Cargando…

Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae

BACKGROUND: During copulation, the major Afro-tropical malaria vector Anopheles gambiae s.s. transfers male accessory gland (MAG) proteins to females as a solid mass (i.e. the "mating plug"). These proteins are postulated to function as important modulators of female post-mating responses....

Descripción completa

Detalles Bibliográficos
Autores principales: Mancini, Emiliano, Baldini, Francesco, Tammaro, Federica, Calzetta, Maria, Serrao, Aurelio, George, Phillip, Morlais, Isabelle, Masiga, Daniel, Sharakhov, Igor V, Rogers, David W, Catteruccia, Flaminia, della Torre, Alessandra
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3199272/
https://www.ncbi.nlm.nih.gov/pubmed/21978124
http://dx.doi.org/10.1186/1471-2148-11-292
_version_ 1782214554283933696
author Mancini, Emiliano
Baldini, Francesco
Tammaro, Federica
Calzetta, Maria
Serrao, Aurelio
George, Phillip
Morlais, Isabelle
Masiga, Daniel
Sharakhov, Igor V
Rogers, David W
Catteruccia, Flaminia
della Torre, Alessandra
author_facet Mancini, Emiliano
Baldini, Francesco
Tammaro, Federica
Calzetta, Maria
Serrao, Aurelio
George, Phillip
Morlais, Isabelle
Masiga, Daniel
Sharakhov, Igor V
Rogers, David W
Catteruccia, Flaminia
della Torre, Alessandra
author_sort Mancini, Emiliano
collection PubMed
description BACKGROUND: During copulation, the major Afro-tropical malaria vector Anopheles gambiae s.s. transfers male accessory gland (MAG) proteins to females as a solid mass (i.e. the "mating plug"). These proteins are postulated to function as important modulators of female post-mating responses. To understand the role of selective forces underlying the evolution of these proteins in the A. gambiae complex, we carried out an evolutionary analysis of gene sequence and expression divergence on a pair of paralog genes called AgAcp34A-1 and AgAcp34A-2. These encode MAG-specific proteins which, based on homology with Drosophila, have been hypothesized to play a role in sperm viability and function. RESULTS: Genetic analysis of 6 species of the A. gambiae complex revealed the existence of a third paralog (68-78% of identity), that we named AgAcp34A-3. FISH assays showed that this gene maps in the same division (34A) of chromosome-3R as the other two paralogs. In particular, immuno-fluorescence assays targeting the C-terminals of AgAcp34A-2 and AgAcp34A-3 revealed that these two proteins are localized in the posterior part of the MAG and concentrated at the apical portion of the mating plug. When transferred to females, this part of the plug lies in proximity to the duct connecting the spermatheca to the uterus, suggesting a potential role for these proteins in regulating sperm motility. AgAcp34A-3 is more polymorphic than the other two paralogs, possibly because of relaxation of purifying selection. Since both unequal crossing-over and gene conversion likely homogenized the members of this gene family, the interpretation of the evolutionary patterns is not straightforward. Although several haplotypes of the three paralogs are shared by most A. gambiae s.l. species, some fixed species-specific replacements (mainly placed in the N- and C-terminal portions of the secreted peptides) were also observed, suggesting some lineage-specific adaptation. CONCLUSIONS: Progress in understanding the signaling cascade in the A. gambiae reproductive pathway will elucidate the interaction of this MAG-specific protein family with their female counterparts. This knowledge will allow a better evaluation of the relative importance of genes involved in the reproductive isolation and fertility of A. gambiae species and could help the interpretation of the observed evolutionary patterns.
format Online
Article
Text
id pubmed-3199272
institution National Center for Biotechnology Information
language English
publishDate 2011
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-31992722011-10-24 Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae Mancini, Emiliano Baldini, Francesco Tammaro, Federica Calzetta, Maria Serrao, Aurelio George, Phillip Morlais, Isabelle Masiga, Daniel Sharakhov, Igor V Rogers, David W Catteruccia, Flaminia della Torre, Alessandra BMC Evol Biol Research Article BACKGROUND: During copulation, the major Afro-tropical malaria vector Anopheles gambiae s.s. transfers male accessory gland (MAG) proteins to females as a solid mass (i.e. the "mating plug"). These proteins are postulated to function as important modulators of female post-mating responses. To understand the role of selective forces underlying the evolution of these proteins in the A. gambiae complex, we carried out an evolutionary analysis of gene sequence and expression divergence on a pair of paralog genes called AgAcp34A-1 and AgAcp34A-2. These encode MAG-specific proteins which, based on homology with Drosophila, have been hypothesized to play a role in sperm viability and function. RESULTS: Genetic analysis of 6 species of the A. gambiae complex revealed the existence of a third paralog (68-78% of identity), that we named AgAcp34A-3. FISH assays showed that this gene maps in the same division (34A) of chromosome-3R as the other two paralogs. In particular, immuno-fluorescence assays targeting the C-terminals of AgAcp34A-2 and AgAcp34A-3 revealed that these two proteins are localized in the posterior part of the MAG and concentrated at the apical portion of the mating plug. When transferred to females, this part of the plug lies in proximity to the duct connecting the spermatheca to the uterus, suggesting a potential role for these proteins in regulating sperm motility. AgAcp34A-3 is more polymorphic than the other two paralogs, possibly because of relaxation of purifying selection. Since both unequal crossing-over and gene conversion likely homogenized the members of this gene family, the interpretation of the evolutionary patterns is not straightforward. Although several haplotypes of the three paralogs are shared by most A. gambiae s.l. species, some fixed species-specific replacements (mainly placed in the N- and C-terminal portions of the secreted peptides) were also observed, suggesting some lineage-specific adaptation. CONCLUSIONS: Progress in understanding the signaling cascade in the A. gambiae reproductive pathway will elucidate the interaction of this MAG-specific protein family with their female counterparts. This knowledge will allow a better evaluation of the relative importance of genes involved in the reproductive isolation and fertility of A. gambiae species and could help the interpretation of the observed evolutionary patterns. BioMed Central 2011-10-06 /pmc/articles/PMC3199272/ /pubmed/21978124 http://dx.doi.org/10.1186/1471-2148-11-292 Text en Copyright ©2011 Mancini 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
Mancini, Emiliano
Baldini, Francesco
Tammaro, Federica
Calzetta, Maria
Serrao, Aurelio
George, Phillip
Morlais, Isabelle
Masiga, Daniel
Sharakhov, Igor V
Rogers, David W
Catteruccia, Flaminia
della Torre, Alessandra
Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae
title Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae
title_full Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae
title_fullStr Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae
title_full_unstemmed Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae
title_short Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae
title_sort molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the african malaria vector anopheles gambiae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3199272/
https://www.ncbi.nlm.nih.gov/pubmed/21978124
http://dx.doi.org/10.1186/1471-2148-11-292
work_keys_str_mv AT manciniemiliano molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT baldinifrancesco molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT tammarofederica molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT calzettamaria molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT serraoaurelio molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT georgephillip molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT morlaisisabelle molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT masigadaniel molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT sharakhovigorv molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT rogersdavidw molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT catterucciaflaminia molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae
AT dellatorrealessandra molecularcharacterizationandevolutionofagenefamilyencodingmalespecificreproductiveproteinsintheafricanmalariavectoranophelesgambiae