larva are a set of exceptionally thermosensitive neurons critical for larval cool avoidance. Here, we show that DOCC cool-sensing is mediated by Ionotropic Receptors (IRs), a family of sensory receptors widely studied in invertebrate chemical sensing. We find that two IRs, IR21a and IR25a, are required to mediate DOCC responses to cooling and are required for cool avoidance behavior. Furthermore, we find that ectopic expression of IR21a can confer cool-responsiveness in an Ir25a-dependent manner, suggesting an instructive role for IR21a in thermosensing. Together, these data show that IR family receptors can function together to mediate thermosensation of exquisite sensitivity.

DOI: http://dx.doi.org/10.7554/eLife.13254.001

eLife digest

Animals need to be able to sense temperatures for a number of reasons. For example, this ability allows animals to avoid conditions that are either too hot or too cold, and to maintain an optimal body temperature. Most animals detect temperature via nerve cells called thermoreceptors. These sensors are often extremely sensitive and some can even detect changes in temperature of just a few thousandths of a degree per second. However, it is not clear how thermoreceptors detect temperature with such sensitivity, and many of the key molecules involved in this ability are unknown.

In 2015, researchers discovered a class of highly sensitive nerve cells that allow fruit fly larvae to navigate away from unfavorably cool temperatures. Now, Ni, Klein et al. – who include some of the researchers involved in the 2015 work – have determined that these nerves use a combination of two receptors to detect cooling. Unexpectedly, these two receptors – Ionotropic Receptors called IR21a and IR25a – had previously been implicated in the detection of chemicals rather than temperature. IR25a was well-known to combine with other related receptors to detect an array of tastes and smells, while IR21a was thought to act in a similar way but had not been associated with detecting any specific chemicals. These findings demonstrate that the combination of IR21a and IR25a detects temperature instead.

Together, these findings reveal a new molecular mechanism that underlies an animal’s ability to sense temperature. These findings also raise the possibility that other “orphan” Ionotropic Receptors, which have not been shown to detect any specific chemicals, might actually contribute to sensing temperature instead. Further work will explore this possibility and attempt to uncover precisely how IR21a and IR25a work to detect cool temperatures.

DOI: http://dx.doi.org/10.7554/eLife.13254.002