Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster
Cartilaginous fishes are the oldest living phylogenetic group of jawed vertebrates. Here, we demonstrate the value of cartilaginous fish sequences in reconstructing the evolutionary history of vertebrate genomes by sequencing the protocadherin cluster in the relatively small genome (910 Mb) of the e...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2008-03, Vol.105 (10), p.3819-3824 |
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| creator | Yu, Wei-Ping Rajasegaran, Vikneswari Yew, Kenneth Loh, Wai-lin Tay, Boon-Hui Amemiya, Chris T Brenner, Sydney Venkatesh, Byrappa |
| description | Cartilaginous fishes are the oldest living phylogenetic group of jawed vertebrates. Here, we demonstrate the value of cartilaginous fish sequences in reconstructing the evolutionary history of vertebrate genomes by sequencing the protocadherin cluster in the relatively small genome (910 Mb) of the elephant shark (Callorhinchus milii). Human and coelacanth contain a single protocadherin cluster with 53 and 49 genes, respectively, that are organized in three subclusters, Pcdhα, Pcdhβ, and Pcdhγ, whereas the duplicated protocadherin clusters in fugu and zebrafish contain >77 and 107 genes, respectively, that are organized in Pcdhα and Pcdhγ subclusters. By contrast, the elephant shark contains a single protocadherin cluster with 47 genes organized in four subclusters (Pcdhδ, Pcdhε, Pcdhμ, and Pcdhν). By comparison with elephant shark sequences, we discovered a Pcdhδ subcluster in teleost fishes, coelacanth, Xenopus, and chicken. Our results suggest that the protocadherin cluster in the ancestral jawed vertebrate contained more subclusters than modern vertebrates, and the evolution of the protocadherin cluster is characterized by lineage-specific differential loss of entire subclusters of genes. In contrast to teleost fish and mammalian protocadherin genes that have undergone gene conversion events, elephant shark protocadherin genes have experienced very little gene conversion. The syntenic block of genes in the elephant shark protocadherin locus is well conserved in human but disrupted in fugu. Thus, the elephant shark genome appears to be less prone to rearrangements compared with teleost fish genomes. The small and "stable" genome of the elephant shark is a valuable reference for understanding the evolution of vertebrate genomes. |
| doi_str_mv | 10.1073/pnas.0800398105 |
| format | Article |
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Here, we demonstrate the value of cartilaginous fish sequences in reconstructing the evolutionary history of vertebrate genomes by sequencing the protocadherin cluster in the relatively small genome (910 Mb) of the elephant shark (Callorhinchus milii). Human and coelacanth contain a single protocadherin cluster with 53 and 49 genes, respectively, that are organized in three subclusters, Pcdhα, Pcdhβ, and Pcdhγ, whereas the duplicated protocadherin clusters in fugu and zebrafish contain >77 and 107 genes, respectively, that are organized in Pcdhα and Pcdhγ subclusters. By contrast, the elephant shark contains a single protocadherin cluster with 47 genes organized in four subclusters (Pcdhδ, Pcdhε, Pcdhμ, and Pcdhν). By comparison with elephant shark sequences, we discovered a Pcdhδ subcluster in teleost fishes, coelacanth, Xenopus, and chicken. Our results suggest that the protocadherin cluster in the ancestral jawed vertebrate contained more subclusters than modern vertebrates, and the evolution of the protocadherin cluster is characterized by lineage-specific differential loss of entire subclusters of genes. In contrast to teleost fish and mammalian protocadherin genes that have undergone gene conversion events, elephant shark protocadherin genes have experienced very little gene conversion. The syntenic block of genes in the elephant shark protocadherin locus is well conserved in human but disrupted in fugu. Thus, the elephant shark genome appears to be less prone to rearrangements compared with teleost fish genomes. The small and "stable" genome of the elephant shark is a valuable reference for understanding the evolution of vertebrate genomes.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0800398105</identifier><identifier>PMID: 18319338</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Amino Acid Substitution ; Animals ; Base Sequence ; Biological Sciences ; Cadherins - genetics ; Callorhinchus milii ; Chickens - genetics ; Codon - genetics ; Conserved Sequence ; Danio rerio ; Elephantidae ; Elephants ; Evolution ; Evolution, Molecular ; Evolutionary biology ; Exons ; Exons - genetics ; Fish ; Freshwater ; Fugu ; Gene Conversion ; Genes ; Genome ; Genomes ; Genomics ; Marine ; Models, Genetic ; Molecular Sequence Data ; Multigene Family ; Phylogenetics ; Phylogeny ; Promoter Regions, Genetic - genetics ; Sequence Analysis, DNA ; Sequence Homology, Nucleic Acid ; Sharks ; Sharks - genetics ; Synteny - genetics ; Takifugu - genetics ; Teleostei ; Vertebrates ; Vertebrates - genetics ; Xenopus ; Xenopus - genetics</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2008-03, Vol.105 (10), p.3819-3824</ispartof><rights>Copyright 2008 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Mar 11, 2008</rights><rights>2008 by The National Academy of Sciences of the USA</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c552t-a6c20a11193a3829ea8998f086b5b7feea28ec634120a59454d8f1048645b8a73</citedby><cites>FETCH-LOGICAL-c552t-a6c20a11193a3829ea8998f086b5b7feea28ec634120a59454d8f1048645b8a73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/105/10.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25461325$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25461325$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18319338$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Wei-Ping</creatorcontrib><creatorcontrib>Rajasegaran, Vikneswari</creatorcontrib><creatorcontrib>Yew, Kenneth</creatorcontrib><creatorcontrib>Loh, Wai-lin</creatorcontrib><creatorcontrib>Tay, Boon-Hui</creatorcontrib><creatorcontrib>Amemiya, Chris T</creatorcontrib><creatorcontrib>Brenner, Sydney</creatorcontrib><creatorcontrib>Venkatesh, Byrappa</creatorcontrib><title>Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Cartilaginous fishes are the oldest living phylogenetic group of jawed vertebrates. Here, we demonstrate the value of cartilaginous fish sequences in reconstructing the evolutionary history of vertebrate genomes by sequencing the protocadherin cluster in the relatively small genome (910 Mb) of the elephant shark (Callorhinchus milii). Human and coelacanth contain a single protocadherin cluster with 53 and 49 genes, respectively, that are organized in three subclusters, Pcdhα, Pcdhβ, and Pcdhγ, whereas the duplicated protocadherin clusters in fugu and zebrafish contain >77 and 107 genes, respectively, that are organized in Pcdhα and Pcdhγ subclusters. By contrast, the elephant shark contains a single protocadherin cluster with 47 genes organized in four subclusters (Pcdhδ, Pcdhε, Pcdhμ, and Pcdhν). By comparison with elephant shark sequences, we discovered a Pcdhδ subcluster in teleost fishes, coelacanth, Xenopus, and chicken. Our results suggest that the protocadherin cluster in the ancestral jawed vertebrate contained more subclusters than modern vertebrates, and the evolution of the protocadherin cluster is characterized by lineage-specific differential loss of entire subclusters of genes. In contrast to teleost fish and mammalian protocadherin genes that have undergone gene conversion events, elephant shark protocadherin genes have experienced very little gene conversion. The syntenic block of genes in the elephant shark protocadherin locus is well conserved in human but disrupted in fugu. Thus, the elephant shark genome appears to be less prone to rearrangements compared with teleost fish genomes. The small and "stable" genome of the elephant shark is a valuable reference for understanding the evolution of vertebrate genomes.</description><subject>Amino Acid Substitution</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Biological Sciences</subject><subject>Cadherins - genetics</subject><subject>Callorhinchus milii</subject><subject>Chickens - genetics</subject><subject>Codon - genetics</subject><subject>Conserved Sequence</subject><subject>Danio rerio</subject><subject>Elephantidae</subject><subject>Elephants</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary biology</subject><subject>Exons</subject><subject>Exons - genetics</subject><subject>Fish</subject><subject>Freshwater</subject><subject>Fugu</subject><subject>Gene Conversion</subject><subject>Genes</subject><subject>Genome</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Marine</subject><subject>Models, Genetic</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Sequence Analysis, DNA</subject><subject>Sequence Homology, Nucleic Acid</subject><subject>Sharks</subject><subject>Sharks - genetics</subject><subject>Synteny - genetics</subject><subject>Takifugu - genetics</subject><subject>Teleostei</subject><subject>Vertebrates</subject><subject>Vertebrates - genetics</subject><subject>Xenopus</subject><subject>Xenopus - genetics</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhiMEoqVw5gRYHBCXbcd27NgckKqqfEiVOEDPljc72XjJ2sF2VvSP8HtxtKsucOA01viZdz7eqnpO4ZxCwy9Gb9M5KACuFQXxoDqloOlC1hoeVqcArFmomtUn1ZOUNgCghYLH1QlVnGrO1Wn163rAsbc-k9Tb-J0k_DGhb5FE3KEdEpm8KxnifHLrPqfyyIHkHgnuwjBlF7yNd6R3KYcSQ0d2GDMuo81I1ugxvSOXpA3b0ZaU2yGx3g53yaWZnXXGGHJo7arH6DxphylljE-rR13pjs8O8ay6_XD97erT4ubLx89XlzeLVgiWF1a2DCylZRnLFdNoldaqAyWXYtl0iJYpbCWvacGErkW9Uh2FWslaLJVt-Fn1fq87Tsstrlr0OdrBjNFty1omWGf-_vGuN-uwM4xJ1UhVBN4cBGIod0rZbF1qcRisxzAlw0Az2UhdwNf_gJswxXKLmaE1NEKKAl3soTaGlCJ295NQMLPhZjbcHA0vFS__XODIHxwuwKsDMFce5cQsyRWdJ3v7f8J00zBk_JkL-mKPbma771kmakk5E8dmnQ3GrqNL5vZrWY8DqAZkQ_lv3nnWBw</recordid><startdate>20080311</startdate><enddate>20080311</enddate><creator>Yu, Wei-Ping</creator><creator>Rajasegaran, Vikneswari</creator><creator>Yew, Kenneth</creator><creator>Loh, Wai-lin</creator><creator>Tay, Boon-Hui</creator><creator>Amemiya, Chris T</creator><creator>Brenner, Sydney</creator><creator>Venkatesh, Byrappa</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7TN</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20080311</creationdate><title>Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster</title><author>Yu, Wei-Ping ; 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Here, we demonstrate the value of cartilaginous fish sequences in reconstructing the evolutionary history of vertebrate genomes by sequencing the protocadherin cluster in the relatively small genome (910 Mb) of the elephant shark (Callorhinchus milii). Human and coelacanth contain a single protocadherin cluster with 53 and 49 genes, respectively, that are organized in three subclusters, Pcdhα, Pcdhβ, and Pcdhγ, whereas the duplicated protocadherin clusters in fugu and zebrafish contain >77 and 107 genes, respectively, that are organized in Pcdhα and Pcdhγ subclusters. By contrast, the elephant shark contains a single protocadherin cluster with 47 genes organized in four subclusters (Pcdhδ, Pcdhε, Pcdhμ, and Pcdhν). By comparison with elephant shark sequences, we discovered a Pcdhδ subcluster in teleost fishes, coelacanth, Xenopus, and chicken. Our results suggest that the protocadherin cluster in the ancestral jawed vertebrate contained more subclusters than modern vertebrates, and the evolution of the protocadherin cluster is characterized by lineage-specific differential loss of entire subclusters of genes. In contrast to teleost fish and mammalian protocadherin genes that have undergone gene conversion events, elephant shark protocadherin genes have experienced very little gene conversion. The syntenic block of genes in the elephant shark protocadherin locus is well conserved in human but disrupted in fugu. Thus, the elephant shark genome appears to be less prone to rearrangements compared with teleost fish genomes. The small and "stable" genome of the elephant shark is a valuable reference for understanding the evolution of vertebrate genomes.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>18319338</pmid><doi>10.1073/pnas.0800398105</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Substitution Animals Base Sequence Biological Sciences Cadherins - genetics Callorhinchus milii Chickens - genetics Codon - genetics Conserved Sequence Danio rerio Elephantidae Elephants Evolution Evolution, Molecular Evolutionary biology Exons Exons - genetics Fish Freshwater Fugu Gene Conversion Genes Genome Genomes Genomics Marine Models, Genetic Molecular Sequence Data Multigene Family Phylogenetics Phylogeny Promoter Regions, Genetic - genetics Sequence Analysis, DNA Sequence Homology, Nucleic Acid Sharks Sharks - genetics Synteny - genetics Takifugu - genetics Teleostei Vertebrates Vertebrates - genetics Xenopus Xenopus - genetics |
| title | Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster |
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