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Duplication and subfunctionalisation of the general transcription factor IIIA (gtf3a) gene in teleost genomes, with ovarian specific transcription of gtf3ab.

ABSTRACT: Fish oogenesis is characterised by a massive growth of oocytes each reproductive season. This growth requires the stockpiling of certain molecules, such as ribosomal RNAs to assist the rapid ribosomal assembly and protein synthesis required to allow developmental processes in the newly formed embryo. Massive 5S rRNA expression in oocytes, facilitated by transcription factor 3A (Gtf3a), serves as marker of intersex condition in fish exposed to xenoestrogens. Our present work on Gtf3a gene evolution has been analysed in silico in teleost genomes and functionally in the case of the zebrafish Danio rerio. Synteny-analysis of fish genomes has allowed the identification of two gtf3a paralog genes, probably emerged from the teleost specific genome duplication event. Functional analyses demonstrated that gtf3ab has evolved as a gene specially transcribed in oocytes as observed in Danio rerio, and also in Oreochromis niloticus. Instead, gtf3aa was observed to be ubiquitously expressed. In addition, in zebrafish embryos gtf3aa transcription began with the activation of the zygotic genome (~8 hpf), while gtf3ab transcription began only at the onset of oogenesis. Under exposure to 100 ng/L 17β-estradiol, fully feminised 61 dpf zebrafish showed transcription of ovarian gtf3ab, while masculinised (100 ng/L 17α-methyltestosterone treated) zebrafish only transcribed gtf3aa. Sex related transcription of gtf3ab coincided with that of cyp19a1a being opposite to that of amh and dmrt1. Such sex dimorphic pattern of gtf3ab transcription was not observed earlier in larvae that had not yet shown any signs of gonad formation after 26 days of oestradiol exposure. Thus, gtf3ab transcription is a consequence of oocyte differentiation and not a direct result of estrogen exposure, and could constitute a useful marker of gonad feminisation and intersex condition.

SUBMITTER: Rojo-Bartolome I

PROVIDER: S-EPMC6991959 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundGene duplication has had a major impact on genome evolution. Localized (or tandem) duplication resulting from unequal crossing over and whole genome duplication are believed to be the two dominant mechanisms contributing to vertebrate genome evolution. While much scrutiny has been directed toward discerning patterns indicative of whole-genome duplication events in teleost species, less attention has been paid to the continuous nature of gene duplications and their impact on the size, gene content, functional diversity, and overall architecture of teleost genomes.ResultsHere, using a Markov clustering algorithm directed approach we catalogue and analyze patterns of gene duplication in the four model teleost species with chromosomal coordinates: zebrafish, medaka, stickleback, and Tetraodon. Our analyses based on set size, duplication type, synonymous substitution rate (Ks), and gene ontology emphasize shared and lineage-specific patterns of genome evolution via gene duplication. Most strikingly, our analyses highlight the extraordinary duplication and retention rate of recent duplicates in zebrafish and their likely role in the structural and functional expansion of the zebrafish genome. We find that the zebrafish genome is remarkable in its large number of duplicated genes, small duplicate set size, biased Ks distribution toward minimal mutational divergence, and proportion of tandem and intra-chromosomal duplicates when compared with the other teleost model genomes. The observed gene duplication patterns have played significant roles in shaping the architecture of teleost genomes and appear to have contributed to the recent functional diversification and divergence of important physiological processes in zebrafish.ConclusionsWe have analyzed gene duplication patterns and duplication types among the available teleost genomes and found that a large number of genes were tandemly and intrachromosomally duplicated, suggesting their origin of independent and continuous duplication. This is particularly true for the zebrafish genome. Further analysis of the duplicated gene sets indicated that a significant portion of duplicated genes in the zebrafish genome were of recent, lineage-specific duplication events. Most strikingly, a subset of duplicated genes is enriched among the recently duplicated genes involved in immune or sensory response pathways. Such findings demonstrated the significance of continuous gene duplication as well as that of whole genome duplication in the course of genome evolution.

Project description:BACKGROUND:Gene duplication is considered important to increasing the genetic diversity in animals. In fish, visual pigment genes are often independently duplicated, and the evolutionary significance of such duplications has long been of interest. Eels have two rhodopsin genes (rho), one of which (freshwater type, fw-rho) functions in freshwater and the other (deep-sea type, ds-rho) in marine environments. Hence, switching of rho expression in retinal cells is tightly linked with eels' unique life cycle, in which they migrate from rivers or lakes to the sea. These rho genes are apparently paralogous, but the timing of their duplication is unclear due to the deep-branching phylogeny. The aim of the present study is to elucidate the evolutionary origin of the two rho copies in eels using comparative genomics methods. RESULTS:In the present study, we sequenced the genome of Japanese eel Anguilla japonica and reconstructed two regions containing rho by de novo assembly. We found a single corresponding region in a non-teleostean primitive ray-finned fish (spotted gar) and two regions in a primitive teleost (Asian arowana). The order of ds-rho and the neighboring genes was highly conserved among the three species. With respect to fw-rho, which was lost in Asian arowana, the neighboring genes were also syntenic between Japanese eel and Asian arowana. In particular, the pattern of gene losses in ds-rho and fw-rho regions was the same as that in Asian arowana, and no discrepancy was found in any of the teleost genomes examined. Phylogenetic analysis supports mutual monophyly of these two teleostean synteny groups, which correspond to the ds-rho and fw-rho regions. CONCLUSIONS:Syntenic and phylogenetic analyses suggest that the duplication of rhodopsin gene in Japanese eel predated the divergence of eel (Elopomorpha) and arowana (Osteoglossomorpha). Thus, based on the principle of parsimony, it is most likely that the rhodopsin paralogs were generated through a whole genome duplication in the ancestor of teleosts, and have remained till the present in eels with distinct functional roles. Our result indicates, for the first time, that teleost-specific genome duplication may have contributed to a gene innovation involved in eel-specific migratory life cycle.

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:BackgroundThe dystroglycan (DG) complex is a major non-integrin cell adhesion system whose multiple biological roles involve, among others, skeletal muscle stability, embryonic development and synapse maturation. DG is composed of two subunits: alpha-DG, extracellular and highly glycosylated, and the transmembrane beta-DG, linking the cytoskeleton to the surrounding basement membrane in a wide variety of tissues. A single copy of the DG gene (DAG1) has been identified so far in humans and other mammals, encoding for a precursor protein which is post-translationally cleaved to liberate the two DG subunits. Similarly, D. rerio (zebrafish) seems to have a single copy of DAG1, whose removal was shown to cause a severe dystrophic phenotype in adult animals, although it is known that during evolution, due to a whole genome duplication (WGD) event, many teleost fish acquired multiple copies of several genes (paralogues).ResultsData mining of pufferfish (T. nigroviridis and T. rubripes) and other teleost fish (O. latipes and G. aculeatus) available nucleotide sequences revealed the presence of two functional paralogous DG sequences. RT-PCR analysis proved that both the DG sequences are transcribed in T. nigroviridis. One of the two DG sequences harbours an additional mini-intronic sequence, 137 bp long, interrupting the uncomplicated exon-intron-exon pattern displayed by DAG1 in mammals and D. rerio. A similar scenario emerged also in D. labrax (sea bass), from whose genome we have cloned and sequenced a new DG sequence that also harbours a shorter additional intronic sequence of 116 bp. Western blot analysis confirmed the presence of DG protein products in all the species analysed including two teleost Antarctic species (T. bernacchii and C. hamatus).ConclusionOur evolutionary analysis has shown that the whole-genome duplication event in the Class Actinopterygii (ray-finned fish) involved also DAG1. We unravelled new important molecular genetic details about fish orthologous DGs, which might help to increase the current knowledge on DG expression, maturation and targeting and on its physiopathological role in higher organisms.

Project description:BACKGROUND: HES/HEY genes encode a family of basic helix-loop-helix (bHLH) transcription factors with both bHLH and Orange domain. HES/HEY proteins are direct targets of the Notch signaling pathway and play an essential role in developmental decisions, such as the developments of nervous system, somitogenesis, blood vessel and heart. Despite their important functions, the origin and evolution of this HES/HEY gene family has yet to be elucidated. METHODS AND FINDINGS: In this study, we identified genes of the HES/HEY family in representative species and performed evolutionary analysis to elucidate their origin and evolutionary process. Our results showed that the HES/HEY genes only existed in metazoans and may originate from the common ancestor of metazoans. We identified HES/HEY genes in more than 10 species representing the main lineages. Combining the bHLH and Orange domain sequences, we constructed the phylogenetic trees by different methods (Bayesian, ML, NJ and ME) and classified the HES/HEY gene family into four groups. Our results indicated that this gene family had undergone three expansions, which were along with the origins of Eumetazoa, vertebrate, and teleost. Gene structure analysis revealed that the HES/HEY genes were involved in exon and/or intron loss in different species lineages. Genes of this family were duplicated in bony fishes and doubled than other vertebrates. Furthermore, we studied the teleost-specific duplications in zebrafish and investigated the expression pattern of duplicated genes in different tissues by RT-PCR. Finally, we proposed a model to show the evolution of this gene family with processes of expansion, exon/intron loss, and motif loss. CONCLUSIONS: Our study revealed the evolution of HES/HEY gene family, the expression and function divergence of duplicated genes, which also provide clues for the research of Notch function in development. This study shows a model of gene family analysis with gene structure evolution and duplication.

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Duplication and subfunctionalisation of the general transcription factor IIIA (gtf3a) gene in teleost genomes, with ovarian specific transcription of gtf3ab.

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