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Identification and characterisation of a novel immune-type receptor (NITR) gene cluster in the European sea bass, Dicentrarchus labrax, reveals recurrent gene expansion and diversification by positive selection.

Ferraresso S, Kuhl H, Milan M, Ritchie DW, Secombes CJ, Reinhardt R, Bargelloni L - Immunogenetics (2009)

Bottom Line: Sea bass NITR genes maintain the three major genomic organisations that appear to be essentially conserved among fish species along with new features presumably involving processes of intron loss, exon deletion and acquisition of new exons.Comparative and evolutionary analyses suggest that these receptors have evolved following a "birth-and-death" model of gene evolution in which duplication events together with lineage-specific gain and loss of individual members contributed to the rapid diversification of individual gene families.In this study, we demonstrate that species-specific gene expansions provide the raw material for diversifying, positive Darwinian selection favouring the evolution of a highly diverse array of molecules.

View Article: PubMed Central - PubMed

Affiliation: Department of Public Health, Comparative Pathology and Veterinary Hygiene, Faculty of Veterinary Medicine, University of Padova, Viale dell'Università 16, 35020 Legnaro, Italy. serena.ferraresso@unipd.it

ABSTRACT
In the last decade, a new gene family encoding non-rearranging receptors, called novel immune-type receptors (NITRs), has been discovered in teleost fish. NITRs belong to the immunoglobulin superfamily and represent an extraordinarily divergent and rapidly evolving gene complex. Genomic analysis of a region spanning 270 kb led to the discovery of a NITR gene cluster in the European sea bass (Dicentrarchus labrax). In total, 27 NITR genes and three putative pseudogenes, organised in a tandemly arrayed cluster, were identified. Sea bass NITR genes maintain the three major genomic organisations that appear to be essentially conserved among fish species along with new features presumably involving processes of intron loss, exon deletion and acquisition of new exons. Comparative and evolutionary analyses suggest that these receptors have evolved following a "birth-and-death" model of gene evolution in which duplication events together with lineage-specific gain and loss of individual members contributed to the rapid diversification of individual gene families. In this study, we demonstrate that species-specific gene expansions provide the raw material for diversifying, positive Darwinian selection favouring the evolution of a highly diverse array of molecules.

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The synteny of sea bass NITR cluster is conserved in zebrafish, medaka and stickleback. Comparison of the European sea bass NITR gene cluster with the syntenic regions of zebrafish, medaka and stickleback. Genes (boxes) and the distances between them are not to scale
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Fig6: The synteny of sea bass NITR cluster is conserved in zebrafish, medaka and stickleback. Comparison of the European sea bass NITR gene cluster with the syntenic regions of zebrafish, medaka and stickleback. Genes (boxes) and the distances between them are not to scale

Mentions: A comparative genomic analysis was carried out to identify genomic regions showing significant matches with sea bass NITRs. Regions isolated both in zebrafish and medaka correspond to those already described by Yoder and et al. (2002, 2004) and by Desai et al. (2008). In addition, our analysis identified the putative sea bass orthologues of FXR2, RBM4 and TRAF2 binding protein, three genes located in close proximity to NITR gene clusters in medaka chr. 18 and zebrafish chr. 7 (Fig. 6). A NITR gene cluster, situated in the stickleback chromosome/group IV has been already reported (Desai et al. 2008). In the present study, an additional NITR gene complex was found spanning three contigs (contig_7245-7247, ENSEMBL release 54) on G. aculeatus group VII. This cluster encompasses a region of ?250 kb and comprises at least 24 NITRs showing V and I domains encoded either by one or two exons (data not shown). Genes encoding RBM4, FXR2 and TRAF2-binding protein homologous were also found at the 3? of this region, indicating that the sea bass NITR cluster and the stickleback cluster located in group VII share conserved synteny along with those already reported on medaka chr. 18 and zebrafish chr. 7 (Fig. 6).Fig. 6


Identification and characterisation of a novel immune-type receptor (NITR) gene cluster in the European sea bass, Dicentrarchus labrax, reveals recurrent gene expansion and diversification by positive selection.

Ferraresso S, Kuhl H, Milan M, Ritchie DW, Secombes CJ, Reinhardt R, Bargelloni L - Immunogenetics (2009)

The synteny of sea bass NITR cluster is conserved in zebrafish, medaka and stickleback. Comparison of the European sea bass NITR gene cluster with the syntenic regions of zebrafish, medaka and stickleback. Genes (boxes) and the distances between them are not to scale
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2921055&req=5

Fig6: The synteny of sea bass NITR cluster is conserved in zebrafish, medaka and stickleback. Comparison of the European sea bass NITR gene cluster with the syntenic regions of zebrafish, medaka and stickleback. Genes (boxes) and the distances between them are not to scale
Mentions: A comparative genomic analysis was carried out to identify genomic regions showing significant matches with sea bass NITRs. Regions isolated both in zebrafish and medaka correspond to those already described by Yoder and et al. (2002, 2004) and by Desai et al. (2008). In addition, our analysis identified the putative sea bass orthologues of FXR2, RBM4 and TRAF2 binding protein, three genes located in close proximity to NITR gene clusters in medaka chr. 18 and zebrafish chr. 7 (Fig. 6). A NITR gene cluster, situated in the stickleback chromosome/group IV has been already reported (Desai et al. 2008). In the present study, an additional NITR gene complex was found spanning three contigs (contig_7245-7247, ENSEMBL release 54) on G. aculeatus group VII. This cluster encompasses a region of ?250 kb and comprises at least 24 NITRs showing V and I domains encoded either by one or two exons (data not shown). Genes encoding RBM4, FXR2 and TRAF2-binding protein homologous were also found at the 3? of this region, indicating that the sea bass NITR cluster and the stickleback cluster located in group VII share conserved synteny along with those already reported on medaka chr. 18 and zebrafish chr. 7 (Fig. 6).Fig. 6

Bottom Line: Sea bass NITR genes maintain the three major genomic organisations that appear to be essentially conserved among fish species along with new features presumably involving processes of intron loss, exon deletion and acquisition of new exons.Comparative and evolutionary analyses suggest that these receptors have evolved following a "birth-and-death" model of gene evolution in which duplication events together with lineage-specific gain and loss of individual members contributed to the rapid diversification of individual gene families.In this study, we demonstrate that species-specific gene expansions provide the raw material for diversifying, positive Darwinian selection favouring the evolution of a highly diverse array of molecules.

View Article: PubMed Central - PubMed

Affiliation: Department of Public Health, Comparative Pathology and Veterinary Hygiene, Faculty of Veterinary Medicine, University of Padova, Viale dell'Università 16, 35020 Legnaro, Italy. serena.ferraresso@unipd.it

ABSTRACT
In the last decade, a new gene family encoding non-rearranging receptors, called novel immune-type receptors (NITRs), has been discovered in teleost fish. NITRs belong to the immunoglobulin superfamily and represent an extraordinarily divergent and rapidly evolving gene complex. Genomic analysis of a region spanning 270 kb led to the discovery of a NITR gene cluster in the European sea bass (Dicentrarchus labrax). In total, 27 NITR genes and three putative pseudogenes, organised in a tandemly arrayed cluster, were identified. Sea bass NITR genes maintain the three major genomic organisations that appear to be essentially conserved among fish species along with new features presumably involving processes of intron loss, exon deletion and acquisition of new exons. Comparative and evolutionary analyses suggest that these receptors have evolved following a "birth-and-death" model of gene evolution in which duplication events together with lineage-specific gain and loss of individual members contributed to the rapid diversification of individual gene families. In this study, we demonstrate that species-specific gene expansions provide the raw material for diversifying, positive Darwinian selection favouring the evolution of a highly diverse array of molecules.

Show MeSH