Microbial Danger Signals Control Transcriptional Induction of Distinct MHC Class I L Lineage Genes in Atlantic Salmon

2020

Preprint

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.

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

MHC class I evolution; from Northern pike to salmonids

2020

Preprint

“…A structural investigation of L lineage sequences found them to be able to bind quite hydrophobic structures, possibly analogue to mammalian CD1 molecules [5]. Our understanding of the L gene function has since advanced with the study by Edholm and co-workers [23] showing that L lineage genes display different responses upon stimulation. Six Atlantic salmon L lineage genes were included in their study where Sasa-LIA responded to a single-stranded RNA virus but not when challenged with a bacteria.…”

Section: Z Lineage Evolutionmentioning

confidence: 99%

“…The L lineage molecules most likely binds hydrophobic ligands, and can be traced back to spotted gar, a species that separated from teleosts before the teleost speci c third whole genome duplication event (3WGD) [5]. Different Atlantic salmon L lineage genes were recently shown to vary in their response to pathogen stimulations [23], suggesting they have different roles in defence against pathogens.…”

Section: Introductionmentioning

confidence: 99%

MHC class I evolution; from Northern pike to salmonids

2020

Preprint

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.

“…The L lineage molecules most likely binds hydrophobic ligands, and can be traced back to spotted gar, a species that separated from teleosts before the teleost specific third whole genome duplication event (3WGD) [ 8 ]. Different Atlantic salmon L lineage genes were recently shown to vary in their response to pathogen stimulations [ 18 ], suggesting they have different roles in defence against pathogens.…”

Section: Introductionmentioning

confidence: 99%

MHC class I evolution; from Northern pike to salmonids

2021

BMC Ecol Evo

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.