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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Main Authors: Weerachai Jaratlerdsiri, Janine Deakin, Ricardo M Godinez, Xueyan Shan, Daniel G Peterson, Sylvain Marthey, Eric Lyons, Fiona M McCarthy, Sally R Isberg, Damien P Higgins, Amanda Y Chong, John St John, Travis C Glenn, David A Ray, Jaime Gongora
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0114631
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spelling doaj-4b4f6cf4129a43dc8c740bb4d15544a22021-03-03T20:10:59ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-01912e11463110.1371/journal.pone.0114631Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.Weerachai JaratlerdsiriJanine DeakinRicardo M GodinezXueyan ShanDaniel G PetersonSylvain MartheyEric LyonsFiona M McCarthySally R IsbergDamien P HigginsAmanda Y ChongJohn St JohnTravis C GlennDavid A RayJaime GongoraThe 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.https://doi.org/10.1371/journal.pone.0114631
collection DOAJ
language English
format Article
sources DOAJ
author Weerachai Jaratlerdsiri
Janine Deakin
Ricardo M Godinez
Xueyan Shan
Daniel G Peterson
Sylvain Marthey
Eric Lyons
Fiona M McCarthy
Sally R Isberg
Damien P Higgins
Amanda Y Chong
John St John
Travis C Glenn
David A Ray
Jaime Gongora
spellingShingle Weerachai Jaratlerdsiri
Janine Deakin
Ricardo M Godinez
Xueyan Shan
Daniel G Peterson
Sylvain Marthey
Eric Lyons
Fiona M McCarthy
Sally R Isberg
Damien P Higgins
Amanda Y Chong
John St John
Travis C Glenn
David A Ray
Jaime Gongora
Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.
PLoS ONE
author_facet Weerachai Jaratlerdsiri
Janine Deakin
Ricardo M Godinez
Xueyan Shan
Daniel G Peterson
Sylvain Marthey
Eric Lyons
Fiona M McCarthy
Sally R Isberg
Damien P Higgins
Amanda Y Chong
John St John
Travis C Glenn
David A Ray
Jaime Gongora
author_sort Weerachai Jaratlerdsiri
title Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.
title_short Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.
title_full Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.
title_fullStr Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.
title_full_unstemmed Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.
title_sort comparative genome analyses reveal distinct structure in the saltwater crocodile mhc.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
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.
url https://doi.org/10.1371/journal.pone.0114631
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