The planarian TRPA1 homolog mediates extraocular behavioral responses to near-ultraviolet light.

Taylor R Birkholz,Wendy S Beane

doi:10.1242/jeb.152298

Taylor R Birkholz, Wendy S Beane

Open Access

https://doi.org/10.1242/jeb.152298

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Abstract

ABSTRACTAlthough light is most commonly thought of as a visual cue, many animals possess mechanisms to detect light outside of the eye for various functions, including predator avoidance, circadian rhythms, phototaxis and migration. Here we confirm that planarians (like Caenorhabditis elegans, leeches and Drosophila larvae) are capable of detecting and responding to light using extraocular photoreception. We found that, when either eyeless or decapitated worms were exposed to near-ultraviolet (near-UV) light, intense wild-type photophobic behaviors were still observed. Our data also revealed that behavioral responses to green wavelengths were mediated by ocular mechanisms, whereas near-UV responses were driven by extraocular mechanisms. As part of a candidate screen to uncover the genetic basis of extraocular photoreception in the planarian species Schmidtea mediterranea, we identified a potential role for a homolog of the transient receptor potential channel A1 (TRPA1) in mediating behavioral responses to extraocular light cues. RNA interference (RNAi) to Smed-TrpA resulted in worms that lacked extraocular photophobic responses to near-UV light, a mechanism previously only identified in Drosophila. These data show that the planarian TRPA1 homolog is required for planarian extraocular-light avoidance and may represent a potential ancestral function of this gene. TRPA1 is an evolutionarily conserved detector of temperature and chemical irritants, including reactive oxygen species that are byproducts of UV-light exposure. Our results suggest that planarians possess extraocular photoreception and display an unconventional TRPA1-mediated photophobic response to near-UV light.

Highlights

The ability to detect and respond to light is a fundamental characteristic of living organisms
Our results support the hypothesis that planarians are capable of extraocular photoreception and that light detection occurs along the entire body
We found that extraocular exposure to either red or green wavelengths did not elicit photophobic responses, unlike the significant tail thinning that was observed when planarians were exposed to near-UV light

Summary

Introduction

The ability to detect and respond to light is a fundamental characteristic of living organisms. Ocular photoreception (or vision) is what is most commonly associated with light detection and image formation, an ability that requires central nervous system processing from cells found in the eye organ. Many animals have the ability to detect light using light-sensitive structures outside of the eye.

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