cGMP-dependent pathway and a GPCR kinase are required for photoresponse in the nematodePristionchus pacificus

Abstract

AbstractLight sensing is a critical function in most organisms and is mediated by photoreceptor proteins and phototransduction. Although most nematodes lack eyes, some species exhibit phototaxis. In the nematodeCaenorhabditis elegans, the unique photoreceptor proteinCel-LITE-1, its downstream G proteins, and cyclic GMP (cGMP)-dependent pathways are required for phototransduction. However, the mechanism of light-sensing in other nematodes remains unknown. To address this question, we used the nematodePristionchus pacificus, which was established as a satellite model organism for comparison withC. elegans. Similar toC. elegans, illumination with short-wavelength light induces avoidance behavior inP. pacificus. Opsin, cryptochrome/photolyase, andlite-1were not detected in theP. pacificusgenome using orthology and domain prediction-based analyses. To identify the genes related to phototransduction inP. pacificus, we conducted forward genetic screening for light-avoidance behavior and isolated four light-unresponsive mutants. Whole-genome sequencing and genetic mapping revealed that the cGMP-dependent pathway andPpa-grk-2, which encodes a G protein-coupled receptor kinase (GRK) are required for light avoidance. Although the cGMP-dependent pathway is conserved inC. elegansphototransduction, GRK is not necessary for light avoidance inC. elegans. This suggests similarities and differences in light-sensing mechanisms between the two species. Using a reverse genetics approach, we showed that GABA and glutamate were involved in light avoidance. Through reporter analysis and suppression of synapse transmission, we identified candidate photosensory neurons. These findings advance our understanding of the diversity of phototransduction in nematodes even in the absence of eyes.Author summaryNematodes are a highly diverse group of animals found in a wide variety of habitats and sensory systems. In particular, light-induced behavior has been found to differ among species. The photoreceptor and its downstream pathways inCaenorhabditis eleganshave been identified, revealing unique and distinct characteristics compared to those in other animals. However, the mechanisms of photoreception in other nematodes remain largely unknown. This study focused on the analysis of the photoreception mechanisms inPristionchus pacificus, a species for which many genetic and molecular tools are available. Similar toC. elegans,P. pacificusalso exhibits light avoidance behavior towards short-wavelength light; however, known animal photoreceptor genes could not be identified in theP. pacificusgenome using bioinformatic approaches. Using forward and reverse genetic approaches, we found that certain genes and neurons are required for light avoidance, some of which are conserved inC. elegansphotoreception. These results suggest that the light-sensing mechanisms ofC. elegansandP. pacificusare similar, yet there are differences between the two species. These findings highlight the various light-sensing mechanisms in nematodes.