MHC architecture in amphibians - ancestral reconstruction, gene rearrangements and duplication patterns.

Amphibians Copy number variation Genomic data MHC architecture Macroevolution Major Histocompatibility Complex

Journal

Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707

Informations de publication

Date de publication:
12 May 2023
Historique:
received: 06 12 2022
revised: 29 03 2023
accepted: 02 05 2023
medline: 12 5 2023
pubmed: 12 5 2023
entrez: 12 5 2023
Statut: aheadofprint

Résumé

The hypervariable major histocompatibility complex (MHC) is a crucial component of vertebrate adaptive immunity, but large-scale studies on MHC macroevolution in non-model vertebrates have long been constrained by methodological limitations. Here, we used rapidly accumulating genomic data to reconstruct macroevolution of the MHC region in amphibians. We retrieved contigs containing the MHC region from genome assemblies of 32 amphibian species and examined major structural rearrangements, duplication patterns and gene structure across the amphibian phylogeny. Based on the few available caecilian and urodele genomes we showed that the structure of ancestral MHC region in amphibians was probably relatively simple and compact, with a close physical linkage between MHC-I and MHC-II regions. This ancestral MHC architecture was generally conserved in anurans, although the evolution of class I subregion proceeded towards more extensive duplication and rapid expansion of gene copy number, providing evidence for dynamic evolutionary trajectories. Although in anurans we recorded tandems of duplicated MHC-I genes outside the core subregion, our phylogenetic analyses of MHC-I sequences provided little support for an expansion of nonclassical MHC-Ib genes across amphibian families. Finally, we found that intronic regions of amphibian classical MHC genes were much longer when compared to other tetrapod lineages (birds and mammals), which could partly be driven by the expansion of genome size. Our study reveals novel evolutionary patterns of the MHC region in amphibians and provides a comprehensive framework for further studies on the MHC macroevolution across vertebrates.

Identifiants

pubmed: 37170911
pii: 7160678
doi: 10.1093/gbe/evad079
pmc: PMC10210626
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

Références

Immunol Rev. 2002 Dec;190:69-85
pubmed: 12493007
Ecol Evol. 2019 Jun 14;9(13):7861-7874
pubmed: 31346446
Genome Biol Evol. 2012;4(10):1033-43
pubmed: 22930760
Nat Ecol Evol. 2018 May;2(5):850-858
pubmed: 29581588
Proc Natl Acad Sci U S A. 2018 Apr 24;115(17):E4023-E4031
pubmed: 29610296
Immunogenetics. 2003 Dec;55(9):605-14
pubmed: 14608490
Annu Rev Immunol. 2018 Apr 26;36:383-409
pubmed: 29677478
Heredity (Edinb). 2012 Sep;109(3):146-55
pubmed: 22549517
Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7799-806
pubmed: 9223266
Nature. 1999 Oct 28;401(6756):923-5
pubmed: 10553909
Evolution. 2018 Jun;72(6):1278-1293
pubmed: 29665025
Immunogenetics. 2021 Oct;73(5):405-417
pubmed: 33978784
BMC Genomics. 2009 Jul 14;10:310
pubmed: 19602235
BMC Genomics. 2012 Oct 15;13:553
pubmed: 23066932
Nature. 2021 Jul;595(7868):501-510
pubmed: 34290426
Nat Rev Immunol. 2012 Jul 13;12(8):557-69
pubmed: 22790179
Trends Genet. 2020 Apr;36(4):298-311
pubmed: 32044115
Genet Med. 2018 Jan;20(1):159-163
pubmed: 28640241
J Immunol. 2006 Mar 15;176(6):3674-85
pubmed: 16517736
Semin Immunol. 1994 Dec;6(6):411-24
pubmed: 7654997
Nucleic Acids Res. 2020 Jan 8;48(D1):D948-D955
pubmed: 31667505
Immunology. 2017 Feb;150(2):127-138
pubmed: 27395034
Immunol Rev. 2002 Dec;190:95-122
pubmed: 12493009
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Syst Biol. 2021 Jan 1;70(1):49-66
pubmed: 32359157
Immunogenetics. 1988;27(4):273-80
pubmed: 2894354
PLoS Biol. 2006 Mar;4(3):e46
pubmed: 16435885
J Immunol. 1986 Dec 15;137(12):3891-9
pubmed: 3537126
Nature. 2020 Aug;584(7821):403-409
pubmed: 32760000
J Immunol. 2021 Aug 1;207(3):824-836
pubmed: 34301841
Evolution. 2022 Oct;76(10):2436-2449
pubmed: 36000494
Nat Commun. 2021 Jul 23;12(1):4489
pubmed: 34301952
Nature. 2011 Aug 10;477(7363):207-10
pubmed: 21832995
J Immunol. 2011 Jan 1;186(1):372-81
pubmed: 21115732
Mol Biol Evol. 2020 Jan 1;37(1):291-294
pubmed: 31432070
Nature. 2021 Apr;592(7856):737-746
pubmed: 33911273
Proc Natl Acad Sci U S A. 2013 Aug 27;110(35):14342-7
pubmed: 23940320
Science. 2020 Sep 25;369(6511):1608-1615
pubmed: 32732279
Nature. 2018 Feb 1;554(7690):50-55
pubmed: 29364872
Eur J Immunol. 1999 Sep;29(9):2897-907
pubmed: 10508264
Dev Comp Immunol. 2014 Feb;42(2):311-22
pubmed: 24135718
Cell Mol Life Sci. 2014 Dec;71(24):4763-80
pubmed: 25117267
Gigascience. 2019 Sep 1;8(9):
pubmed: 31544214
Cell. 2018 Sep 6;174(6):1586-1598.e12
pubmed: 30100188
Philos Trans R Soc Lond B Biol Sci. 2015 Sep 26;370(1678):20140331
pubmed: 26323762
Nat Genet. 2016 Oct;48(10):1204-10
pubmed: 27548311
Nature. 2021 Apr;592(7856):756-762
pubmed: 33408411
Genome Biol Evol. 2021 Feb 3;13(2):
pubmed: 33501944
Annu Rev Immunol. 2013;31:529-61
pubmed: 23298204
Integr Zool. 2015 Sep;10(5):465-81
pubmed: 26037662
Mol Ecol. 2021 Dec;30(23):6072-6086
pubmed: 34137092
Immunogenetics. 2014 Oct;66(9-10):513-23
pubmed: 24898512
J Immunol. 2019 Oct 1;203(7):1882-1896
pubmed: 31492741
Genome Res. 2003 Jun;13(6A):1169-79
pubmed: 12743023
Front Immunol. 2019 Apr 04;10:696
pubmed: 31019512
Mol Biol Evol. 2021 Oct 27;38(11):5092-5106
pubmed: 34375431
BMC Genomics. 2014 Mar 06;15:180
pubmed: 24602261
Adv Cancer Res. 2001;83:117-58
pubmed: 11665717
G3 (Bethesda). 2015 May 07;5(7):1439-51
pubmed: 25953959
EMBO J. 1993 Nov;12(11):4385-96
pubmed: 8223448
Cytogenet Genome Res. 2015;145(3-4):283-301
pubmed: 26279165
Bioinformatics. 2020 May 1;36(9):2896-2898
pubmed: 31971576
Immunogenetics. 2015 Apr;67(4):259-64
pubmed: 25737310
BMC Genomics. 2011 Aug 19;12:421
pubmed: 21854592
Front Genet. 2022 Feb 17;13:823686
pubmed: 35251132
Nature. 2023 Feb;614(7946):102-107
pubmed: 36697827
BMC Genomics. 2019 Jun 11;20(1):479
pubmed: 31185912
PLoS Comput Biol. 2019 May 16;15(5):e1007015
pubmed: 31095555
J Mol Evol. 1999 Sep;49(3):376-84
pubmed: 10473779
Immunol Rev. 1998 Dec;166:221-30
pubmed: 9914915
Proc Natl Acad Sci U S A. 2021 Apr 13;118(15):
pubmed: 33827918
Proc Natl Acad Sci U S A. 1989 Feb;86(3):958-62
pubmed: 2492668
Nature. 2016 Oct 19;538(7625):336-343
pubmed: 27762356
Front Genet. 2022 Mar 02;13:829891
pubmed: 35309138
Mol Ecol Resour. 2022 Aug;22(6):2379-2395
pubmed: 35348299
Front Genet. 2022 Nov 08;13:979746
pubmed: 36425073
Genome Biol Evol. 2021 Feb 3;13(2):
pubmed: 33367721
Nat Rev Immunol. 2018 Jul;18(7):438-453
pubmed: 29556016

Auteurs

Ke He (K)

College of Animal Science and Technology, College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Hangzhou, China.

Wiesław Babik (W)

Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland.

Mateusz Majda (M)

Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland.

Piotr Minias (P)

Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland.

Classifications MeSH