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Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord

Schindelman, Gary and Whittaker, Allyson J. and Thum, Jian Yuan and Gharib, Shahla and Sternberg, Paul W. (2006) Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord. BMC Biology, 4 . Art. no. 26. ISSN 1741-7007. PMCID PMC1564418. https://resolver.caltech.edu/CaltechAUTHORS:SCHIbmcbiol06

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Abstract

Background: The Caenorhabditis elegans male exhibits a stereotypic behavioral pattern when attempting to mate. This behavior has been divided into the following steps: response, backing, turning, vulva location, spicule insertion, and sperm transfer. We and others have begun in-depth analyses of all these steps in order to understand how complex behaviors are generated. Here we extend our understanding of the sperm-transfer step of male mating behavior. Results: Based on observation of wild-type males and on genetic analysis, we have divided the sperm-transfer step of mating behavior into four sub-steps: initiation, release, continued transfer, and cessation. To begin to understand how these sub-steps of sperm transfer are regulated, we screened for ethylmethanesulfonate (EMS)-induced mutations that cause males to transfer sperm aberrantly. We isolated an allele of unc-18, a previously reported member of the Sec1/Munc-18 (SM) family of proteins that is necessary for regulated exocytosis in C. elegans motor neurons. Our allele, sy671, is defective in two distinct sub-steps of sperm transfer: initiation and continued transfer. By a series of transgenic site-of-action experiments, we found that motor neurons in the ventral nerve cord require UNC-18 for the initiation of sperm transfer, and that UNC-18 acts downstream or in parallel to the SPV sensory neurons in this process. In addition to this neuronal requirement, we found that non-neuronal expression of UNC-18, in the male gonad, is necessary for the continuation of sperm transfer. Conclusions: Our division of sperm-transfer behavior into sub-steps has provided a framework for the further detailed analysis of sperm transfer and its integration with other aspects of mating behavior. By determining the site of action of UNC-18 in sperm-transfer behavior, and its relation to the SPV sensory neurons, we have further defined the cells and tissues involved in the generation of this behavior. We have shown both a neuronal and non-neuronal requirement for UNC-18 in distinct sub-steps of sperm-transfer behavior. The definition of circuit components is a crucial first step toward understanding how genes specify the neural circuit and hence the behavior.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1564418/PubMed CentralArticle
ORCID:
AuthorORCID
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2006 Schindelman et al., licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Submission date 17 January 2006; Acceptance date 15 August 2006; Publication date 15 August 2006. GS, AJW and PWS conceived the study. GS, AJW, JYT, and SG all contributed to the genetic screening and the initial characterization of isolated male mating-behavior mutants. GS performed laser ablations, genetic manipulations, and behavioral assays on transformants. JYT was involved in the behavioral assays on transformants. GS drafted the manuscript, with AJW, JYT, SG, and PWS revising it critically for important intellectual content. All authors read and approved the final manuscript. We thank Cheryl Van Buskirk, Jagan Srinivasan and Rene Garcia and members of his laboratory for critical reading of this manuscript. We thank Ryuji Hosono, Erik Jorgensen and James Rand for additional alleles of unc-18. This research was supported by the Howard Hughes Medical Institute, with which P.W.S. is an investigator. G.S. and A.J.W. were supported by NIH postdoctoral fellowships NS043037 and NS042497, respectively.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIH Postdoctoral FellowshipNS043037
NIH Postdoctoral FellowshipNS042497
PubMed Central ID:PMC1564418
Record Number:CaltechAUTHORS:SCHIbmcbiol06
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:SCHIbmcbiol06
Alternative URL:http://dx.doi.org/10.1186/1741-7007-4-26
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:4396
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:21 Aug 2006
Last Modified:02 Oct 2019 23:12

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