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Signaling by AWC Olfactory Neurons Is Necessary for Caenorhabditis elegans' Response to Prenol, an Odor Associated with Nematode-Infected Insects

Baiocchi, Tiffany and Anesko, Kyle and Mercado, Nathan and Park, Heenam and Kin, Kassandra and Strickhouser-Monzon, Brandon and Robles, Priscila and Bowman, Christian and Wang, Han and Sternberg, Paul W. and Dillman, Adler R. (2020) Signaling by AWC Olfactory Neurons Is Necessary for Caenorhabditis elegans' Response to Prenol, an Odor Associated with Nematode-Infected Insects. Genetics, 216 (1). pp. 145-157. ISSN 0016-6731. PMCID PMC7463287. https://resolver.caltech.edu/CaltechAUTHORS:20200727-090420630

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Abstract

Chemosensation plays a role in the behaviors and life cycles of numerous organisms, including nematodes. Many guilds of nematodes exist, ranging from the free-living Caenorhabditis elegans to various parasitic species such as entomopathogenic nematodes (EPNs), which are parasites of insects. Despite ecological differences, previous research has shown that both EPNs and C. elegans respond to prenol (3-methyl-2-buten-1-ol), an odor associated with EPN infections. However, it is unclear how C. elegans responds to prenol. By utilizing natural variation and genetic neuron ablation to investigate the response of C. elegans to prenol, we found that the AWC neurons are involved in the detection of prenol and that several genes (including dcap-1, dcap-2, and clec-39) influence response to this odorant. Furthermore, we identified that the response to prenol is mediated by the canonically proposed pathway required for other AWC-sensed attractants. However, upon testing genetically diverse isolates, we found that the response of some strains to prenol differed from their response to isoamyl alcohol, suggesting that the pathways mediating response to these two odorants may be genetically distinct. Further, evaluations leveraging natural variation and genome wide association revealed specific genes that influence nematode behavior and provide a foundation for future studies to better understand the role of prenol in nematode behavioral ecology.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1534/genetics.120.303280DOIArticle
https://doi.org/10.25386/genetics.12616691DOISupplementary Material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7463287PubMed CentralArticle
ORCID:
AuthorORCID
Sternberg, Paul W.0000-0002-7699-0173
Dillman, Adler R.0000-0001-7171-4332
Additional Information:© 2020 Baiocchi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Available freely online through the author-supported open access option. Manuscript received April 21, 2020; accepted for publication July 14, 2020; published Early Online July 17, 2020. We thank the C. elegans Natural Diversity Resource (CeNDR) for providing the natural variants used in this study as well as the C. elegans Genetics Center, which is funded by National Institutes of Health Office of Research Infrastructure Programs (P40 OD010440); the Mitani Laboratory at the Tokyo Women’s Medical University School of Medicine; and the providers of (lf) mutants from a variety of laboratory (which have been listed in Table S21; resources summary), including the C. elegans gene knockout project at the Oklahoma Medical Research foundation, which is part of the international C. elegans gene knockout consortium and created a large number of the (lf) mutants used in this study. This research was supported by the US Department of Agriculture National Institute of Food and Agriculture Hatch project (accession no. 1011296) to A.R.D., K99 GM126137/National Institute of General Medical Sciences to H.W., R24 OD023041/Office of the Director/National Institutes of Health to P.W.S., and the Graduate Research Mentorship Project from University of California Riverside, which provided support to T.B. Author contributions: T.B. and A.R.D. conceived and designed the behavioral experiments. M.C, K.K., B.S-M, K.A., P.R., and C.B performed behavioral experiments. H.W., H.P., and P.W.S. created CRISPR/Cas9-mediated knockout strains and generated dcap-2 rescue lines for use in behavioral experiments and provided information for the methods on creation of knockout strains, as well as feedback and suggestions for manuscript edits. T.B. and A.R.D. analyzed and interpreted behavioral data. T.B. and A.R.D. wrote and revised the manuscript. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
NIHP40 OD010440
Tokyo Women’s Medical University School of MedicineUNSPECIFIED
Oklahoma Medical Research FoundationUNSPECIFIED
Department of Agriculture1011296
NIHK99 GM126137
NIHR24 OD023041
University of California, RiversideUNSPECIFIED
Subject Keywords:prenol, 3-methyl-2-buten-1-ol, dcap-1, dcap-2, and clec-39
Issue or Number:1
PubMed Central ID:PMC7463287
Record Number:CaltechAUTHORS:20200727-090420630
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200727-090420630
Official Citation:Signaling by AWC Olfactory Neurons Is Necessary for Caenorhabditis elegans’ Response to Prenol, an Odor Associated with Nematode-Infected Insects. Tiffany Baiocchi, Kyle Anesko, Nathan Mercado, Heenam Park, Kassandra Kin, Brandon Strickhouser-Monzon, Priscila Robles, Christian Bowman, Han Wang, Paul W. Sternberg and Adler R. Dillman. GENETICS September 1, 2020 vol. 216 no. 1 145-157; https://doi.org/10.1534/genetics.120.303280
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104582
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:27 Jul 2020 16:59
Last Modified:15 Sep 2020 17:50

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