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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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Chromosomal synteny between human and chicken genomes and sequence alignment of degenerated CatSperβ and CatSper3 fragments from bird genomes.A, chromosomal regions harboring degenerate DNA fragment of putative CatSperβ on chicken chromosome 5 with synteny to human chromosome 14. Shown here are ten genes flanking H. sapiens CatSperβ on human chromosome 14 and syntenic genes on chicken chromosome 5 (not to the scale of base-pair length). CatSperβ is indicated with a black rectangle and other genes with gray rectangles. The location of the degenerate genomic fragment of putative chicken CatSperβ is specified with an open rectangle, and the translated sequence is aligned with HsaCatSperβ. B, H. sapiens CatSper3 is aligned with the short stretch of sequences translated from putative degenerate chicken and zebra finch CatSper3 fragments. Abbreviations for flanking genes can be found in Table S2.
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pone-0003569-g004: Chromosomal synteny between human and chicken genomes and sequence alignment of degenerated CatSperβ and CatSper3 fragments from bird genomes.A, chromosomal regions harboring degenerate DNA fragment of putative CatSperβ on chicken chromosome 5 with synteny to human chromosome 14. Shown here are ten genes flanking H. sapiens CatSperβ on human chromosome 14 and syntenic genes on chicken chromosome 5 (not to the scale of base-pair length). CatSperβ is indicated with a black rectangle and other genes with gray rectangles. The location of the degenerate genomic fragment of putative chicken CatSperβ is specified with an open rectangle, and the translated sequence is aligned with HsaCatSperβ. B, H. sapiens CatSper3 is aligned with the short stretch of sequences translated from putative degenerate chicken and zebra finch CatSper3 fragments. Abbreviations for flanking genes can be found in Table S2.

Mentions: By examining genomic regions with the ECR browser and the NCBI genomic database, we found highly conserved synteny between selected regions of the mouse and human genomes and those of the chicken genome for CatSper2-4 and CatSperβ (Fig. 4 and Table S2, S3, S4, S5, S6). As shown in Fig. 4A and Table S2, 10 genes flanking the 5′- and 3′-end of CatSperβ on human chromosome 14 and corresponding orthologous genes on chicken chromosome 5 are syntenic. By using three different gene-finding programs [37], subsequent examination of chicken genomic sequence located between SMEK1 and TC2N genes did not yield any obvious gene coding region, but a portion of the genomic sequence could be translated into a 66-aa fragment with high similarity to human CatSperβ (Fig. 4A) and other CatSperβ sequences (data not shown). Similar observations have also been observed for CatSper2 and CatSper3 (Tables S4 and S5). Thus, CatSper sequences might have been degenerated in chick genomes, with short fragments of coding sequences still present.


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)

Chromosomal synteny between human and chicken genomes and sequence alignment of degenerated CatSperβ and CatSper3 fragments from bird genomes.A, chromosomal regions harboring degenerate DNA fragment of putative CatSperβ on chicken chromosome 5 with synteny to human chromosome 14. Shown here are ten genes flanking H. sapiens CatSperβ on human chromosome 14 and syntenic genes on chicken chromosome 5 (not to the scale of base-pair length). CatSperβ is indicated with a black rectangle and other genes with gray rectangles. The location of the degenerate genomic fragment of putative chicken CatSperβ is specified with an open rectangle, and the translated sequence is aligned with HsaCatSperβ. B, H. sapiens CatSper3 is aligned with the short stretch of sequences translated from putative degenerate chicken and zebra finch CatSper3 fragments. Abbreviations for flanking genes can be found in Table S2.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2572835&req=5

pone-0003569-g004: Chromosomal synteny between human and chicken genomes and sequence alignment of degenerated CatSperβ and CatSper3 fragments from bird genomes.A, chromosomal regions harboring degenerate DNA fragment of putative CatSperβ on chicken chromosome 5 with synteny to human chromosome 14. Shown here are ten genes flanking H. sapiens CatSperβ on human chromosome 14 and syntenic genes on chicken chromosome 5 (not to the scale of base-pair length). CatSperβ is indicated with a black rectangle and other genes with gray rectangles. The location of the degenerate genomic fragment of putative chicken CatSperβ is specified with an open rectangle, and the translated sequence is aligned with HsaCatSperβ. B, H. sapiens CatSper3 is aligned with the short stretch of sequences translated from putative degenerate chicken and zebra finch CatSper3 fragments. Abbreviations for flanking genes can be found in Table S2.
Mentions: By examining genomic regions with the ECR browser and the NCBI genomic database, we found highly conserved synteny between selected regions of the mouse and human genomes and those of the chicken genome for CatSper2-4 and CatSperβ (Fig. 4 and Table S2, S3, S4, S5, S6). As shown in Fig. 4A and Table S2, 10 genes flanking the 5′- and 3′-end of CatSperβ on human chromosome 14 and corresponding orthologous genes on chicken chromosome 5 are syntenic. By using three different gene-finding programs [37], subsequent examination of chicken genomic sequence located between SMEK1 and TC2N genes did not yield any obvious gene coding region, but a portion of the genomic sequence could be translated into a 66-aa fragment with high similarity to human CatSperβ (Fig. 4A) and other CatSperβ sequences (data not shown). Similar observations have also been observed for CatSper2 and CatSper3 (Tables S4 and S5). Thus, CatSper sequences might have been degenerated in chick genomes, with short fragments of coding sequences still present.

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