MHC class I evolution; from Northern pike to salmonids

Genome Duplication ◽

Northern Pike ◽

Class I ◽

Specific Gene ◽

Whole Genome ◽

Gene Duplications ◽

Abstract Background: Salmonids are of major importance both as farmed and wild animals. With the changing environment comes changes in pathogenic pressures so understanding the immune system of all salmonid species is of essence. Major histocompatibility complex (MHC) genes are key players in the adaptive immune system signalling infection to responding T-cells populations. Classical MHC class I (MHCI) genes, defined by high polymorphism, broad expression patterns and peptide binding ability, have a key role in inducing immunity. In salmonids, the fourth whole genome duplication that occurred 94 million years ago has provided salmonids with duplicate MHCI regions, while Northern Pike, a basal sister clade to salmonids, represent a species which has not experienced this whole genome duplication. Results: Comparing the gene organization and evolution of MHC class I gene sequences in Northern pike versus salmonids displays a complex picture of how many of these genes evolved. Regional salmonid Ia and Ib Z lineage gene duplicates are not orthologs to the Northern pike Z lineage sequences. Instead, salmonids have experienced unique gene duplications in both duplicate regions as well as in the Salmo and Oncorhynchus branch. Species-specific gene duplications are even more pronounced for some L lineage genes. Conclusions: Although both Northern pike as well as salmonids have expanded their U and Z lineage genes, these gene duplications occurred separately in pike and in salmonids. However, the similarity between these duplications suggest the transposable machinery was present in a common ancestor. The salmonid MHCIa and MHCIb regions were formed during the 94 MYA since the split from pike and before the Oncorhynchus and Salmo branch separated. As seen in tetrapods, the non-classical U lineage genes are diversified duplicates of their classical counterpart. One MHCI lineage, the L lineage, experienced massive species-specific gene duplications after Oncorhynchus and Salmo split approximately 25 MYA. Based on what we currently know about L lineage genes, this large variation in number of L lineage genes also signals a large functional diversity in salmonids.

MHC class I evolution; from Northern pike to salmonids

10.21203/rs.3.rs-36819/v2 ◽

2020 ◽

Author(s):

Unni Grimholt ◽

Morten Lukacs

Keyword(s):

Immune System ◽

Mhc Class I ◽

Genome Duplication ◽

Northern Pike ◽

Class I ◽

Specific Gene ◽

Whole Genome ◽

Gene Duplications ◽

MHC class I evolution; from Northern pike to salmonids

10.21203/rs.3.rs-36819/v3 ◽

2020 ◽

Author(s):

Unni Grimholt ◽

Morten Lukacs

Keyword(s):

Immune System ◽

Mhc Class I ◽

Genome Duplication ◽

Northern Pike ◽

Class I ◽

Specific Gene ◽

Whole Genome ◽

Gene Duplications ◽

Abstract BackgroundSalmonids are of major importance both as farmed and wild animals. With the changing environment comes changes in pathogenic pressures so understanding the immune system of all salmonid species is of essence. Major histocompatibility complex (MHC) genes are key players in the adaptive immune system signalling infection to responding T-cells populations. Classical MHC class I (MHCI) genes, defined by high polymorphism, broad expression patterns and peptide binding ability, have a key role in inducing immunity. In salmonids, the fourth whole genome duplication that occurred 94 million years ago has provided salmonids with duplicate MHCI regions, while Northern Pike, a basal sister clade to salmonids, represent a species which has not experienced this whole genome duplication. ResultsComparing the gene organization and evolution of MHC class I gene sequences in Northern pike versus salmonids displays a complex picture of how many of these genes evolved. Regional salmonid Ia and Ib Z lineage gene duplicates are not orthologs to the Northern pike Z lineage sequences. Instead, salmonids have experienced unique gene duplications in both duplicate regions as well as in the Salmo and Oncorhynchus branch. Species-specific gene duplications are even more pronounced for some L lineage genes. ConclusionsAlthough both Northern pike as well as salmonids have expanded their U and Z lineage genes, these gene duplications occurred separately in pike and in salmonids. However, the similarity between these duplications suggest the transposable machinery was present in a common ancestor. The salmonid MHCIa and MHCIb regions were formed during the 94 MYA since the split from pike and before the Oncorhynchus and Salmo branch separated. As seen in tetrapods, the non-classical U lineage genes are diversified duplicates of their classical counterpart. One MHCI lineage, the L lineage, experienced massive species-specific gene duplications after Oncorhynchus and Salmo split approximately 25 MYA. Based on what we currently know about L lineage genes, this large variation in number of L lineage genes also signals a large functional diversity in salmonids.

MHC class I evolution; from Northern pike to salmonids

BMC Ecology and Evolution ◽

10.1186/s12862-020-01736-y ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

U. Grimholt ◽

M. Lukacs

Keyword(s):

Immune System ◽

Mhc Class I ◽

Genome Duplication ◽

Northern Pike ◽

Class I ◽

Specific Gene ◽

Whole Genome ◽

Gene Duplications ◽

Abstract Background Salmonids are of major importance both as farmed and wild animals. With the changing environment comes changes in pathogenic pressures so understanding the immune system of all salmonid species is of essence. Major histocompatibility complex (MHC) genes are key players in the adaptive immune system signalling infection to responding T-cells populations. Classical MHC class I (MHCI) genes, defined by high polymorphism, broad expression patterns and peptide binding ability, have a key role in inducing immunity. In salmonids, the fourth whole genome duplication that occurred 94 million years ago has provided salmonids with duplicate MHCI regions, while Northern Pike, a basal sister clade to salmonids, represent a species which has not experienced this whole genome duplication. Results Comparing the gene organization and evolution of MHC class I gene sequences in Northern pike versus salmonids displays a complex picture of how many of these genes evolved. Regional salmonid Ia and Ib Z lineage gene duplicates are not orthologs to the Northern pike Z lineage sequences. Instead, salmonids have experienced unique gene duplications in both duplicate regions as well as in the Salmo and Oncorhynchus branch. Species-specific gene duplications are even more pronounced for some L lineage genes. Conclusions Although both Northern pike as well as salmonids have expanded their U and Z lineage genes, these gene duplications occurred separately in pike and in salmonids. However, the similarity between these duplications suggest the transposable machinery was present in a common ancestor. The salmonid MHCIa and MHCIb regions were formed during the 94 MYA since the split from pike and before the Oncorhynchus and Salmo branch separated. As seen in tetrapods, the non-classical U lineage genes are diversified duplicates of their classical counterpart. One MHCI lineage, the L lineage, experienced massive species-specific gene duplications after Oncorhynchus and Salmo split approximately 25 MYA. Based on what we currently know about L lineage genes, this large variation in number of L lineage genes also signals a large functional diversity in salmonids.

MHC class I evolution; from Northern pike to salmonids

10.21203/rs.3.rs-36819/v1 ◽

2020 ◽

Author(s):

Unni Grimholt ◽

Morten Lukacs

Keyword(s):

Immune System ◽

Rural Communities ◽

Mhc Class I ◽

Northern Pike ◽

Gene Organization ◽

Class I ◽

Individual Species ◽

Specific Gene ◽

Gene Duplications ◽

Classical Counterpart

Abstract Background Salmonids are of major importance both as farmed and wild animals. The financial importance to aquacultural industry as well as to rural communities that profit from wild salmon fishing is substantial. With the changing environment comes changes in pathogenic pressures so understanding the immune system of all salmonid species is of essence. Major histocompatibility complex (MHC) genes are key players in the adaptive immune system signalling infection to responding T-cells populations. Their key role in inducing immunity and their link to disease resistance instigate studies on structure, function and evolution. Northern Pike, a basal sister clade to salmonids, represent a species which has not experienced the fourth salmonid specific whole genome duplication. Results Comparing the gene organization and evolution of MHC class I gene sequences in Northern pike versus salmonids displays a complex picture of how many of these genes evolved. Salmonid Ia and Ib Z lineage genes are not orthologs to the Northern pike Z lineage sequences. Instead, the salmonid genes have experienced unique gene duplications in the two duplicated regions as well as in the Salmo and Oncorhynchus branch. Potentially, transposase elements enabling these duplications were already present in the Northern pike Z lineage gene. Conclusions Although both Northern pike as well as salmonids have expanded their U and Z lineage genes, these gene duplications have occurred separately in pike and in a salmonid ancestor. However, the similarity between these duplications suggest the transposable machinery was present in a common ancestor. The salmonid MHCIa and MHCIb regions were mostly formed during the 80MYA since the split from pike and before the Oncorhynchus and Salmon branch separated. As seen in tetrapods, the non-classical U lineage genes are diversified duplicates of their classical counterpart. One MHCI lineage, the L lineage, experienced massive species-specific gene duplications after Oncorhynchus and Salmo split approximately 25 MYA. Based on what we currently know about L lineage genes, this diversity will most likely affect immune responses in individual species.

Reconstruction of the Carbohydrate 6-O Sulfotransferase Gene Family Evolution in Vertebrates Reveals Novel Member, CHST16, Lost in Amniotes

Genome Biology and Evolution ◽

10.1093/gbe/evz274 ◽

2019 ◽

Vol 12 (7) ◽

pp. 993-1012

Author(s):

Daniel Ocampo Daza ◽

Tatjana Haitina

Keyword(s):

Genome Duplication ◽

Phylogenetic Reconstruction ◽

Sulfated Polysaccharide ◽

Gene Family Evolution ◽

Vertebrate Evolution ◽

Specific Gene ◽

Whole Genome ◽

Gene Duplications ◽

First Time

Abstract Glycosaminoglycans are sulfated polysaccharide molecules, essential for many biological processes. The 6-O sulfation of glycosaminoglycans is carried out by carbohydrate 6-O sulfotransferases (C6OSTs), previously named Gal/GalNAc/GlcNAc 6-O sulfotransferases. Here, for the first time, we present a detailed phylogenetic reconstruction, analysis of gene synteny conservation and propose an evolutionary scenario for the C6OST family in major vertebrate groups, including mammals, birds, nonavian reptiles, amphibians, lobe-finned fishes, ray-finned fishes, cartilaginous fishes, and jawless vertebrates. The C6OST gene expansion likely started early in the chordate lineage, giving rise to four ancestral genes after the divergence of tunicates and before the emergence of extant vertebrates. The two rounds of whole-genome duplication in early vertebrate evolution (1R/2R) only contributed two additional C6OST subtype genes, increasing the vertebrate repertoire from four genes to six, divided into two branches. The first branch includes CHST1 and CHST3 as well as a previously unrecognized subtype, CHST16 that was lost in amniotes. The second branch includes CHST2, CHST7, and CHST5. Subsequently, local duplications of CHST5 gave rise to CHST4 in the ancestor of tetrapods, and to CHST6 in the ancestor of primates. The teleost-specific gene duplicates were identified for CHST1, CHST2, and CHST3 and are result of whole-genome duplication (3R) in the teleost lineage. We could also detect multiple, more recent lineage-specific duplicates. Thus, the vertebrate repertoire of C6OST genes has been shaped by gene duplications and gene losses at several stages of vertebrate evolution, with implications for the evolution of skeleton, nervous system, and cell–cell interactions.

Large scale gene duplication affected the European eel (Anguilla anguilla) after the 3R teleost duplication

10.1101/232918 ◽

2017 ◽

Cited By ~ 1

Author(s):

Christoffer Rozenfeld ◽

Jose Blanca ◽

Victor Gallego ◽

Víctor García-Carpintero ◽

Juan Germán Herranz-Jusdado ◽

...

Keyword(s):

Gene Duplication ◽

Large Scale ◽

Tandem Repeats ◽

Genome Duplication ◽

Genetic Material ◽

Specific Gene ◽

European Eel ◽

Whole Genome ◽

Gene Duplications

AbstractGenomic scale duplication of genes generates raw genetic material, which may facilitate new adaptations for the organism. Previous studies on eels have reported specific gene duplications, however a species-specific large-scale gene duplication has never before been proposed. In this study, we have assembled a de novo European eel transcriptome and the data show more than a thousand gene duplications that happened, according to a 4dTv analysis, after the teleost specific 3R whole genome duplication (WGD). The European eel has a complex and peculiar life cycle, which involves extensive migration, drastic habitat changes and metamorphoses, all of which could have been facilitated by the genes derived from this large-scale gene duplication.Of the paralogs created, those with a lower genetic distance are mostly found in tandem repeats, indicating that they are young segmental duplications. The older eel paralogs showed a different pattern, with more extensive synteny suggesting that a Whole Genome Duplication (WGD) event may have happened in the eel lineage. Furthermore, an enrichment analysis of eel specific paralogs further revealed GO-terms typically enriched after a WGD. Thus, this study, to the best of our knowledge, is the first to present evidence indicating an Anguillidae family specific large-scale gene duplication, which may include a 4R WGD.

Evolution and Expression of the Immune System of a Facultatively Anadromous Salmonid

Frontiers in Immunology ◽

10.3389/fimmu.2021.568729 ◽

2021 ◽

Vol 12 ◽

Author(s):

Thomas J. Colgan ◽

Peter A. Moran ◽

Louise C. Archer ◽

Robert Wynne ◽

Stephen A. Hutton ◽

...

Keyword(s):

Life Cycle ◽

Immune System ◽

Brown Trout ◽

Salmo Trutta ◽

Genome Duplication ◽

Immune Gene ◽

Whole Genome ◽

Gene Repertoire ◽

Immune Genes

Vertebrates have evolved a complex immune system required for the identification of and coordinated response to harmful pathogens. Migratory species spend periods of their life-cycle in more than one environment, and their immune system consequently faces a greater diversity of pathogens residing in different environments. In facultatively anadromous salmonids, individuals may spend parts of their life-cycle in freshwater and marine environments. For species such as the brown trout Salmo trutta, sexes differ in their life-histories with females more likely to migrate to sea while males are more likely to stay and complete their life-cycle in their natal river. Salmonids have also undergone a lineage-specific whole genome duplication event, which may provide novel immune innovations but our current understanding of the differences in salmonid immune expression between the sexes is limited. We characterized the brown trout immune gene repertoire, identifying a number of canonical immune genes in non-salmonid teleosts to be duplicated in S. trutta, with genes involved in innate and adaptive immunity. Through genome-wide transcriptional profiling (“RNA-seq”) of male and female livers to investigate sex differences in gene expression amplitude and alternative splicing, we identified immune genes as being generally male-biased in expression. Our study provides important insights into the evolutionary consequences of whole genome duplication events on the salmonid immune gene repertoire and how the sexes differ in constitutive immune expression.

The Genome Sequence of Alpine Megacarpaea delavayi Identifies Species-Specific Whole-Genome Duplication

Frontiers in Genetics ◽

10.3389/fgene.2020.00812 ◽

2020 ◽

Vol 11 ◽

Author(s):

Qiao Yang ◽

Hao Bi ◽

Wenjie Yang ◽

Ting Li ◽

Jiebei Jiang ◽

...

Keyword(s):

Genome Sequence ◽

Genome Duplication ◽

Whole Genome ◽

Fate of MHCII in salmonids following 4WGD

Immunogenetics ◽

10.1007/s00251-020-01190-6 ◽

2020 ◽

Cited By ~ 1

Author(s):

Unni Grimholt ◽

Morten Lukacs

Keyword(s):

Mhc Class Ii ◽

Genome Duplication ◽

Northern Pike ◽

Class Ii ◽

Whole Genome ◽

Clear Cut ◽

Mhc Genes ◽

Histocompatibility Complex ◽

Peptide Loading

AbstractMajor histocompatibility complex (MHC) genes are key players in the adaptive immunity providing a defense against invading pathogens. Although the basic structures are similar when comparing mammalian and teleost MHC class II (MHCII) molecules, there are also clear-cut differences. Based on structural requirements, the teleosts non-classical MHCII molecules do not comply with a function similar to the human HLA-DM and HLA-DO, i.e., assisting in peptide loading and editing of classical MHCII molecules. We have previously studied the evolution of teleost class II genes identifying various lineages and tracing their phylogenetic occurrence back to ancient ray-finned fishes. We found no syntenic MHCII regions shared between cyprinids, salmonids, and neoteleosts, suggesting regional instabilities. Salmonids have experienced a unique whole genome duplication 94 million years ago, providing them with the opportunity to experiment with gene duplicates. Many salmonid genomes have recently become available, and here we set out to investigate how MHCII has evolved in salmonids using Northern pike as a diploid sister phyla, that split from the salmonid lineage prior to the fourth whole genome duplication (4WGD) event. We identified 120 MHCII genes in pike and salmonids, ranging from 11 to 20 genes per species analyzed where DB-group genes had the most expansions. Comparing the MHC of Northern pike with that of Atlantic salmon and other salmonids species provides a tale of gene loss, translocations, and genome rearrangements.