Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the tuatara sphenodon punctatus

Hilary C Miller, Denis O’Meally, Tariq EZAZ, Chris Amemiya, Jennifer Graves, Scott Edwards

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Major histocompatibility complex (MHC) genes are a central component of the vertebrate immune system and usually exist in a single genomic region. However, considerable differences in MHC organization and size exist between different vertebrate lineages. Reptiles occupy a key evolutionary position for understanding how variation in MHC structure evolved in vertebrates, but information on the structure of the MHC region in reptiles is limited. In this study, we investigate the organization and cytogenetic location of MHC genes in the tuatara (Sphenodon punctatus), the sole extant representative of the early-diverging reptilian order Rhynchocephalia. Sequencing and mapping of 12 clones containing class I and II MHC genes from a bacterial artificial chromosome library indicated that the core MHC region is located on chromosome 13q. However, duplication and translocation of MHC genes outside of thecore region was evident, because additional class I MHC genes were located on chromosome 4p. We found a total of seven class I sequences and 11 class II ß sequences, with evidence for duplication and pseudogenization of genes within the tuatara lineage. The tuatara MHC is characterized by high repeat content and low gene density compared with other species and we found no antigen processing or MHC framework genes on the MHC gene-containing clones. Our findings indicate substantial differences in MHC organization in tuatara compared with mammalian and avian MHCs and highlight the dynamic nature of the MHC. Further sequencing and annotation of tuatara and other reptile MHCs will determine if the tuatara MHC is representative of nonavian reptiles in general.
Original languageEnglish
Pages (from-to)1439-1451
Number of pages13
JournalG3: Genes, Genomes, Genetics
Volume5
Issue number7
DOIs
Publication statusPublished - 2015
Externally publishedYes

Fingerprint

Reptiles
Major Histocompatibility Complex
Chromosomes
Genes
Vertebrates
Clone Cells
Bacterial Artificial Chromosomes
Gene Duplication
Antigen Presentation
Cytogenetics

Cite this

Miller, Hilary C ; O’Meally, Denis ; EZAZ, Tariq ; Amemiya, Chris ; Graves, Jennifer ; Edwards, Scott. / Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the tuatara sphenodon punctatus. In: G3: Genes, Genomes, Genetics. 2015 ; Vol. 5, No. 7. pp. 1439-1451.
@article{ee0e4777c85b4619a3493ab62c8a029e,
title = "Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the tuatara sphenodon punctatus",
abstract = "Major histocompatibility complex (MHC) genes are a central component of the vertebrate immune system and usually exist in a single genomic region. However, considerable differences in MHC organization and size exist between different vertebrate lineages. Reptiles occupy a key evolutionary position for understanding how variation in MHC structure evolved in vertebrates, but information on the structure of the MHC region in reptiles is limited. In this study, we investigate the organization and cytogenetic location of MHC genes in the tuatara (Sphenodon punctatus), the sole extant representative of the early-diverging reptilian order Rhynchocephalia. Sequencing and mapping of 12 clones containing class I and II MHC genes from a bacterial artificial chromosome library indicated that the core MHC region is located on chromosome 13q. However, duplication and translocation of MHC genes outside of thecore region was evident, because additional class I MHC genes were located on chromosome 4p. We found a total of seven class I sequences and 11 class II {\ss} sequences, with evidence for duplication and pseudogenization of genes within the tuatara lineage. The tuatara MHC is characterized by high repeat content and low gene density compared with other species and we found no antigen processing or MHC framework genes on the MHC gene-containing clones. Our findings indicate substantial differences in MHC organization in tuatara compared with mammalian and avian MHCs and highlight the dynamic nature of the MHC. Further sequencing and annotation of tuatara and other reptile MHCs will determine if the tuatara MHC is representative of nonavian reptiles in general.",
author = "Miller, {Hilary C} and Denis O’Meally and Tariq EZAZ and Chris Amemiya and Jennifer Graves and Scott Edwards",
year = "2015",
doi = "10.1534/g3.115.017467",
language = "English",
volume = "5",
pages = "1439--1451",
journal = "G3: Genes, Genomes, Genetics",
issn = "2160-1836",
publisher = "Genetics Society of America",
number = "7",

}

Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the tuatara sphenodon punctatus. / Miller, Hilary C; O’Meally, Denis; EZAZ, Tariq; Amemiya, Chris; Graves, Jennifer; Edwards, Scott.

In: G3: Genes, Genomes, Genetics, Vol. 5, No. 7, 2015, p. 1439-1451.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the tuatara sphenodon punctatus

AU - Miller, Hilary C

AU - O’Meally, Denis

AU - EZAZ, Tariq

AU - Amemiya, Chris

AU - Graves, Jennifer

AU - Edwards, Scott

PY - 2015

Y1 - 2015

N2 - Major histocompatibility complex (MHC) genes are a central component of the vertebrate immune system and usually exist in a single genomic region. However, considerable differences in MHC organization and size exist between different vertebrate lineages. Reptiles occupy a key evolutionary position for understanding how variation in MHC structure evolved in vertebrates, but information on the structure of the MHC region in reptiles is limited. In this study, we investigate the organization and cytogenetic location of MHC genes in the tuatara (Sphenodon punctatus), the sole extant representative of the early-diverging reptilian order Rhynchocephalia. Sequencing and mapping of 12 clones containing class I and II MHC genes from a bacterial artificial chromosome library indicated that the core MHC region is located on chromosome 13q. However, duplication and translocation of MHC genes outside of thecore region was evident, because additional class I MHC genes were located on chromosome 4p. We found a total of seven class I sequences and 11 class II ß sequences, with evidence for duplication and pseudogenization of genes within the tuatara lineage. The tuatara MHC is characterized by high repeat content and low gene density compared with other species and we found no antigen processing or MHC framework genes on the MHC gene-containing clones. Our findings indicate substantial differences in MHC organization in tuatara compared with mammalian and avian MHCs and highlight the dynamic nature of the MHC. Further sequencing and annotation of tuatara and other reptile MHCs will determine if the tuatara MHC is representative of nonavian reptiles in general.

AB - Major histocompatibility complex (MHC) genes are a central component of the vertebrate immune system and usually exist in a single genomic region. However, considerable differences in MHC organization and size exist between different vertebrate lineages. Reptiles occupy a key evolutionary position for understanding how variation in MHC structure evolved in vertebrates, but information on the structure of the MHC region in reptiles is limited. In this study, we investigate the organization and cytogenetic location of MHC genes in the tuatara (Sphenodon punctatus), the sole extant representative of the early-diverging reptilian order Rhynchocephalia. Sequencing and mapping of 12 clones containing class I and II MHC genes from a bacterial artificial chromosome library indicated that the core MHC region is located on chromosome 13q. However, duplication and translocation of MHC genes outside of thecore region was evident, because additional class I MHC genes were located on chromosome 4p. We found a total of seven class I sequences and 11 class II ß sequences, with evidence for duplication and pseudogenization of genes within the tuatara lineage. The tuatara MHC is characterized by high repeat content and low gene density compared with other species and we found no antigen processing or MHC framework genes on the MHC gene-containing clones. Our findings indicate substantial differences in MHC organization in tuatara compared with mammalian and avian MHCs and highlight the dynamic nature of the MHC. Further sequencing and annotation of tuatara and other reptile MHCs will determine if the tuatara MHC is representative of nonavian reptiles in general.

U2 - 10.1534/g3.115.017467

DO - 10.1534/g3.115.017467

M3 - Article

VL - 5

SP - 1439

EP - 1451

JO - G3: Genes, Genomes, Genetics

JF - G3: Genes, Genomes, Genetics

SN - 2160-1836

IS - 7

ER -