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Transcriptomic profiling of sex-specific olfactory neurons reveals subset-specific receptor expression in C. elegans

Reilly, Douglas K. and Schwarz, Erich M. and Muirhead, Caroline S. and Robidoux, Annalise N. and Antoshechkin, Igor and Narayan, Anusha and Doma, Meenakshi K. and Sternberg, Paul W. and Srinivasan, Jagan (2021) Transcriptomic profiling of sex-specific olfactory neurons reveals subset-specific receptor expression in C. elegans. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20211102-173632613

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Abstract

The nematode Caenorhabditis elegans utilizes chemosensation to navigate an ever-changing environment for its survival. A class of secreted small-molecule pheromones, termed ascarosides, play an important role in olfactory perception by affecting a host of biological function ranging from development to behavior. The ascaroside ascr#8 mediates sex-specific behaviors, driving avoidance in hermaphrodites and attraction in males. Males sense ascr#8 via the ciliated male-specific cephalic sensory (CEM) neurons, which exhibit radial symmetry along dorsal-ventral and left-right axes. Calcium imaging studies suggest a complex neural coding mechanism that translates stochastic physiological responses in these neurons to reliable behavioral outputs. To test the hypothesis that the neurophysiological complexity arises from differential expression of genes within subsets of these neurons, we performed cell-specific transcriptomic profiling of these sensory neurons. Expression profiling revealed between 20 and 639 genes enriched at least two-fold per CEM neuron and identified multiple G protein coupled receptor (GPCR) candidates enriched in non-overlapping subsets of CEM neurons. GFP reporter analysis confirmed that RNA expression of two of the GPCR genes, srw-97 and dmsr-12, is enriched in specific subsets of the CEM neurons. Single CRISPR-Cas9 knockouts of either srw-97 or dmsr-12 resulted in partial defects, while a double knockout of both srw-97 and dmsr-12 completely abolished the attractive response to ascr#8, suggesting that each receptor acts in a non-redundant manner in discrete olfactory neurons. Together, our results suggest that the evolutionarily distinct GPCRs SRW-97 and DMSR-12 act to facilitate male-specific sensation of ascr#8 through discrete subsets of CEM neurons.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.10.26.465928DOIDiscussion Paper
ORCID:
AuthorORCID
Schwarz, Erich M.0000-0003-3151-4381
Antoshechkin, Igor0000-0002-9934-3040
Sternberg, Paul W.0000-0002-7699-0173
Srinivasan, Jagan0000-0001-5449-7938
Alternate Title:Male pheromone G protein-coupled receptors in C. elegans
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This version posted October 28, 2021. We thank the Caenorhabditis Genetics Center, which is funded by the NIH Office of Research Infrastructure Programs (P40 OD01044), as well as the National BioResource Project, L. Rene Garcia (Texas A&M University), and Douglas Portman (University of Rochester Medical Center) for providing strains. We also thank InVivo Biosystems for generating transgenic and CRISPR knockout animals. The synthetic ascr#8 utilized in this study was provided by Frank Schroeder (Cornell University). The research reported in this publication was supported by NIH R01 DC016058 (J.S.), R01 GM084389 (P.W.S.), the Howard Hughes Medical Institute (P.W.S.), Moore Foundation Grant No. 4551 (E.M.S.), and Cornell startup funding (E.M.S.). We thank Titus Brown and the Michigan State University High-Performance Computing Center (supported by U.S. Department of Agriculture grant 2010-65205-20361 and NIFA–National Science Foundation (NSF) grant IOS-0923812) for computational support; additional computing was enabled by start-up and research allocations from NSF XSEDE (TG-MCB180039 and TG-MCB190010). Data availability: RNA-seq reads will be submitted to the Sequence Read Archive (SRA; https://www.ncbi.nlm.nih.gov/sra). The authors have declared no competing interest.
Funders:
Funding AgencyGrant Number
NIHP40 OD010440
Texas A&M UniversityUNSPECIFIED
University of RochesterUNSPECIFIED
NIHR01 DC016058
NIHR01 GM084389
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore Foundation4551
Cornell UniversityUNSPECIFIED
Department of Agriculture2010-65205-20361
NSFIOS-0923812
NSFTG-MCB180039
NSFTG-MCB190010
Subject Keywords:C. elegans, Pheromone, Sex-specific, G Protein-Coupled Receptors, Transcriptomes, Single-Cell
DOI:10.1101/2021.10.26.465928
Record Number:CaltechAUTHORS:20211102-173632613
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211102-173632613
Official Citation:Transcriptomic profiling of sex-specific olfactory neurons reveals subset-specific receptor expression in C. elegans. Douglas K. Reilly, Erich M. Schwarz, Caroline S. Muirhead, Annalise N. Robidoux, Igor Antoshechkin, Anusha Narayan, Meenakshi K. Doma, Paul W. Sternberg, Jagan Srinivasan. bioRxiv 2021.10.26.465928; doi: https://doi.org/10.1101/2021.10.26.465928
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:111706
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:02 Nov 2021 21:36
Last Modified:02 Nov 2021 21:36

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