Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC

The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with di...

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Veröffentlicht in:PloS one 2014-12, Vol.9 (12), p.e114631
Hauptverfasser: Jaratlerdsiri, Weerachai, Deakin, Janine, Godinez, Ricardo M, Shan, Xueyan, Peterson, Daniel G, Marthey, Sylvain, Lyons, Eric, McCarthy, Fiona M, Isberg, Sally R, Higgins, Damien P, Chong, Amanda Y, John, John St, Glenn, Travis C, Ray, David A, Gongora, Jaime
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container_issue 12
container_start_page e114631
container_title PloS one
container_volume 9
creator Jaratlerdsiri, Weerachai
Deakin, Janine
Godinez, Ricardo M
Shan, Xueyan
Peterson, Daniel G
Marthey, Sylvain
Lyons, Eric
McCarthy, Fiona M
Isberg, Sally R
Higgins, Damien P
Chong, Amanda Y
John, John St
Glenn, Travis C
Ray, David A
Gongora, Jaime
description The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with different gene number and organisation. Crocodylia (crocodilians) are widely distributed and represent an evolutionary distinct group among higher vertebrates, but the genomic organisation of MHC within this lineage has been largely unexplored. Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa. We characterised genomic clusters encompassing MHC class I and class II genes in the saltwater crocodile based on sequencing of bacterial artificial chromosomes. Six gene clusters spanning ∼452 kb were identified to contain nine MHC class I genes, six MHC class II genes, three TAP genes, and a TRIM gene. These MHC class I and class II genes were in separate scaffold regions and were greater in length (2-6 times longer) than their counterparts in well-studied fowl B loci, suggesting that the compaction of avian MHC occurred after the crocodilian-avian split. Comparative analyses between the saltwater crocodile MHC and that from the alligator and gharial showed large syntenic areas (>80% identity) with similar gene order. Comparisons with other vertebrates showed that the saltwater crocodile had MHC class I genes located along with TAP, consistent with birds studied. Linkage between MHC class I and TRIM39 observed in the saltwater crocodile resembled MHC in eutherians compared, but absent in avian MHC, suggesting that the saltwater crocodile MHC appears to have gene organisation intermediate between these two lineages. These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.
doi_str_mv 10.1371/journal.pone.0114631
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These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.</description><subject>Adaptive immunity</subject><subject>Alligators</subject><subject>Alligators and Crocodiles - genetics</subject><subject>Alligators and Crocodiles - virology</subject><subject>Analysis</subject><subject>Animals</subject><subject>Antigen presentation</subject><subject>Aquatic reptiles</subject><subject>Artificial chromosomes</subject><subject>Bacterial artificial chromosomes</subject><subject>Biochemistry</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Biotechnology</subject><subject>Birds</subject><subject>Chromosomes</subject><subject>Chromosomes, Artificial, Bacterial - genetics</subject><subject>Clusters</subject><subject>Contig Mapping</subject><subject>Crocodiles</subject><subject>Crocodylidae</subject><subject>Crocodylus porosus</subject><subject>Gene clusters</subject><subject>Gene order</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genes, MHC Class I - genetics</subject><subject>Genes, MHC Class II - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Immunity</subject><subject>Life Sciences</subject><subject>Major histocompatibility complex</subject><subject>Molecular biology</subject><subject>Plant pathology</subject><subject>Reptiles &amp; amphibians</subject><subject>Retroelements - genetics</subject><subject>Retroviridae - genetics</subject><subject>Saline water</subject><subject>Science</subject><subject>Six gene</subject><subject>Species Specificity</subject><subject>Synteny</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl-L00AUxYMo7rr6DUQDgrAPrZm_SV6EUtQWKgu6-jpMZu60s6SZ7sykut_eqc0ujShIIBkmv3Mu996TZS9RMUWkRO9uXO872U53roNpgRDlBD3KzlFN8ITjgjw-OZ9lz0K4KQpGKs6fZmeYsYIwjM6z67nb7qSX0e4hX0PntpDLZHsXIOQe9iDbXNsQbadiHqLvVew95LbL4wbyINv4Q0bwufJOOW1byD8v5s-zJ0a2AV4M34vs28cP1_PFZHX1aTmfrSaqxDxOENKGSV0DJsqUStISM2wQawiumoaXzNAGikbXSHMKtS5NWZGqNgwX6QWIXGSvj7671gUxDCQIxFNvtKYlScTySGgnb8TO2630d8JJK35fOL8W0kerWhC0oYYrQxGuJSVaVaqkRdNQjRijVOLk9X6o1jdb0Aq66GU7Mh3_6exGrN1eUMwJ51UyuDwabP6QLWYrcbhLW6xpUbP9obU3QzHvbnsI8R_tDdRapg5sZ1wqrLY2KDGjqEpg2nOipn-h0qNha1WKj0l7GwsuR4LERPgZ17IPQSy_fvl_9ur7mH17wm5StuImuLaP1nVhDNIjmGIVggfzMC5UiEP676chDukXQ_qT7NXphh5E93EnvwDu6_64</recordid><startdate>20141211</startdate><enddate>20141211</enddate><creator>Jaratlerdsiri, Weerachai</creator><creator>Deakin, Janine</creator><creator>Godinez, Ricardo M</creator><creator>Shan, Xueyan</creator><creator>Peterson, Daniel G</creator><creator>Marthey, Sylvain</creator><creator>Lyons, Eric</creator><creator>McCarthy, Fiona M</creator><creator>Isberg, Sally R</creator><creator>Higgins, Damien P</creator><creator>Chong, Amanda Y</creator><creator>John, John St</creator><creator>Glenn, Travis C</creator><creator>Ray, David A</creator><creator>Gongora, Jaime</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20141211</creationdate><title>Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC</title><author>Jaratlerdsiri, Weerachai ; 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Medical Research Collection</collection><collection>ProQuest One Academic Middle East (New)</collection><collection>ProQuest One Health &amp; Nursing</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Applied &amp; Life Sciences</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jaratlerdsiri, Weerachai</au><au>Deakin, Janine</au><au>Godinez, Ricardo M</au><au>Shan, Xueyan</au><au>Peterson, Daniel G</au><au>Marthey, Sylvain</au><au>Lyons, Eric</au><au>McCarthy, Fiona M</au><au>Isberg, Sally R</au><au>Higgins, Damien P</au><au>Chong, Amanda Y</au><au>John, John St</au><au>Glenn, Travis C</au><au>Ray, David A</au><au>Gongora, Jaime</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-12-11</date><risdate>2014</risdate><volume>9</volume><issue>12</issue><spage>e114631</spage><pages>e114631-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with different gene number and organisation. Crocodylia (crocodilians) are widely distributed and represent an evolutionary distinct group among higher vertebrates, but the genomic organisation of MHC within this lineage has been largely unexplored. Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa. We characterised genomic clusters encompassing MHC class I and class II genes in the saltwater crocodile based on sequencing of bacterial artificial chromosomes. Six gene clusters spanning ∼452 kb were identified to contain nine MHC class I genes, six MHC class II genes, three TAP genes, and a TRIM gene. These MHC class I and class II genes were in separate scaffold regions and were greater in length (2-6 times longer) than their counterparts in well-studied fowl B loci, suggesting that the compaction of avian MHC occurred after the crocodilian-avian split. Comparative analyses between the saltwater crocodile MHC and that from the alligator and gharial showed large syntenic areas (&gt;80% identity) with similar gene order. Comparisons with other vertebrates showed that the saltwater crocodile had MHC class I genes located along with TAP, consistent with birds studied. Linkage between MHC class I and TRIM39 observed in the saltwater crocodile resembled MHC in eutherians compared, but absent in avian MHC, suggesting that the saltwater crocodile MHC appears to have gene organisation intermediate between these two lineages. These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25503521</pmid><doi>10.1371/journal.pone.0114631</doi><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2014-12, Vol.9 (12), p.e114631
issn 1932-6203
1932-6203
language eng
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source Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry
subjects Adaptive immunity
Alligators
Alligators and Crocodiles - genetics
Alligators and Crocodiles - virology
Analysis
Animals
Antigen presentation
Aquatic reptiles
Artificial chromosomes
Bacterial artificial chromosomes
Biochemistry
Bioinformatics
Biology and Life Sciences
Biotechnology
Birds
Chromosomes
Chromosomes, Artificial, Bacterial - genetics
Clusters
Contig Mapping
Crocodiles
Crocodylidae
Crocodylus porosus
Gene clusters
Gene order
Gene sequencing
Genes
Genes, MHC Class I - genetics
Genes, MHC Class II - genetics
Genomes
Genomics
Immunity
Life Sciences
Major histocompatibility complex
Molecular biology
Plant pathology
Reptiles & amphibians
Retroelements - genetics
Retroviridae - genetics
Saline water
Science
Six gene
Species Specificity
Synteny
Vertebrates
Zebrafish
title Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC
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