U Grimholt1, M Lukacs2. 1. Fish Research Group, Norwegian Veterinary Institute, Ullevaalsveien 68, 0454, Oslo, Norway. Unni.Grimholt@vetinst.no. 2. Fish Research Group, Norwegian Veterinary Institute, Ullevaalsveien 68, 0454, Oslo, Norway.
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.
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.
Authors: Bastiaan Star; Alexander J Nederbragt; Sissel Jentoft; Unni Grimholt; Martin Malmstrøm; Tone F Gregers; Trine B Rounge; Jonas Paulsen; Monica H Solbakken; Animesh Sharma; Ola F Wetten; Anders Lanzén; Roger Winer; James Knight; Jan-Hinnerk Vogel; Bronwen Aken; Oivind Andersen; Karin Lagesen; Ave Tooming-Klunderud; Rolf B Edvardsen; Kirubakaran G Tina; Mari Espelund; Chirag Nepal; Christopher Previti; Bård Ove Karlsen; Truls Moum; Morten Skage; Paul R Berg; Tor Gjøen; Heiner Kuhl; Jim Thorsen; Ketil Malde; Richard Reinhardt; Lei Du; Steinar D Johansen; Steve Searle; Sigbjørn Lien; Frank Nilsen; Inge Jonassen; Stig W Omholt; Nils Chr Stenseth; Kjetill S Jakobsen Journal: Nature Date: 2011-08-10 Impact factor: 49.962
Authors: Sean C McConnell; Kyle M Hernandez; Dustin J Wcisel; Ross N Kettleborough; Derek L Stemple; Jeffrey A Yoder; Jorge Andrade; Jill L O de Jong Journal: Proc Natl Acad Sci U S A Date: 2016-08-04 Impact factor: 11.205
Authors: B P Shum; L Guethlein; L R Flodin; M A Adkison; R P Hedrick; R B Nehring; R J Stet; C Secombes; P Parham Journal: J Immunol Date: 2001-03-01 Impact factor: 5.422
Authors: Unni Grimholt; Kentaro Tsukamoto; Teruo Azuma; Jong Leong; Ben F Koop; Johannes M Dijkstra Journal: BMC Evol Biol Date: 2015-03-06 Impact factor: 3.260
Authors: Kris A Christensen; Jong S Leong; Dionne Sakhrani; Carlo A Biagi; David R Minkley; Ruth E Withler; Eric B Rondeau; Ben F Koop; Robert H Devlin Journal: PLoS One Date: 2018-04-05 Impact factor: 3.240