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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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The metazoan phylogeny describing the presence or absence of CatSpers and CatSperβ in examined metazoan genomes.The phylogenetic branching patterns of metazoans (not proportional to the evolutionary rates) were extracted from the Tree of Life project (http://www.tolweb.org/tree/) as of July 30, 2008. The metazoan lineages known to contain the CatSper channel complex are indicated by boxes with a solid line and gray background, while those believed to lack the channel complex are marked by boxes with a broken line and white background. Two lineages (Porifera and cartilaginous fishes) are underlined since the results obtained from these lineages are based solely on survey genome or genomic traces rather than complete genome sequences. The availability of more metazoan genome sequences in the future will probably expand and/or refine the lineage branches shown here.
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pone-0003569-g003: The metazoan phylogeny describing the presence or absence of CatSpers and CatSperβ in examined metazoan genomes.The phylogenetic branching patterns of metazoans (not proportional to the evolutionary rates) were extracted from the Tree of Life project (http://www.tolweb.org/tree/) as of July 30, 2008. The metazoan lineages known to contain the CatSper channel complex are indicated by boxes with a solid line and gray background, while those believed to lack the channel complex are marked by boxes with a broken line and white background. Two lineages (Porifera and cartilaginous fishes) are underlined since the results obtained from these lineages are based solely on survey genome or genomic traces rather than complete genome sequences. The availability of more metazoan genome sequences in the future will probably expand and/or refine the lineage branches shown here.

Mentions: Fig. 3 shows the comprehensive evolutionary genomics of the CatSper ion channel complex. We have identified novel CatSper sequences from non-mammal vertebrates, such as the Anole lizard Anolis carolinensis, and cartilaginous fishes Callorhinchus milii and Leucoraja erinacea (Table S1). The CatSper channel complex is completely absent from a diverse sampling of protostome genomes. Interestingly, even though they are present in basal Chordata (amphioxus and sea squirts), all four CatSpers and CatSperβ appear to be lacking in several vertebrate lineages such as Agnatha (jawless fishes), Teleostei (bony fishes), Amphibia (frogs), and Aves (birds). This distinctive lineage distribution pattern of the CatSper channel complex (Fig. 3) is in drastic contrast to that of most ion channels and transporters characterized previously, which are usually highly conserved in metazoans [29], [31], [32], [40], [47], [48].


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)

The metazoan phylogeny describing the presence or absence of CatSpers and CatSperβ in examined metazoan genomes.The phylogenetic branching patterns of metazoans (not proportional to the evolutionary rates) were extracted from the Tree of Life project (http://www.tolweb.org/tree/) as of July 30, 2008. The metazoan lineages known to contain the CatSper channel complex are indicated by boxes with a solid line and gray background, while those believed to lack the channel complex are marked by boxes with a broken line and white background. Two lineages (Porifera and cartilaginous fishes) are underlined since the results obtained from these lineages are based solely on survey genome or genomic traces rather than complete genome sequences. The availability of more metazoan genome sequences in the future will probably expand and/or refine the lineage branches shown here.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0003569-g003: The metazoan phylogeny describing the presence or absence of CatSpers and CatSperβ in examined metazoan genomes.The phylogenetic branching patterns of metazoans (not proportional to the evolutionary rates) were extracted from the Tree of Life project (http://www.tolweb.org/tree/) as of July 30, 2008. The metazoan lineages known to contain the CatSper channel complex are indicated by boxes with a solid line and gray background, while those believed to lack the channel complex are marked by boxes with a broken line and white background. Two lineages (Porifera and cartilaginous fishes) are underlined since the results obtained from these lineages are based solely on survey genome or genomic traces rather than complete genome sequences. The availability of more metazoan genome sequences in the future will probably expand and/or refine the lineage branches shown here.
Mentions: Fig. 3 shows the comprehensive evolutionary genomics of the CatSper ion channel complex. We have identified novel CatSper sequences from non-mammal vertebrates, such as the Anole lizard Anolis carolinensis, and cartilaginous fishes Callorhinchus milii and Leucoraja erinacea (Table S1). The CatSper channel complex is completely absent from a diverse sampling of protostome genomes. Interestingly, even though they are present in basal Chordata (amphioxus and sea squirts), all four CatSpers and CatSperβ appear to be lacking in several vertebrate lineages such as Agnatha (jawless fishes), Teleostei (bony fishes), Amphibia (frogs), and Aves (birds). This distinctive lineage distribution pattern of the CatSper channel complex (Fig. 3) is in drastic contrast to that of most ion channels and transporters characterized previously, which are usually highly conserved in metazoans [29], [31], [32], [40], [47], [48].

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