Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
BMC Evol Biol
2016 Jan 05;16:5. doi: 10.1186/s12862-015-0577-9.
Show Gene links
Show Anatomy links
Molecular evolution of candidate male reproductive genes in the brown algal model Ectocarpus.
Lipinska AP, Van Damme EJ, De Clerck O.
???displayArticle.abstract???
BACKGROUND: Evolutionary studies of genes that mediate recognition between sperm and egg contribute to our understanding of reproductive isolation and speciation. Surface receptors involved in fertilization are targets of sexual selection, reinforcement, and other evolutionary forces including positive selection. This observation was made across different lineages of the eukaryotic tree from land plants to mammals, and is particularly evident in free-spawning animals. Here we use the brown algal model species Ectocarpus (Phaeophyceae) to investigate the evolution of candidate gamete recognition proteins in a distant major phylogenetic group of eukaryotes.
RESULTS: Male gamete specific genes were identified by comparing transcriptome data covering different stages of the Ectocarpus life cycle and screened for characteristics expected from gamete recognition receptors. Selected genes were sequenced in a representative number of strains from distant geographical locations and varying stages of reproductive isolation, to search for signatures of adaptive evolution. One of the genes (Esi0130_0068) showed evidence of selective pressure. Interestingly, that gene displayed domain similarities to the receptor for egg jelly (REJ) protein involved in sperm-egg recognition in sea urchins.
CONCLUSIONS: We have identified a male gamete specific gene with similarity to known gamete recognition receptors and signatures of adaptation. Altogether, this gene could contribute to gamete interaction during reproduction as well as reproductive isolation in Ectocarpus and is therefore a good candidate for further functional evaluation.
Fig. 1. Species tree and species sexual compatibility. Maximum likelihood tree based on the cox3 gene from nine Ectocarpus strains and two Scytosiphon lomentaria specimens. Strains used in this study are marked with blue bars. ML bootstrap (left) and Bayesian posterior probability (right) values are shown. Red lines define species with prezygotic barriers to fertilization; dotted lines describe species with uncertain gamete compatibility; grey shading indicates pairwise d
N
/d
Sâ>â1 (PAML) (see Additional file 4)
Fig. 3. Topology of Esi0130_0068 as predicted by Phyre2 and Blast2GO. The extracellular and cytoplasmic sides of the membrane are labeled and the beginning and end of each transmembrane helix are indicated by the residue index. Positively selected sites identified by PAML 4 are marked with orange arrows, sites identified by HyPhy are marked in blue
Altschul,
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
1997, Pubmed
Altschul,
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
1997,
Pubmed Armbrust,
Identification of a new gene family expressed during the onset of sexual reproduction in the centric diatom Thalassiosira weissflogii.
1999,
Pubmed Armbrust,
Rapid evolution of a sexual reproduction gene in centric diatoms of the genus Thalassiosira.
2001,
Pubmed Bernasconi,
Evolutionary ecology of the prezygotic stage.
2004,
Pubmed Blackman,
Identification of a mastigoneme protein from Phytophthora nicotianae.
2011,
Pubmed Bolwell,
Fertilization in brown algae. II. Evidence for lectin-sensitive complementary receptors involved in gamete recognition in Fucus serratus.
1979,
Pubmed Bolwell,
Fertilization in brown algae. III. Preliminary characterization of putative gamete receptors from eggs and sperm of Fucus serratus.
1980,
Pubmed Chapman,
Evolutionary conflicts of interest between males and females.
2006,
Pubmed Civetta,
Sex-related genes, directional sexual selection, and speciation.
1998,
Pubmed Civetta,
High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species.
1995,
Pubmed Clark,
Coevolution of interacting fertilization proteins.
2009,
Pubmed Clark,
Evolution of reproductive proteins from animals and plants.
2006,
Pubmed Clark,
Pervasive adaptive evolution in primate seminal proteins.
2005,
Pubmed Cock,
The Ectocarpus genome and the independent evolution of multicellularity in brown algae.
2010,
Pubmed Cock,
The Ectocarpus genome sequence: insights into brown algal biology and the evolutionary diversity of the eukaryotes.
2010,
Pubmed Coelho,
Ectocarpus: a model organism for the brown algae.
2012,
Pubmed Conesa,
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research.
2005,
Pubmed Delport,
Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology.
2010,
Pubmed Ellegren,
The evolution of sex-biased genes and sex-biased gene expression.
2007,
Pubmed Felsenstein,
Evolutionary trees from DNA sequences: a maximum likelihood approach.
1981,
Pubmed Ferris,
Rapid evolution of sex-related genes in Chlamydomonas.
1997,
Pubmed Galindo,
Positive selection in the egg receptor for abalone sperm lysin.
2003,
Pubmed Gossmann,
Selection-driven evolution of sex-biased genes is consistent with sexual selection in Arabidopsis thaliana.
2014,
Pubmed Gschloessl,
HECTAR: a method to predict subcellular targeting in heterokonts.
2008,
Pubmed Gunaratne,
The 10 sea urchin receptor for egg jelly proteins (SpREJ) are members of the polycystic kidney disease-1 (PKD1) family.
2007,
Pubmed
,
Echinobase Hamm,
Evidence of amino acid diversity-enhancing selection within humans and among primates at the candidate sperm-receptor gene PKDREJ.
2007,
Pubmed Hart,
Next-generation studies of mating system evolution.
2012,
Pubmed Hart,
Incipient speciation of sea star populations by adaptive gamete recognition coevolution.
2014,
Pubmed
,
Echinobase Hellberg,
Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods.
1999,
Pubmed Hirohashi,
Egg and sperm recognition systems during fertilization.
2008,
Pubmed
,
Echinobase Honda,
Homologs of the sexually induced gene 1 (sig1) product constitute the stramenopile mastigonemes.
2007,
Pubmed Hughes,
Identification of a human homologue of the sea urchin receptor for egg jelly: a polycystic kidney disease-like protein.
1999,
Pubmed
,
Echinobase Kelley,
Protein structure prediction on the Web: a case study using the Phyre server.
2009,
Pubmed Koressaar,
Enhancements and modifications of primer design program Primer3.
2007,
Pubmed Kosman,
Sperm competition and the evolution of gametic compatibility in externally fertilizing taxa.
2014,
Pubmed Krogh,
Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
2001,
Pubmed Larkin,
Clustal W and Clustal X version 2.0.
2007,
Pubmed Lee,
Positive selection is a general phenomenon in the evolution of abalone sperm lysin.
1995,
Pubmed Lessios,
Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution.
2012,
Pubmed
,
Echinobase Lipinska,
Sexual dimorphism and the evolution of sex-biased gene expression in the brown alga ectocarpus.
2015,
Pubmed Lipinska,
Uncovering the genetic basis for early isogamete differentiation: a case study of Ectocarpus siliculosus.
2013,
Pubmed Mah,
Positive selection in the carbohydrate recognition domains of sea urchin sperm receptor for egg jelly (suREJ) proteins.
2005,
Pubmed
,
Echinobase Mank,
Are sex-biased genes more dispensable?
2009,
Pubmed Mank,
Rapid evolution of female-biased, but not male-biased, genes expressed in the avian brain.
2007,
Pubmed Metz,
Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin.
1996,
Pubmed
,
Echinobase Moy,
The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1.
1996,
Pubmed
,
Echinobase Mugal,
Why time matters: codon evolution and the temporal dynamics of dN/dS.
2014,
Pubmed Murrell,
Detecting individual sites subject to episodic diversifying selection.
2012,
Pubmed Nydam,
Reproductive protein evolution in two cryptic species of marine chordate.
2011,
Pubmed Palumbi,
Speciation and the evolution of gamete recognition genes: pattern and process.
2009,
Pubmed
,
Echinobase Parfrey,
Estimating the timing of early eukaryotic diversification with multigene molecular clocks.
2011,
Pubmed Pond,
HyPhy: hypothesis testing using phylogenies.
2005,
Pubmed Qian,
Cleavage of polycystin-1 requires the receptor for egg jelly domain and is disrupted by human autosomal-dominant polycystic kidney disease 1-associated mutations.
2002,
Pubmed Ronquist,
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.
2012,
Pubmed Sonnhammer,
A hidden Markov model for predicting transmembrane helices in protein sequences.
1998,
Pubmed Sorhannus,
The effect of positive selection on a sexual reproduction gene in Thalassiosira weissflogii (Bacillariophyta): results obtained from maximum-likelihood and parsimony-based methods.
2003,
Pubmed Sorhannus,
Evidence for positive selection on a sexual reproduction gene in the diatom genus Thalassiosira (Bacillariophyta).
2006,
Pubmed Stamatakis,
A rapid bootstrap algorithm for the RAxML Web servers.
2008,
Pubmed Sterck,
ORCAE: online resource for community annotation of eukaryotes.
2012,
Pubmed Swanson,
Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.
2001,
Pubmed Swanson,
Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein.
1998,
Pubmed Tamura,
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.
2013,
Pubmed Trimmer,
Monoclonal antibodies increase intracellular Ca2+ in sea urchin spermatozoa.
1986,
Pubmed
,
Echinobase Turner,
Causes and consequences of the evolution of reproductive proteins.
2008,
Pubmed Untergasser,
Primer3--new capabilities and interfaces.
2012,
Pubmed Vacquier,
The fucose sulfate polymer of egg jelly binds to sperm REJ and is the inducer of the sea urchin sperm acrosome reaction.
1997,
Pubmed
,
Echinobase Vacquier,
Selection in the rapid evolution of gamete recognition proteins in marine invertebrates.
2011,
Pubmed
,
Echinobase Wang,
Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata.
2001,
Pubmed Yang,
PAML 4: phylogenetic analysis by maximum likelihood.
2007,
Pubmed Yang,
Codon-substitution models for heterogeneous selection pressure at amino acid sites.
2000,
Pubmed Yang,
Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution.
1998,
Pubmed Yang,
Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A.
2000,
Pubmed