Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.

Seminal fluid proteins transferred from males to females during copulation are required for full fertility and can exert dramatic effects on female physiology and behavior. In Drosophila melanogaster, the seminal protein sex peptide (SP) affects mated females by increasing egg production and decreas...

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Autores principales: Geoffrey D Findlay, Jessica L Sitnik, Wenke Wang, Charles F Aquadro, Nathan L Clark, Mariana F Wolfner
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Publicado: Public Library of Science (PLoS) 2014
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Acceso en línea:https://doaj.org/article/906410bd63ef4837b735c12ae1f64da6
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spelling oai:doaj.org-article:906410bd63ef4837b735c12ae1f64da62021-11-18T06:21:18ZEvolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.1553-73901553-740410.1371/journal.pgen.1004108https://doaj.org/article/906410bd63ef4837b735c12ae1f64da62014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24453993/pdf/?tool=EBIhttps://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Seminal fluid proteins transferred from males to females during copulation are required for full fertility and can exert dramatic effects on female physiology and behavior. In Drosophila melanogaster, the seminal protein sex peptide (SP) affects mated females by increasing egg production and decreasing receptivity to courtship. These behavioral changes persist for several days because SP binds to sperm that are stored in the female. SP is then gradually released, allowing it to interact with its female-expressed receptor. The binding of SP to sperm requires five additional seminal proteins, which act together in a network. Hundreds of uncharacterized male and female proteins have been identified in this species, but individually screening each protein for network function would present a logistical challenge. To prioritize the screening of these proteins for involvement in the SP network, we used a comparative genomic method to identify candidate proteins whose evolutionary rates across the Drosophila phylogeny co-vary with those of the SP network proteins. Subsequent functional testing of 18 co-varying candidates by RNA interference identified three male seminal proteins and three female reproductive tract proteins that are each required for the long-term persistence of SP responses in females. Molecular genetic analysis showed the three new male proteins are required for the transfer of other network proteins to females and for SP to become bound to sperm that are stored in mated females. The three female proteins, in contrast, act downstream of SP binding and sperm storage. These findings expand the number of seminal proteins required for SP's actions in the female and show that multiple female proteins are necessary for the SP response. Furthermore, our functional analyses demonstrate that evolutionary rate covariation is a valuable predictive tool for identifying candidate members of interacting protein networks.Geoffrey D FindlayJessica L SitnikWenke WangCharles F AquadroNathan L ClarkMariana F WolfnerPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 10, Iss 1, p e1004108 (2014)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Geoffrey D Findlay
Jessica L Sitnik
Wenke Wang
Charles F Aquadro
Nathan L Clark
Mariana F Wolfner
Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.
description Seminal fluid proteins transferred from males to females during copulation are required for full fertility and can exert dramatic effects on female physiology and behavior. In Drosophila melanogaster, the seminal protein sex peptide (SP) affects mated females by increasing egg production and decreasing receptivity to courtship. These behavioral changes persist for several days because SP binds to sperm that are stored in the female. SP is then gradually released, allowing it to interact with its female-expressed receptor. The binding of SP to sperm requires five additional seminal proteins, which act together in a network. Hundreds of uncharacterized male and female proteins have been identified in this species, but individually screening each protein for network function would present a logistical challenge. To prioritize the screening of these proteins for involvement in the SP network, we used a comparative genomic method to identify candidate proteins whose evolutionary rates across the Drosophila phylogeny co-vary with those of the SP network proteins. Subsequent functional testing of 18 co-varying candidates by RNA interference identified three male seminal proteins and three female reproductive tract proteins that are each required for the long-term persistence of SP responses in females. Molecular genetic analysis showed the three new male proteins are required for the transfer of other network proteins to females and for SP to become bound to sperm that are stored in mated females. The three female proteins, in contrast, act downstream of SP binding and sperm storage. These findings expand the number of seminal proteins required for SP's actions in the female and show that multiple female proteins are necessary for the SP response. Furthermore, our functional analyses demonstrate that evolutionary rate covariation is a valuable predictive tool for identifying candidate members of interacting protein networks.
format article
author Geoffrey D Findlay
Jessica L Sitnik
Wenke Wang
Charles F Aquadro
Nathan L Clark
Mariana F Wolfner
author_facet Geoffrey D Findlay
Jessica L Sitnik
Wenke Wang
Charles F Aquadro
Nathan L Clark
Mariana F Wolfner
author_sort Geoffrey D Findlay
title Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.
title_short Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.
title_full Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.
title_fullStr Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.
title_full_unstemmed Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses.
title_sort evolutionary rate covariation identifies new members of a protein network required for drosophila melanogaster female post-mating responses.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/906410bd63ef4837b735c12ae1f64da6
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