Non-classical roles for opsins in taste and smell

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Abstract The goal of the proposed project is to build on our recent discovery of non-classical roles for opsins in diverse sensory contexts, and specifically to unravel their contributions to the senses of taste and smell. It turns out that opsins, which have been studied for >100 years as light sensors, are expressed outside of the visual system and function in a variety of sensory modalities. Rather than serving exclusively in photosensation, we are finding that opsins are broadly required sensory receptors, potentially playing roles as far-ranging as TRP channels. In mammals, opsins are expressed in a large variety of extra-retinal cell types and organs. However, the extra-ocular roles of these opsins are essentially unexplored. We propose to bring to bear a wide combination of tools available for use in Drosophila to elucidate extra-retinal roles for opsins. The project will employ an extensive suite of in vivo approaches including electrophysiology and Ca2+ imaging, behavioral assays, cell biology and state-of-the art molecular genetic approaches, to study unconventional roles we found for opsins in gustation and olfaction. In addition to the six rhodopsins that are required in the visual system (Rh1-Rh6), flies encode a seventh family member (Rh7). Aim 1 will clarify a light-independent role for Rh7 in the response of gustatory receptor neurons (GRNs) to an aversive tastant. We will test the proposal that Rh7 couples to a signaling cascade that endows GRNs with high sensitivity to the aversive chemical. Aim 2 will investigate a potential role for an opsin in olfaction. Conceptually similar to our recent discovery that opsins expressed in thermosensory neurons allow flies to sense small increases in temperature in the comfortable range, we propose to test that an opsin acts in olfactory receptor neurons to detect minute concentrations of an aversive odorant through an amplification cascade. Aim 3 focuses on illuminating the potential roles of two opsins in the discrimination of foods on the basis of texture. The physical features of food include the viscosity of liquid foods, and the hardness of solid foods. However, the mechanisms underlying food texture sensation are poorly understood. We will investigate the contributions of two opsins to sensing the physical properties of foods. Temperature also influences food palatability. Aim 4 will address the concept that the temperature- dependent change in appeal of sugar-containing foods requires a member of the opsin family. In summary, the proposed project will deepen our understanding of light-independent roles of opsins in gustation and olfaction, and shape the proposal that opsins are broad, polymodal sensors. In view of the wide extra-ocular expression of mammalian opsins, we suggest that this project will provide the conceptual framework for exploring similar roles for opsins in mammals. Finally, taste and smell are critical for insect disease vectors to identify and bite human hosts, and thereby spread diseases that afflict over a billion people annually. Therefore, unraveling highly sensitive receptors for gustation and olfaction in insects has important potential for developing new strategies for interfering with the recognition and attraction of humans by insect disease vectors.