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Sex-specific mating pheromones in the nematode Panagrellus redivivus

Choe, Andrea and Chuman, Tatsuji and von Reuss, Stephan H. and Dossey, Aaron T. and Yim, Joshua J. and Ajredini, Ramadan and Kolawa, Adam A. and Kaplan, Fatma and Alborn, Hans T. and Teal, Peter E. A. and Schroeder, Frank C. and Sternberg, Paul W. and Edison, Arthur S. (2012) Sex-specific mating pheromones in the nematode Panagrellus redivivus. Proceedings of the National Academy of Sciences of the United States of America, 109 (51). pp. 20949-20954. ISSN 0027-8424. PMCID PMC3529029. https://resolver.caltech.edu/CaltechAUTHORS:20130208-132151908

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Abstract

Nematodes use an extensive chemical language based on glycosides of the dideoxysugar ascarylose for developmental regulation (dauer formation), male sex attraction, aggregation, and dispersal. However, no examples of a female- or hermaphrodite-specific sex attractant have been identified to date. In this study, we investigated the pheromone system of the gonochoristic sour paste nematode Panagrellus redivivus, which produces sex-specific attractants of the opposite sex. Activity-guided fractionation of the P. redivivus exometabolome revealed that males are strongly attracted to ascr#1 (also known as daumone), an ascaroside previously identified from Caenorhabditis elegans hermaphrodites. Female P. redivivus are repelled by high concentrations of ascr#1 but are specifically attracted to a previously unknown ascaroside that we named dhas#18, a dihydroxy derivative of the known ascr#18 and an ascaroside that features extensive functionalization of the lipid-derived side chain. Targeted profiling of the P. redivivus exometabolome revealed several additional ascarosides that did not induce strong chemotaxis. We show that P. redivivus females, but not males, produce the male-attracting ascr#1, whereas males, but not females, produce the female-attracting dhas#18. These results show that ascaroside biosynthesis in P. redivivus is highly sex-specific. Furthermore, the extensive side chain functionalization in dhas#18, which is reminiscent of polyketide-derived natural products, indicates unanticipated biosynthetic capabilities in nematodes.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1218302109 DOIArticle
http://www.pnas.org/content/109/51/20949PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3529029/PubMed CentralArticle
ORCID:
AuthorORCID
Schroeder, Frank C.0000-0002-4420-0237
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2012 National Academy of Sciences. Contributed by Paul W. Sternberg, October 23, 2012 (sent for review July 5, 2012). Published online before print December 3, 2012. We thank James R. Rocca for expert assistance in NMR data collection and interpretation. NMR data were collected in the University of Florida Advanced Magnetic Resonance Imaging and Spectroscopy (AMRIS) Facility, which is supported in part by the National Science Foundation-funded National High Magnetic Field Laboratory. Support for this study was from National Institutes of Health Grant R01GM085285. Author contributions: A.C., T.C., S.H.v.R., A.T.D., R.A., F.C.S., P.W.S., and A.S.E. designed research; A.C., T.C., S.H.v.R., A.T.D., J.J.Y., R.A., A.A.K., and F.K. performed research; J.J.Y., A.A.K., H.T.A., and P.E.A.T. contributed new reagents/analytic tools; A.C., T.C., S.H.v.R., A.T.D., F.C.S., P.W.S., and A.S.E. analyzed data; A.C., T.C., S.H.v.R., F.C.S., P.W.S., and A.S.E. wrote the paper; A.C., P.W.S., and A.S.E. conceived of purification of Panagrellus redivivus cues; A.C. performed the behavior assays for the activity-guided fractionation; A.C. and A.A.K. performed the behavior assays for the synthesized ascarosides; T.C., S.H.v.R., A.T.D., and R.A. conducted activity-guided fractionation, purification, and structural elucidation of dhas#18 and ascr#1; S.H.v.R. and F.C.S. conducted targeted screening of ascarosides and the Mosher analysis for absolute configuration of dhas#18; J.J.Y. and F.C.S. synthesized dhas#18; R.A. grew large-scale liquid cultures of P. redivivus and performed solid-phase extractions; and F.K., H.T.A., and P.E.A.T. trained T.C. for the activity-guided purification of Panagrellus mating pheromone and developed methods for LC-MS to analyze and purify the fractions.
Funders:
Funding AgencyGrant Number
NIHR01GM085285
Subject Keywords:chemical ecology; chemical signaling; peroxisomal β-oxidation; metabolomics
Issue or Number:51
PubMed Central ID:PMC3529029
Record Number:CaltechAUTHORS:20130208-132151908
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130208-132151908
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:36828
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:08 Feb 2013 22:27
Last Modified:03 Oct 2019 04:41

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