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Whole-genome duplication and the functional diversification of teleost fish hemoglobins.

ABSTRACT: Subsequent to the two rounds of whole-genome duplication that occurred in the common ancestor of vertebrates, a third genome duplication occurred in the stem lineage of teleost fishes. This teleost-specific genome duplication (TGD) is thought to have provided genetic raw materials for the physiological, morphological, and behavioral diversification of this highly speciose group. The extreme physiological versatility of teleost fish is manifest in their diversity of blood-gas transport traits, which reflects the myriad solutions that have evolved to maintain tissue O(2) delivery in the face of changing metabolic demands and environmental O(2) availability during different ontogenetic stages. During the course of development, regulatory changes in blood-O(2) transport are mediated by the expression of multiple, functionally distinct hemoglobin (Hb) isoforms that meet the particular O(2)-transport challenges encountered by the developing embryo or fetus (in viviparous or oviparous species) and in free-swimming larvae and adults. The main objective of the present study was to assess the relative contributions of whole-genome duplication, large-scale segmental duplication, and small-scale gene duplication in producing the extraordinary functional diversity of teleost Hbs. To accomplish this, we integrated phylogenetic reconstructions with analyses of conserved synteny to characterize the genomic organization and evolutionary history of the globin gene clusters of teleosts. These results were then integrated with available experimental data on functional properties and developmental patterns of stage-specific gene expression. Our results indicate that multiple ?- and ?-globin genes were present in the common ancestor of gars (order Lepisoteiformes) and teleosts. The comparative genomic analysis revealed that teleosts possess a dual set of TGD-derived globin gene clusters, each of which has undergone lineage-specific changes in gene content via repeated duplication and deletion events. Phylogenetic reconstructions revealed that paralogous genes convergently evolved similar functional properties in different teleost lineages. Consistent with other recent studies of globin gene family evolution in vertebrates, our results revealed evidence for repeated evolutionary transitions in the developmental regulation of Hb synthesis.

SUBMITTER: Opazo JC

PROVIDER: S-EPMC3525417 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Whole-genome duplication and the functional diversification of teleost fish hemoglobins.

Opazo Juan C JC Butts G Tyler GT Nery Mariana F MF Storz Jay F JF Hoffmann Federico G FG

Molecular biology and evolution 20120904 1

Subsequent to the two rounds of whole-genome duplication that occurred in the common ancestor of vertebrates, a third genome duplication occurred in the stem lineage of teleost fishes. This teleost-specific genome duplication (TGD) is thought to have provided genetic raw materials for the physiological, morphological, and behavioral diversification of this highly speciose group. The extreme physiological versatility of teleost fish is manifest in their diversity of blood-gas transport traits, wh ...[more]

PMID: 22949522

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Project description:BACKGROUND:Teleost radiation in the oceans required specific physiological adaptations in eggs and early embryos to survive in the hyper-osmotic seawater. Investigating the evolution of aquaporins (AQPs) in these vertebrates should help to elucidate how mechanisms for water homeostasis evolved. The marine teleost gilthead sea bream (Sparus aurata) has a mammalian aquaporin-1 (AQP1)-related channel, termed AQP1o, with a specialized physiological role in mediating egg hydration. However, teleosts have an additional AQP isoform structurally more similar to AQP1, though its relationship with AQP1o is unclear. RESULTS:By using phylogenetic and genomic analyses we show here that teleosts, unlike tetrapods, have two closely linked AQP1 paralogous genes, termed aqp1a and aqp1b (formerly AQP1o). In marine teleosts that produce hydrated eggs, aqp1b is highly expressed in the ovary, whereas in freshwater species that produce non-hydrated eggs, aqp1b has a completely different expression pattern or is not found in the genome. Both Aqp1a and Aqp1b are functional water-selective channels when expressed in Xenopus laevis oocytes. However, expression of chimeric and mutated proteins in oocytes revealed that the sea bream Aqp1b C-terminus, unlike that of Aqp1a, contains specific residues involved in the control of Aqp1b intracellular trafficking through phosphorylation-independent and -dependent mechanisms. CONCLUSION:We propose that 1) Aqp1a and Aqp1b are encoded by distinct genes that probably originated specifically in the teleost lineage by duplication of a common ancestor soon after divergence from tetrapods, 2) Aqp1b possibly represents a neofunctionalized AQP adapted to oocytes of marine and catadromous teleosts, thereby contributing to a water reservoir in eggs and early embryos that increases their survival in the ocean, and 3) Aqp1b independently acquired regulatory domains in the cytoplasmatic C-terminal tail for the specific control of Aqp1b expression in the plasma membrane.

Project description:BackgroundWhole genome duplications (WGDs) have been proposed to have made a significant impact on vertebrate evolution. Two rounds of WGD (1R and 2R) occurred in the common ancestor of Gnathostomata and Cyclostomata, followed by the third-round WGD (3R) in a common ancestor of all modern teleosts. The 3R-derived paralogs are good models for understanding the evolution of genes after WGD, which have the potential to facilitate phenotypic diversification. However, the recent studies of 3R-derived paralogs tend to be based on in silico analyses. Here we analyzed the paralogs encoding teleost olfactory marker protein (OMP), which was shown to be specifically expressed in mature olfactory sensory neurons and is expected to be involved in olfactory transduction.ResultsOur genome database search identified two OMPs (OMP1 and OMP2) in teleosts, whereas only one was present in other vertebrates. Phylogenetic and synteny analyses suggested that OMP1 and 2 were derived from 3R. Both OMPs showed distinct expression patterns in zebrafish; OMP1 was expressed in the deep layer of the olfactory epithelium (OE), which is consistent with previous studies of mice and zebrafish, whereas OMP2 was sporadically expressed in the superficial layer. Interestingly, OMP2 was expressed in a very restricted region of the retina as well as in the OE. In addition, the analysis of transcriptome data of spotted gar, a non-teleost fish, revealed that single OMP gene was expressed in the eyes.ConclusionWe found distinct expression patterns of zebrafish OMP1 and 2 at the tissue and cellular level. These differences in expression patterns may be explained by subfunctionalization as the model of molecular evolution. Namely, single OMP gene was speculated to be originally expressed in the OE and the eyes in the common ancestor of all Osteichthyes (bony fish including tetrapods). Then, two OMP gene paralogs derived from 3R-WGD reduced and specialized the expression patterns. This study provides a good example for analyzing a functional subdivision of the teleost OE and eyes as revealed by 3R-derived paralogs of OMPs.

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Whole-genome duplication and the functional diversification of teleost fish hemoglobins.

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Whole-genome duplication and the functional diversification of teleost fish hemoglobins.

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