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The genomic architecture of the passerine MHC region : High repeat content and contrasting evolutionary histories of single copy and tandemly duplicated MHC genes

Westerdahl, Helena LU ; Mellinger, Samantha LU ; Sigeman, Hanna LU ; Kutschera, Verena E. ; Proux-Wéra, Estelle ; Lundberg, Max LU ; Weissensteiner, Matthias ; Churcher, Allison ; Bunikis, Ignas and Hansson, Bengt LU orcid , et al. (2022) In Molecular Ecology Resources 22(6). p.2379-2395
Abstract

The major histocompatibility complex (MHC) is of central importance to the immune system, and an optimal MHC diversity is believed to maximize pathogen elimination. Birds show substantial variation in MHC diversity, ranging from few genes in most bird orders to very many genes in passerines. Our understanding of the evolutionary trajectories of the MHC in passerines is hampered by lack of data on genomic organization. Therefore, we assembled and annotated the MHC genomic region of the great reed warbler (Acrocephalus arundinaceus), using long-read sequencing and optical mapping. The MHC region is large (>5.5 Mb), characterized by structural changes compared to hitherto investigated bird orders and shows higher repeat content than the... (More)

The major histocompatibility complex (MHC) is of central importance to the immune system, and an optimal MHC diversity is believed to maximize pathogen elimination. Birds show substantial variation in MHC diversity, ranging from few genes in most bird orders to very many genes in passerines. Our understanding of the evolutionary trajectories of the MHC in passerines is hampered by lack of data on genomic organization. Therefore, we assembled and annotated the MHC genomic region of the great reed warbler (Acrocephalus arundinaceus), using long-read sequencing and optical mapping. The MHC region is large (>5.5 Mb), characterized by structural changes compared to hitherto investigated bird orders and shows higher repeat content than the genome average. These features were supported by analyses in three additional passerines. MHC genes in passerines are found in two different chromosomal arrangements, either as single copy MHC genes located among non-MHC genes, or as tandemly duplicated tightly linked MHC genes. Some single copy MHC genes are old and putative orthologues among species. In contrast tandemly duplicated MHC genes are monophyletic within species and have evolved by simultaneous gene duplication of several MHC genes. Structural differences in the MHC genomic region among bird orders seem substantial compared to mammals and have possibly been fuelled by clade-specific immune system adaptations. Our study provides methodological guidance in characterizing complex genomic regions, constitutes a resource for MHC research in birds, and calls for a revision of the general belief that avian MHC has a conserved gene order and small size compared to mammals.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
gene order, major histocompatibility complex (MHC), Passeriformes, repeats, single copy genes, tandemly duplicated genes
in
Molecular Ecology Resources
volume
22
issue
6
pages
2379 - 2395
publisher
Wiley-Blackwell
external identifiers
  • pmid:35348299
  • scopus:85127943929
ISSN
1755-098X
DOI
10.1111/1755-0998.13614
language
English
LU publication?
yes
id
f6501340-f78b-41af-8882-a35da198abfe
date added to LUP
2022-06-17 14:15:26
date last changed
2024-05-02 13:36:21
@article{f6501340-f78b-41af-8882-a35da198abfe,
  abstract     = {{<p>The major histocompatibility complex (MHC) is of central importance to the immune system, and an optimal MHC diversity is believed to maximize pathogen elimination. Birds show substantial variation in MHC diversity, ranging from few genes in most bird orders to very many genes in passerines. Our understanding of the evolutionary trajectories of the MHC in passerines is hampered by lack of data on genomic organization. Therefore, we assembled and annotated the MHC genomic region of the great reed warbler (Acrocephalus arundinaceus), using long-read sequencing and optical mapping. The MHC region is large (&gt;5.5 Mb), characterized by structural changes compared to hitherto investigated bird orders and shows higher repeat content than the genome average. These features were supported by analyses in three additional passerines. MHC genes in passerines are found in two different chromosomal arrangements, either as single copy MHC genes located among non-MHC genes, or as tandemly duplicated tightly linked MHC genes. Some single copy MHC genes are old and putative orthologues among species. In contrast tandemly duplicated MHC genes are monophyletic within species and have evolved by simultaneous gene duplication of several MHC genes. Structural differences in the MHC genomic region among bird orders seem substantial compared to mammals and have possibly been fuelled by clade-specific immune system adaptations. Our study provides methodological guidance in characterizing complex genomic regions, constitutes a resource for MHC research in birds, and calls for a revision of the general belief that avian MHC has a conserved gene order and small size compared to mammals.</p>}},
  author       = {{Westerdahl, Helena and Mellinger, Samantha and Sigeman, Hanna and Kutschera, Verena E. and Proux-Wéra, Estelle and Lundberg, Max and Weissensteiner, Matthias and Churcher, Allison and Bunikis, Ignas and Hansson, Bengt and Wolf, Jochen B.W. and Strandh, Maria}},
  issn         = {{1755-098X}},
  keywords     = {{gene order; major histocompatibility complex (MHC); Passeriformes; repeats; single copy genes; tandemly duplicated genes}},
  language     = {{eng}},
  number       = {{6}},
  pages        = {{2379--2395}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Molecular Ecology Resources}},
  title        = {{The genomic architecture of the passerine MHC region : High repeat content and contrasting evolutionary histories of single copy and tandemly duplicated MHC genes}},
  url          = {{http://dx.doi.org/10.1111/1755-0998.13614}},
  doi          = {{10.1111/1755-0998.13614}},
  volume       = {{22}},
  year         = {{2022}},
}