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cGMP-dependent pathway and a GPCR kinase are required for photoresponse in the nematode Pristionchus pacificus.

Kenichi Nakayama | Hirokuni Hiraga | Aya Manabe | Takahiro Chihara | Misako Okumura
PLoS genetics | 2024

Light 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 nematode Caenorhabditis elegans, the unique photoreceptor protein Cel-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 nematode Pristionchus pacificus, which was established as a satellite model organism for comparison with C. elegans. Similar to C. elegans, illumination with short-wavelength light induces avoidance behavior in P. pacificus. Opsin, cryptochrome/photolyase, and lite-1 were not detected in the P. pacificus genome using orthology and domain prediction-based analyses. To identify the genes related to phototransduction in P. pacificus, we conducted forward genetic screening for light-avoidance behavior and isolated five light-unresponsive mutants. Whole-genome sequencing and genetic mapping revealed that the cGMP-dependent pathway and Ppa-grk-2, which encodes a G protein-coupled receptor kinase (GRK) are required for light avoidance. Although the cGMP-dependent pathway is conserved in C. elegans phototransduction, GRK is not necessary for light avoidance in C. elegans. This suggests similarities and differences in light-sensing mechanisms between the two species. Using a reverse genetic approach, we showed that gamma-aminobutyric acid (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.

Pubmed ID: 39541254

Associated grants

None

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Fiji (tool)

RRID:SCR_002285

Software package as distribution of ImageJ and ImageJ2 together with Java, Java3D and plugins organized into coherent menu structure. Used to assist research in life sciences.

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Pristionchus.org (tool)

RRID:SCR_003414

This data resource is a genetic, molecular, and genomic toolkit that establishes one particular species, Pristionchus pacificus, as a major satellite system for evolutionary developmental biology. Users may download Pristionchus Sequences and use the Pristionchus pacificus genome browser where they may find gene or gene prediction data. Users can also use the BLAST feature, which allows users to search the assembly for position information of bacs, reads and contigs using the mapping tool. The center of the site's research is the evolutionary analysis of vulva formation. The general aim of the Department is to develop the nematode vulva as a suitable case study into the evolutionary alterations of developmental processes. By studying and comparing two distantly related species of the same phylum, such as P. pacificus and C. elegans, macroevolutionary alterations of developmental processes and mechanisms can be identified. The final goal of the Department is to achieve a comprehensive description of macro- and microevolutionary changes of developmental mechanisms at the molecular level in a phylogenetic and ecological context.

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RRID:SCR_004726

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RRID:SCR_005375

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RRID:SCR_005829

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RRID:SCR_006549

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RRID:SCR_011811

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RRID:SCR_011822

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RRID:SCR_017118

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RRID:SCR_019214

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