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Ascaroside Expression in Caenorhabditis elegans Is Strongly Dependent on Diet and Developmental Stage

Kaplan, Fatma and Srinivasan, Jagan and Mahanti, Parag and Ajredini, Ramadan and Durak, Omer and Nimalendran, Rathika and Sternberg, Paul W. and Teal, Peter E. A. and Schroeder, Frank C. and Edison, Arthur S. and Alborn, Hans T. (2011) Ascaroside Expression in Caenorhabditis elegans Is Strongly Dependent on Diet and Developmental Stage. PLoS ONE, 6 (3). Art. No. e17804. ISSN 1932-6203. PMCID PMC3058051. https://resolver.caltech.edu/CaltechAUTHORS:20110411-105726989

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Abstract

Background: The ascarosides form a family of small molecules that have been isolated from cultures of the nematode Caenorhabditis elegans. They are often referred to as “dauer pheromones” because most of them induce formation of long-lived and highly stress resistant dauer larvae. More recent studies have shown that ascarosides serve additional functions as social signals and mating pheromones. Thus, ascarosides have multiple functions. Until now, it has been generally assumed that ascarosides are constitutively expressed during nematode development. Methodology/Principal Findings: Cultures of C. elegans were developmentally synchronized on controlled diets. Ascarosides released into the media, as well as stored internally, were quantified by LC/MS. We found that ascaroside biosynthesis and release were strongly dependent on developmental stage and diet. The male attracting pheromone was verified to be a blend of at least four ascarosides, and peak production of the two most potent mating pheromone components, ascr#3 and asc#8 immediately preceded or coincided with the temporal window for mating. The concentration of ascr#2 increased under starvation conditions and peaked during dauer formation, strongly supporting ascr#2 as the main population density signal (dauer pheromone). After dauer formation, ascaroside production largely ceased and dauer larvae did not release any ascarosides. These findings show that both total ascaroside production and the relative proportions of individual ascarosides strongly correlate with these compounds' stage-specific biological functions. Conclusions/Significance: Ascaroside expression changes with development and environmental conditions. This is consistent with multiple functions of these signaling molecules. Knowledge of such differential regulation will make it possible to associate ascaroside production to gene expression profiles (transcript, protein or enzyme activity) and help to determine genetic pathways that control ascaroside biosynthesis. In conjunction with findings from previous studies, our results show that the pheromone system of C. elegans mimics that of insects in many ways, suggesting that pheromone signaling in C. elegans may exhibit functional homology also at the sensory level. In addition, our results provide a strong foundation for future behavioral modeling studies.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pone.0017804DOIArticle
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0017804PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3058051/PubMed CentralArticle
ORCID:
AuthorORCID
Srinivasan, Jagan0000-0001-5449-7938
Sternberg, Paul W.0000-0002-7699-0173
Schroeder, Frank C.0000-0002-4420-0237
Additional Information:© 2011 Kaplan et al. This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. Received October 26, 2010; Accepted February 11, 2011; Published March 15, 2011. Editor: Paulo Ho, Instituto Butantan, Brazil. Partially funded by National Institutes of Health (1R01GM085285-01A1, 3R01GM085285-01A1S1, and GM088290). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No additional external funding received for this study. Author Contributions: Conceived and designed the experiments: FK HTA JS PWS ASE FCS. Performed the experiments: FK HTA JS PM RA OD RN. Analyzed the data: FK JS HTA FCS ASE PEAT PWS. Contributed reagents/materials/ analysis tools: ASE FCS PWS HTA PEAT. Wrote the paper: FK JS HTA FCS ASE PEAT PWS. Collected nematode secretions in water or M9 buffer: FK RA RN. Collected nematode secretions in liquid culture: RA RN. Performed ascaroside extraction from nematodes: FK. Performed quantification of ascarosides by LC-MS: FK HTA. Designed the biological experiments: JS PWS. Performed all the biological experiments: JS OMD. Synthesized ascr#1, ascr#2, ascr#3, ascr#4 and ascr#8: FCS PM.
Funders:
Funding AgencyGrant Number
NIH1R01GM085285-01A1
NIH3R01GM085285-01A1S1
NIHGM088290
Issue or Number:3
PubMed Central ID:PMC3058051
Record Number:CaltechAUTHORS:20110411-105726989
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110411-105726989
Official Citation:Kaplan F, Srinivasan J, Mahanti P, Ajredini R, Durak O, et al. (2011) Ascaroside Expression in Caenorhabditis elegans Is Strongly Dependent on Diet and Developmental Stage. PLoS ONE 6(3): e17804. doi:10.1371/journal.pone.0017804
Usage Policy:This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
ID Code:23276
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:12 Apr 2011 14:47
Last Modified:03 Oct 2019 02:45

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