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

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...

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Autores principales: Schindelman, Gary, Whittaker, Allyson J, Thum, Jian Yuan, Gharib, Shahla, Sternberg, Paul W
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2006
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1564418/
https://www.ncbi.nlm.nih.gov/pubmed/16911797
http://dx.doi.org/10.1186/1741-7007-4-26
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author Schindelman, Gary
Whittaker, Allyson J
Thum, Jian Yuan
Gharib, Shahla
Sternberg, Paul W
author_facet Schindelman, Gary
Whittaker, Allyson J
Thum, Jian Yuan
Gharib, Shahla
Sternberg, Paul W
author_sort Schindelman, Gary
collection PubMed
description 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. CONCLUSION: 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.
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spelling pubmed-15644182006-09-14 Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord Schindelman, Gary Whittaker, Allyson J Thum, Jian Yuan Gharib, Shahla Sternberg, Paul W BMC Biol Research Article 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. CONCLUSION: 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. BioMed Central 2006-08-15 /pmc/articles/PMC1564418/ /pubmed/16911797 http://dx.doi.org/10.1186/1741-7007-4-26 Text en Copyright © 2006 Schindelman et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 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.
spellingShingle Research Article
Schindelman, Gary
Whittaker, Allyson J
Thum, Jian Yuan
Gharib, Shahla
Sternberg, Paul W
Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord
title Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord
title_full Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord
title_fullStr Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord
title_full_unstemmed Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord
title_short Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord
title_sort initiation of male sperm-transfer behavior in caenorhabditis elegans requires input from the ventral nerve cord
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1564418/
https://www.ncbi.nlm.nih.gov/pubmed/16911797
http://dx.doi.org/10.1186/1741-7007-4-26
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