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Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperbeta.

Cai X, Clapham DE - PLoS ONE (2008)

Bottom Line: The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis.The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes.These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Duke University Medical Center, Durham, North Carolina, USA. xinjiang.cai@duke.edu

ABSTRACT
The mammalian CatSper ion channel family consists of four sperm-specific voltage-gated Ca2+ channels that are crucial for sperm hyperactivation and male fertility. All four CatSper subunits are believed to assemble into a heteromultimeric channel complex, together with an auxiliary subunit, CatSperbeta. Here, we report a comprehensive comparative genomics study and evolutionary analysis of CatSpers and CatSperbeta, with important correlation to physiological significance of molecular evolution of the CatSper channel complex. The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis. Comparative genomics revealed extensive lineage-specific gene loss of all four CatSpers and CatSperbeta through metazoan evolution, especially in vertebrates. The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes. These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

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Related in: MedlinePlus

Phylogenetic reconstruction of the evolutionary history of CatSpers and CatSperβ in metazoans.The phylogenetic trees of the CatSper protein family (A) and the CatSperβ protein family (B) were constructed using the maximum likelihood approach [37]. Two putative primitive Ca2+ channels (MbrCaVS5 and NveCaVS17) were used as the outgroup for the CatSper family. Bootstrap values of more than 60 are shown at corresponding branches. The CatSper1-4 groups are indicated by rectangular bars, with invertebrate CatSpers filled with white and vertebrate CatSpers with gray. Note that protein sequences that failed in the chi-square test in Tree-Puzzle [69] or contained more than 15% gaps in the refined alignments were not subjected to phylogenetic analysis (Table S1). Abbreviations used: Aca, A. carolinensis; Bfl, B. floridae; Bta, B. taurus; Cfa, C. familiaris; Cin, C. intestinalis; Cja, C. jacchus; Cpo, C. porcellus; Csa, C. savignyi; Eca, E. caballus; Hsa, H. sapiens; Mdo, M. domestica; Mmu, M. mulatta; Mus, M. musculus; Nve, N. vectensis; Oan, O. anatinus; Pan, P. anubis; Ptr, P. troglodytes; Rno, R. norvegicus; Spu, S. purpuratus.
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pone-0003569-g001: Phylogenetic reconstruction of the evolutionary history of CatSpers and CatSperβ in metazoans.The phylogenetic trees of the CatSper protein family (A) and the CatSperβ protein family (B) were constructed using the maximum likelihood approach [37]. Two putative primitive Ca2+ channels (MbrCaVS5 and NveCaVS17) were used as the outgroup for the CatSper family. Bootstrap values of more than 60 are shown at corresponding branches. The CatSper1-4 groups are indicated by rectangular bars, with invertebrate CatSpers filled with white and vertebrate CatSpers with gray. Note that protein sequences that failed in the chi-square test in Tree-Puzzle [69] or contained more than 15% gaps in the refined alignments were not subjected to phylogenetic analysis (Table S1). Abbreviations used: Aca, A. carolinensis; Bfl, B. floridae; Bta, B. taurus; Cfa, C. familiaris; Cin, C. intestinalis; Cja, C. jacchus; Cpo, C. porcellus; Csa, C. savignyi; Eca, E. caballus; Hsa, H. sapiens; Mdo, M. domestica; Mmu, M. mulatta; Mus, M. musculus; Nve, N. vectensis; Oan, O. anatinus; Pan, P. anubis; Ptr, P. troglodytes; Rno, R. norvegicus; Spu, S. purpuratus.

Mentions: Mouse gene knockout studies indicate that all four CatSper subunits are required to mediate functional Ca2+-selective sperm currents necessary for sperm hyperactivation [12]–[14], [21]. However, previous reports have suggested the presence of fewer copies of CatSper homologues in early deuterostomes: three in Ciona intestinalis [40] and two in sea urchin testis [24]. Here, extensive genomic analysis of two sea squirts, C. intestinalis and Ciona savignyi, the sea urchin, Strongylocentrotus purpuratus, and the most basal extant chordate lineage, the amphioxus Branchiostoma floridae [41], [42], demonstrated the presence of four CatSper subunits and single copies of CatSperβ in these four species (Fig. 1A and Supplementary Table S1). Therefore, the CatSper channel complex containing four CatSper subunits and one CatSperβ had developed in early deuterostomes.


Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperbeta.

Cai X, Clapham DE - PLoS ONE (2008)

Phylogenetic reconstruction of the evolutionary history of CatSpers and CatSperβ in metazoans.The phylogenetic trees of the CatSper protein family (A) and the CatSperβ protein family (B) were constructed using the maximum likelihood approach [37]. Two putative primitive Ca2+ channels (MbrCaVS5 and NveCaVS17) were used as the outgroup for the CatSper family. Bootstrap values of more than 60 are shown at corresponding branches. The CatSper1-4 groups are indicated by rectangular bars, with invertebrate CatSpers filled with white and vertebrate CatSpers with gray. Note that protein sequences that failed in the chi-square test in Tree-Puzzle [69] or contained more than 15% gaps in the refined alignments were not subjected to phylogenetic analysis (Table S1). Abbreviations used: Aca, A. carolinensis; Bfl, B. floridae; Bta, B. taurus; Cfa, C. familiaris; Cin, C. intestinalis; Cja, C. jacchus; Cpo, C. porcellus; Csa, C. savignyi; Eca, E. caballus; Hsa, H. sapiens; Mdo, M. domestica; Mmu, M. mulatta; Mus, M. musculus; Nve, N. vectensis; Oan, O. anatinus; Pan, P. anubis; Ptr, P. troglodytes; Rno, R. norvegicus; Spu, S. purpuratus.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2572835&req=5

pone-0003569-g001: Phylogenetic reconstruction of the evolutionary history of CatSpers and CatSperβ in metazoans.The phylogenetic trees of the CatSper protein family (A) and the CatSperβ protein family (B) were constructed using the maximum likelihood approach [37]. Two putative primitive Ca2+ channels (MbrCaVS5 and NveCaVS17) were used as the outgroup for the CatSper family. Bootstrap values of more than 60 are shown at corresponding branches. The CatSper1-4 groups are indicated by rectangular bars, with invertebrate CatSpers filled with white and vertebrate CatSpers with gray. Note that protein sequences that failed in the chi-square test in Tree-Puzzle [69] or contained more than 15% gaps in the refined alignments were not subjected to phylogenetic analysis (Table S1). Abbreviations used: Aca, A. carolinensis; Bfl, B. floridae; Bta, B. taurus; Cfa, C. familiaris; Cin, C. intestinalis; Cja, C. jacchus; Cpo, C. porcellus; Csa, C. savignyi; Eca, E. caballus; Hsa, H. sapiens; Mdo, M. domestica; Mmu, M. mulatta; Mus, M. musculus; Nve, N. vectensis; Oan, O. anatinus; Pan, P. anubis; Ptr, P. troglodytes; Rno, R. norvegicus; Spu, S. purpuratus.
Mentions: Mouse gene knockout studies indicate that all four CatSper subunits are required to mediate functional Ca2+-selective sperm currents necessary for sperm hyperactivation [12]–[14], [21]. However, previous reports have suggested the presence of fewer copies of CatSper homologues in early deuterostomes: three in Ciona intestinalis [40] and two in sea urchin testis [24]. Here, extensive genomic analysis of two sea squirts, C. intestinalis and Ciona savignyi, the sea urchin, Strongylocentrotus purpuratus, and the most basal extant chordate lineage, the amphioxus Branchiostoma floridae [41], [42], demonstrated the presence of four CatSper subunits and single copies of CatSperβ in these four species (Fig. 1A and Supplementary Table S1). Therefore, the CatSper channel complex containing four CatSper subunits and one CatSperβ had developed in early deuterostomes.

Bottom Line: The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis.The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes.These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Duke University Medical Center, Durham, North Carolina, USA. xinjiang.cai@duke.edu

ABSTRACT
The mammalian CatSper ion channel family consists of four sperm-specific voltage-gated Ca2+ channels that are crucial for sperm hyperactivation and male fertility. All four CatSper subunits are believed to assemble into a heteromultimeric channel complex, together with an auxiliary subunit, CatSperbeta. Here, we report a comprehensive comparative genomics study and evolutionary analysis of CatSpers and CatSperbeta, with important correlation to physiological significance of molecular evolution of the CatSper channel complex. The development of the CatSper channel complex with four CatSpers and CatSperbeta originated as early as primitive metazoans such as the Cnidarian Nematostella vectensis. Comparative genomics revealed extensive lineage-specific gene loss of all four CatSpers and CatSperbeta through metazoan evolution, especially in vertebrates. The CatSper channel complex underwent rapid evolution and functional divergence, while distinct evolutionary constraints appear to have acted on different domains and specific sites of the four CatSper genes. These results reveal unique evolutionary characteristics of sperm-specific Ca2+ channels and their adaptation to sperm biology through metazoan evolution.

Show MeSH
Related in: MedlinePlus