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Multiple vitellogenins in zebrafish (Danio rerio): quantitative inventory of genes, transcripts and proteins, and relation to egg quality

Authors:
Ozlem Yilmaz at Institute of Marine Research in Norway
Ozlem Yilmaz
Amélie Patinote
Amélie Patinote
Amélie Patinote
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Thaovi Nguyen
Thaovi Nguyen
Thaovi Nguyen
  • This person is not on ResearchGate, or hasn't claimed this research yet.
Julien Bobe at French National Institute for Agriculture, Food, and Environment (INRAE)
Julien Bobe
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Abstract and Figures

Scrutiny of the zebrafish (Danio rerio) genomic database confirmed eight functional vitellogenin (vtg) genes, each with one or two transcript variants, and the encoded Vtg polypeptides were structurally and functionally characterized in detail by in silico and experimental analyses. There were five type I (vtgs1, 4, 5, 6, and 7), two type II (vtg2 and vtg8), and one type III (vtg3) vtg gene(s) encoding three major types of Vtg protein based on subdomain structure (Vtg-I, Vtg-II, and Vtg-III, respectively). Among various tissues of mature zebrafish, transcripts of the eight vtg genes were detected by RNA-Seq only in liver and intestine, with liver being the main site of vtg expression. All vtg transcripts except vtg8 were also detected in mature female liver by RT-qPCR. The relative abundances of Vtg proteins and their variants were quantified by LC-MS/MS in the liver of mature females and in eggs. The Vtgs were generally several fold more abundant in eggs, but profiles of abundance of the 19 different forms of Vtg evaluated were otherwise similar in liver and eggs, suggesting that yolk protein composition is determined largely by hepatic Vtg synthesis and secretion. Based on transcript and protein levels, Vtg-I is, by far, the dominant type of Vtg in zebrafish, followed by Vtg-II and then Vtg-III. When relative abundances of the different forms of Vtg were evaluated by LC-MS/MS in egg batches of good versus poor quality, no differences in the proportional abundance of individual forms of Vtg, or of different Vtg types, attributable to egg quality were observed.
Protein dendrogram nomenclature and domain structure of vitellogenins (Vtgs) in zebrafish compared to those in diverse array of other fishes. The dendrogram (left panel) shows clustering by similarity of the zebrafish Vtg polypeptide sequences deduced from cDNAs with those from other representative fish species for which full-length Vtg cDNAs are available. YP domain structures of some major forms of fish Vtg emphasizing the three main types of zebrafish Vtg are given in the right panel. Representative species were selected to illustrate variation in the presence and structural organization of Vtg YP domains. Names of non-teleost species and Vtgs (VtgABCD, VtgAB, VgA2, VgB1) are shown in black. Names of other species and Vtgs are color-coded by Vtg type with the names of zebrafish Vtgs emphasized by dashed lines and zebrafish icons to their right. The number of deduced zebrafish polypeptides of each structural type is given in parentheses in the right panel. Further details on Vtg nomenclature are given by Reading and Sullivan (2010) and Sullivan and Yilmaz (2018). For details on evolution of corresponding vtg genes in zebrafish and other teleosts (not shown), see Babin (2008), Finn et al. (2009), and Andersen et al. (2017)
Protein dendrogram nomenclature and domain structure of vitellogenins (Vtgs) in zebrafish compared to those in diverse array of other fishes. The dendrogram (left panel) shows clustering by similarity of the zebrafish Vtg polypeptide sequences deduced from cDNAs with those from other representative fish species for which full-length Vtg cDNAs are available. YP domain structures of some major forms of fish Vtg emphasizing the three main types of zebrafish Vtg are given in the right panel. Representative species were selected to illustrate variation in the presence and structural organization of Vtg YP domains. Names of non-teleost species and Vtgs (VtgABCD, VtgAB, VgA2, VgB1) are shown in black. Names of other species and Vtgs are color-coded by Vtg type with the names of zebrafish Vtgs emphasized by dashed lines and zebrafish icons to their right. The number of deduced zebrafish polypeptides of each structural type is given in parentheses in the right panel. Further details on Vtg nomenclature are given by Reading and Sullivan (2010) and Sullivan and Yilmaz (2018). For details on evolution of corresponding vtg genes in zebrafish and other teleosts (not shown), see Babin (2008), Finn et al. (2009), and Andersen et al. (2017)
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Syntenic organization of multiple vitellogenin genes in the zebrafish genome. Genomic locations for vitellogenin (vtg) genes and neighboring genes are shown. Polygons indicate individual genes and show their available transcriptional orientation, with abbreviated gene names appearing above; different colors indicate different types of zebrafish vtg with red, blue, and yellow indicating zebrafish type I, type II, and type III vtgs, respectively (gray indicates genes other than vtgs). Chr, chromosome
Syntenic organization of multiple vitellogenin genes in the zebrafish genome. Genomic locations for vitellogenin (vtg) genes and neighboring genes are shown. Polygons indicate individual genes and show their available transcriptional orientation, with abbreviated gene names appearing above; different colors indicate different types of zebrafish vtg with red, blue, and yellow indicating zebrafish type I, type II, and type III vtgs, respectively (gray indicates genes other than vtgs). Chr, chromosome
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Relative expression of zebrafish vitellogenin genes in various tissues. Zebrafish vtg cDNA sequences were mapped to RNA-Seq data from the PhyloFish database where species specific databases were constructed from separate libraries from the following tissues or organs from single female individuals plus a testis from a male individual, to allow analysis of tissue specific expression patterns: brain, liver, gills, heart, muscle, liver, kidney, bones, intestine, ovary, and testis (Pasquier et al. 2016). Obtained reads were normalized for sequencing depth bias and for transcript length as indicated in “Materials and methods”
Relative expression of zebrafish vitellogenin genes in various tissues. Zebrafish vtg cDNA sequences were mapped to RNA-Seq data from the PhyloFish database where species specific databases were constructed from separate libraries from the following tissues or organs from single female individuals plus a testis from a male individual, to allow analysis of tissue specific expression patterns: brain, liver, gills, heart, muscle, liver, kidney, bones, intestine, ovary, and testis (Pasquier et al. 2016). Obtained reads were normalized for sequencing depth bias and for transcript length as indicated in “Materials and methods”
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Relative expression levels of zebrafish vitellogenin genes in female liver. a Relative quantification of vtg expression via RNA-Seq. Zebrafish vtg cDNA sequences were mapped to RNA-Seq data from PhyloFish database (Pasquier et al. 2016) and obtained reads were normalized for sequencing depth bias and for transcript length as indicated in “Materials and methods” (results also shown in Fig. 3). Vertical bars represent normalized number of reads that are also given above each bar. b Relative quantification of expression zebrafish vtgs in female liver (N = 4) via RT-qPCR using gene-specific primers. Vertical bars indicate normalized expression ratios with respect to the mean expression level of three reference genes (eif1a, rpl13a, and 18S) and vertical brackets indicate SEM
Relative expression levels of zebrafish vitellogenin genes in female liver. a Relative quantification of vtg expression via RNA-Seq. Zebrafish vtg cDNA sequences were mapped to RNA-Seq data from PhyloFish database (Pasquier et al. 2016) and obtained reads were normalized for sequencing depth bias and for transcript length as indicated in “Materials and methods” (results also shown in Fig. 3). Vertical bars represent normalized number of reads that are also given above each bar. b Relative quantification of expression zebrafish vtgs in female liver (N = 4) via RT-qPCR using gene-specific primers. Vertical bars indicate normalized expression ratios with respect to the mean expression level of three reference genes (eif1a, rpl13a, and 18S) and vertical brackets indicate SEM
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Relative abundance of multiple vitellogenins and their variants in zebrafish. a Vitellogenin (Vtg) levels in adult female liver. b Levels of yolk proteins (YPs) derived from each form of Vtg in eggs. The mean normalized spectral counts (N-SC) for each form of Vtg or YPs are shown. Bars of the same color represent Vtgs (or Vtg products) of the same type with red, blue, and yellow indicating zebrafish type I Vtg, type II Vtg, and type III Vtg, respectively. Vertical brackets indicate SEM. Results for transcript variants are grouped by horizontal brackets above corresponding bars and transcript names representing each protein variant are given with the same convention used in Figs. S1 and S2. Bars labeled with the same letter superscript indicate mean values (N = 4) for variants of the same form of Vtg (or YP) that are not significantly different (p < 0.05). NSD, not significantly different; ND, not detected; N/A, not applicable
+2
Relative abundance of multiple vitellogenins and their variants in zebrafish. a Vitellogenin (Vtg) levels in adult female liver. b Levels of yolk proteins (YPs) derived from each form of Vtg in eggs. The mean normalized spectral counts (N-SC) for each form of Vtg or YPs are shown. Bars of the same color represent Vtgs (or Vtg products) of the same type with red, blue, and yellow indicating zebrafish type I Vtg, type II Vtg, and type III Vtg, respectively. Vertical brackets indicate SEM. Results for transcript variants are grouped by horizontal brackets above corresponding bars and transcript names representing each protein variant are given with the same convention used in Figs. S1 and S2. Bars labeled with the same letter superscript indicate mean values (N = 4) for variants of the same form of Vtg (or YP) that are not significantly different (p < 0.05). NSD, not significantly different; ND, not detected; N/A, not applicable
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... Vtg is encoded by a variable number of paralog gene families, and the diversity of Vtgs has been extensively confirmed and explored in past studies [6][7][8]. The current understanding suggests that teleosts produce multiple variants of Vtg, as evidenced by the discovery of 8 Vtg genes in zebrafish (Danio rerio) [9] and up to 20 Vtg genes in rainbow trout (Oncorhynchus mykiss) [10]. The evolutionary history of the vitellogenin gene family has been extensively studied, and it is widely believed that the presence of multiple Int. ...
... It is worth noting that vtg6, although nominally classified as a type I Vtg, possesses the LvH domain that is missing a large number of amino acids compared to other type I Vtgs, which results in low sequence similarity between vtg6 and other vtgs. Phylogenetic analyses showed that Sichuan bream Vtg6 and zebrafish Vtg8 are phylogenetically close to each other, possibly because they both exhibit miniaturization and incompleteness in the LvH structural domain [9]. The expression levels of Vtg6, similar to zebrafish Vtg8, were found to be the lowest in subsequent expression analyses, suggesting that this small Vtg has a limited contribution to vitellogenesis. ...
... In addition, the β ′ -c and Ct domains have been shown to be homologous to the von Willebrand factor type D domain (vWFD) and have been found to be involved in physiological processes such as immunity and coagulation [49,50]. However, there is a general lack of characterization of the β ′ -c and Ct domains nutritional functions [9]. The general lack of β ′ -c and Ct domains in type I and type III Vtgs may imply that the vWFD domain is not essential for the activity of Sichuan bream Vtgs, and it may function only in the Vtg2 monomer. ...
Genome-Wide Identification, Expression and Response to Estrogen of Vitellogenin Gene Family in Sichuan Bream (Sinibrama taeniatus)
Article
Full-text available
  • Jun 2024
  • INT J MOL SCI
To enhance our understanding of teleost reproductive physiology, we identified six Sichuan bream (Sinibrama taeniatus) vitellogenin genes (vtg1-6) and characterized their sequence structures. We categorized them into type Ⅰ (vtg1,4,5 and 6), type Ⅱ (vtg2) and type Ⅲ (vtg3) based on differences in their subdomain structure. The promoter sequence of vtgs has multiple estrogen response elements, and their abundance appears to correlate with the responsiveness of vtg gene expression to estrogen. Gene expression analyses revealed that the vitellogenesis of Sichuan bream involves both heterosynthesis and autosynthesis pathways, with the dominant pathway originating from the liver. The drug treatment experiments revealed that 17β-estradiol (E2) tightly regulated the level of vtg mRNA in the liver. Feeding fish with a diet containing 100 μg/g E2 for three weeks significantly induced vtg gene expression and ovarian development, leading to an earlier onset of vitellogenesis. Additionally, it was observed that the initiation of vtg transcription required E2 binding to its receptor, a process primarily mediated by estrogen receptor alpha in Sichuan bream. The findings of this study provide novel insights into the molecular information of the vitellogenin gene family in teleosts, thereby contributing to the regulation of gonadal development in farmed fish.
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Assessing the chronic exposure of copper oxide and zinc oxide nanoparticles in zebrafish
Article
  • Jun 2024
In the present time, nanomaterial toxicological studies have become important due to the persistent presence of engineered nanomaterials in the environment. Zebrafsh are a versatile and well-established model organism for biosafety assessments of nanomaterials and other toxicants. The present study aimed to investigate the long-term efects of low concentrations of copper oxide (CuO) nanoparticles (NPs) and zinc oxide (ZnO) NPs on zebrafsh focusing on their potential toxicological impact. Methods The efects of CuO NPs and ZnO NPs at varying concentrations (0.01, 0.05, and 0.1 µg/mL) were assessed in adult zebrafsh over 730 days (2 years). At the end of the exposure period, the efects were observed through the study of mortality and body weights, histopathological analysis of gills and intestines, quantitative reverse transcription-polymerase chain reaction (qRT-PCR) of Zpr1, Vtg1, and Th1 genes, levels of tyrosine hydroxylase in zebrafsh brain, and study of malformations in F1 generation of the treated zebrafsh. Results CuO NPs caused mortality and malformations of embryos at 0.1 µg/mL concentration whereas no such efect was observed in the case of ZnO NPs. The weights of zebrafsh treated with CuO NPs decreased with time. It was explained by the disruption of the villi of these zebrafsh after H&E staining. CuO NPs were also found to disrupt the morphology of the gills of zebrafsh over a while. The fold change in the genes related to the Zpr1, Th1, and Vtg1 genes also suggested the potential toxicity caused by CuO NPs. In immunohistochemistry studies, CuO NPs were found to increase the levels of tyrosine hydroxylase in the zebrafsh brain, pointing out its interference with the swimming patterns of the zebrafsh and the induction of stress. The F1 generation of CuO NPs-treated fsh showed a decrease in reproducing ability along with the malformations in the F1 generation. Therefore, CuO NPs caused chronic toxicity at low concentrations whereas no such toxicity was observed in the case of ZnO NPs. Conclusion The data from our study indicated that CuO NPs exhibited elevated toxicity even at lower concentrations when exposed over an extended period. In contrast, exposure to ZnO NPs did not show any signifcant toxicity efects on zebrafsh.
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The role of multiple vitellogenins in early development of fishes
Article
Full-text available
  • Mar 2024
  • GEN COMP ENDOCR
Functions of vitellogenins have been in the limelight of fish reproductive physiology research for decades. The Vtg system of acanthomorph teleosts consists of two complete forms of Vtgs (VtgAa and VtgAb) and an incomplete form, VtgC. Insufficient uptake and processing of Vtgs and their yolk proteins lead to inadequate oocyte hydration ensuing failure in acquisition of egg buoyancy and early developmental deficiencies. This review presents a summary of our studies on utilization of multiple Vtgs in species with different egg buoyancy characteristics, as examples. Studies of moronids revealed limited degradation of all three forms of lipovitellin heavy chain derived from their three respective forms of Vtg, by which they contribute to the free amino acid pool driving oocyte hydration during oocyte maturation. In later studies, CRISPR/Cas9 was employed to invalidate zebrafish type I, type II and type III Vtgs, which are orthologs of acanthamorph VtgAa, VtgAb and VtgC, respectively. Results revealed type I Vtg to have essential developmental and nutritional functions in both late embryos and larvae. Genomic disturbance of type II Vtg led to high mortalities during the first 24 h of embryonic development. Despite being a minor form of Vtg in zebrafish and most other species, type III Vtg was also found to contribute essentially to the developmental potential of zebrafish zygotes and early embryos. Apart from severe effects on progeny survival, these studies also disclosed previously unreported regulatory effects of Vtgs on fecundity and fertility, and on embryo hatching. We recently utilized parallel reactions monitoring based liquid chromatography tandem mass spectrometry to assess the processing and utilization of lipovitellins derived from different forms of Vtg in Atlantic halibut and European plaice. Results showed the Lv heavy chain of VtgAa (LvHAa) to be consumed during oocyte maturation and the Lv light chain of VtgAb (LvLAb) to be utilized specifically during late larval stages, while all remaining YPs (LvLAa, LvHAb, LvHC, and LvLC) were utilized during or after hatching up until first feeding in halibut. In plaice, all YPs except LvHAa, which similarly to halibut supports oocyte maturation, are utilized from late embryo to late larval development up until first feeding. The collective findings from these studies affirm substantial disparity in modes of utilization of different types of Vtgs among fish species with various egg buoyancy characteristics, and they reveal previously unknown regulatory functions of Vtgs in maintenance of reproductive assets such as maternal fecundity and fertility, and in embryonic hatching. Despite the progress that has been made over the past two decades by examining multiple Vtgs and their functions, a higher complexity of these systems with much greater diversity between species in modes of Vtg utilization is now evident. Further research is needed to reveal novel ways each species has evolved to utilize these complex multiple Vtg systems and to discover unifying principles for this evolution in fishes of diverse lineages, habitats and life history characteristics.
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Diversification and Classification of Vitellogenin in Fishes
Chapter
  • Nov 2023
Vitellogenin (Vtg) is a protein synthesized by the liver in response to estrogen expressed in the female bloodstream during vitellogenesis. It is a high-molecular-mass complex protein consisting of sugar, lipid, and phosphorus with other binding elements such as calcium, iron, and zinc. It is the precursor of the lipoproteins and phosphoproteins that makes up most of the protein content of yolk. Vitellogenin transports proteins and some lipids from the liver through the blood to the growing oocytes and functions as the incredible provider and part of the yolk, the vital nutrient to the developing embryos of egg layers (oviparous), both vertebrates and invertebrates. In the oocyte, Vtgs are processed into yolk proteins, stored mostly as yolk granules also termed as globules or platelets and sometimes in an amorphous compartment (fluid yolk). Recent protein and gene analyses have revealed the presence of several vitellogenin variants. Fish Vtgs exhibit complex evolutionary history expressing significant disparity in structure and function. This chapter deals with the diversification and classification of piscine vitellogenin.
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Molecular Cloning and Induction of Vitellogenesis
Chapter
  • Nov 2023
Fish hepatocytes produce vitellogenin, a calcium-binding glycolipophosphoprotein, which can be induced in fishes to synthesize it by either estradiol or xenoestrogens. Regarding estrogenic compounds, the lowest effective doses of vitellogenin were reported, and it can be triggered via xenoestrogens. In aquatic ecosystems, estrogenic molecules such as natural steroidal estrogens and synthetic pollutants are extensively abundant. In recent times, the induction of Vtg has been suggested as a potential biomarker to detect estrogenic pollutants. Indeed, the estrogenicity of distinct compounds and mixtures was intensively explored in laboratories and field research, primarily in fish. However, due to our understanding of the endocrinology of aquatic invertebrates, little focus has been placed on studying the effects of xenoestrogen on these organisms. This chapter describes about the induction of Vtg in aquatic invertebrates which response to exposure of estrogenic compounds in both experimental and natural environments. At last, this chapter points out the molecular cloning on how these estrogenic compounds can modulate Vtg in fishes for a better understanding of the environmental behavior.
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Tools for Identification and Characterization of Vitellogenin in Fishes
Chapter
  • Nov 2023
In teleost fishes and other oviparous vertebrates, vitellogenins (Vtg) are the main precursor of the egg yolk proteins that serve as energy reserves for embryonic development. In most cases, endogenous estrogens, such as 17-estradiol (E2), which are released into the bloodstream and then maintained in developing oocytes in adult females, cause the production of Vtg. It has evolved into a significant biomarker in recent decades for determining the estrogenic potency of chemicals and the exposure of animals to estrogenic pollutants found in aquatic environments. Consequently, a variety of different analytical approaches have been used depending on the expertise of diverse research laboratories to assess whether a molecule or effluent is able to generate Vtg. This insights into the molecular mechanism responsible for vitellogenin synthesis and range of techniques are currently in use to measure the Vtg protein as an indication of estrogenic responses in fishes. Thus, more information on the techniques to detect and quantify the vitellogenin is necessary to clarify their endocrine system and to learn more about how vitellogenin protein is utilized as a sensitive biomarker for detecting estrogenic activities in fishes. Hence, this chapter aims to cover the major tools for vitellogenin identification and characterization were explored.
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Effect of Vitellogenin in the Growth of Ornamental Fishes
Chapter
  • Nov 2023
Fish egg quality has been a focus of research in aquaculture and fisheries for decades since it is essential for successful captive reproduction and recruitment and constitutes a significant life history feature. Since most fish are oviparous and their developing progeny are fully dependent on stored egg yolk for nutritional sustenance, adequate yolk formation is a crucial factor impacting egg quality. These nutrients, which are received from the mother, travel from the liver to the ovary in the form of lipoprotein particles like vitellogenins and are made up of proteins, carbohydrates, lipids, vitamins, minerals, and ions. The food, husbandry, and other intrinsic and extrinsic factors of the brood stock may have an impact on the yolk composition. Additionally, several maternal variables that may affect egg quality, such as gene transcripts that control early embryonic development, are also stored in eggs. Poor quality eggs and failure to flourish within hours of fertilization may be caused by dysfunctional control of gene or protein expression. The gene transcripts may serve as significant markers. In addition to these intrinsic variables, stress can affect fish behavior, fecundity, and ovulation rate and cause ovarian atresia or reproductive failure. This chapter gives a brief overview of the reproductive biology of ornamental fishes before going into detail about the main issues that exist in culture and the hormonal interventions created in recent years to deal with these dysfunctions. Future developments in the field of spawning induction technologies are also taken into account.
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Vitellogenesis and Reproductive Strategies in Fishes
Chapter
  • Nov 2023
Vitellogenesis is a hormonally mediated process in fishes in which the protein vitellogenin is being secreted by reproductive hormones gonadotropins and facilitated by estrogen. Sexual activity of some fish is generally seasonal and fertilization is external. After fertilization, fishes produce haploid eggs and undergo the process of differentiation. Oocyte development occurs at the stage of differentiation. For proper embryonic development, gathering of yolk in oocytes is a vital process which leads the reproduction in a successful manner. Sequentially, there are three main steps involved in oocyte production which are (1) generation of primordial germ cells (PGCs), (2) transformation of PGCs to oogonia, and finally (3) the production of oocytes. Gonadotropins are produced into the bloodstream during the oogenesis process and then delivered to the ovaries to enhance the growth of the oocyte, otherwise known as ovulation. In addition to this, follicle cells are triggered to synthesize estrogen hormone also named as primary estradiol. Sequentially, the estradiol is introduced into the serum of the animal where it is bound by steroid-binding protein or albumin. In fact, the exogenous synthesis of vitellogenin is initiated by gonadotropins and regulated by the hormone estrogens. Estradiol or estrogen plays the key role in triggering vitellogenin production.
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Scrambled eggs: Proteomic portraits and novel biomarkers of egg quality in zebrafish (Danio rerio)
Article
Full-text available
Egg quality is a complex biological trait and a major determinant of reproductive fitness in all animals. This study delivered the first proteomic portraits of egg quality in zebrafish, a leading biomedical model for early development. Egg batches of good and poor quality, evidenced by embryo survival for 24 h, were sampled immediately after spawning and used to create pooled or replicated sample sets whose protein extracts were subjected to different levels of fractionation before liquid chromatography and tandem mass spectrometry. Obtained spectra were searched against a zebrafish proteome database and detected proteins were annotated, categorized and quantified based on normalized spectral counts. Manually curated and automated enrichment analyses revealed poor quality eggs to be deficient of proteins involved in protein synthesis and energy and lipid metabolism, and of some vitellogenin products and lectins, and to have a surfeit of proteins involved in endo-lysosomal activities, autophagy, and apoptosis, and of some oncogene products, lectins and egg envelope proteins. Results of pathway and network analyses suggest that this aberrant proteomic profile results from failure of oocytes giving rise to poor quality eggs to properly transit through final maturation, and implicated Wnt signaling in the etiology of this defect. Quantitative comparisons of abundant proteins in good versus poor quality eggs revealed 17 candidate egg quality markers. Thus, the zebrafish egg proteome is clearly linked to embryo developmental potential, a phenomenon that begs further investigation to elucidate the root causes of poor egg quality, presently a serious and intractable problem in livestock and human reproductive medicine.
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Genomicus 2018: Karyotype evolutionary trees and on-the-fly synteny computing
Article
Full-text available
  • Oct 2017
Since 2010, the Genomicus web server is available online at http://genomicus.biologie.ens.fr/genomicus. This graphical browser provides access to comparative genomic analyses in four different phyla (Vertebrate, Plants, Fungi, and non vertebrate Metazoans). Users can analyse genomic information from extant species, as well as ancestral gene content and gene order for vertebrates and flowering plants, in an integrated evolutionary context. New analyses and visualization tools have recently been implemented in Genomicus Vertebrate. Karyotype structures from several genomes can now be compared along an evolutionary pathway (Multi-KaryotypeView), and synteny blocks can be computed and visualized between any two genomes (PhylDiagView).
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Gene evolution and gene expression after whole genome duplication in fish: The PhyloFish database
Article
Full-text available
  • May 2016
  • BMC GENOMICS
With more than 30,000 species, ray-finned fish represent approximately half of vertebrates. The evolution of ray-finned fish was impacted by several whole genome duplication (WGD) events including a teleost-specific WGD event (TGD) that occurred at the root of the teleost lineage about 350 million years ago (Mya) and more recent WGD events in salmonids, carps, suckers and others. In plants and animals, WGD events are associated with adaptive radiations and evolutionary innovations. WGD-spurred innovation may be especially relevant in the case of teleost fish, which colonized a wide diversity of habitats on earth, including many extreme environments. Fish biodiversity, the use of fish models for human medicine and ecological studies, and the importance of fish in human nutrition, fuel an important need for the characterization of gene expression repertoires and corresponding evolutionary histories of ray-finned fish genes. To this aim, we performed transcriptome analyses and developed the PhyloFish database to provide (i) de novo assembled gene repertoires in 23 different ray-finned fish species including two holosteans (i.e. a group that diverged from teleosts before TGD) and 21 teleosts (including six salmonids), and (ii) gene expression levels in ten different tissues and organs (and embryos for many) in the same species. This resource was generated using a common deep RNA sequencing protocol to obtain the most exhaustive gene repertoire possible in each species that allows between-species comparisons to study the evolution of gene expression in different lineages. The PhyloFish database described here can be accessed and searched using RNAbrowse, a simple and efficient solution to give access to RNA-seq de novo assembled transcripts.
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The Reproductive Organs and Processes: Vitellogenesis in Fishes
Article
Full-text available
  • Dec 2011
Developing offspring of oviparous animals are entirely dependent on stored egg yolk for nutritional sustenance. The nutrients stored in the ovulated egg must be sufficient to sustain progeny development from the time of fertilization to the onset of exogenous feeding. Vitellogenesis is the process whereby the required yolk nutrients are deposited into growing oocytes, which eventually give rise to eggs. These nutrients consist of maternally derived substances, including proteins, carbohydrates, lipids, vitamins, minerals, and ions that are collectively transported from the liver to the ovary in the form of circulating yolk precursors called vitellogenins.
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Resolving the complexity of vitellogenins and their receptors in the tetraploid Atlantic salmon (Salmo salar): Ancient origin of the phosvitin‐less VtgC in chondrichthyean fishes
Article
  • Aug 2017
  • MOL REPROD DEV
Egg yolk proteins are mainly derived from vitellogenin (Vtg), and serve as essential nutrients during early development in oviparous organisms. Vertebrate Vtgs are predominantly synthesized in the liver of maturing females, and are internalized by the oocyte after binding to specific surface receptors (VtgR). Here we clarify the evolutionary history of the vertebrate Vtgs, including the teleost VtgC, which lacks phosvitin, and investigate the repertoire of Vtgs and VtgRs in the tetraploid Atlantic salmon (Salmo salar). Conserved synteny of the vtg genes in elephant fish (Callorhinchus milii) strongly indicates that the vtg gene cluster was present in the ancestor of tetrapods and ray-finned fish. The shortened phosvitin in the VtgC ortholog of this chondrichthyean fish may have resulted from early truncation events that eventually allowed the total disappearance of phosvitin in teleost VtgC. In contrast, the tandem-duplicated VtgCs identified in spotted gar (Lepisosteus oculatus) both contain the phosvitin domain. The Atlantic salmon genome harbors four vtg genes encoding the complete VtgAsa1, phosvitin-less VtgC and truncated VtgAsb proteins; vtgAsa2 is a pseudogene. The three vtg genes were mainly expressed in the liver of maturing females, and the vtgAsa1 transcript predominated prior to spawning. The splice variant lacking the O-linked sugar domain dominated ovarian expression of vtgr1 and vtgr2. Strongly increased vtgAsa1 expression during vitellogenesis contrasted with the peaks of vtgr1 and vtgr2 in the previtellogenic oocytes, which gradually decreased over the same period. Recycling of the oocyte VtgRs is probably not sufficient to maintain receptor number during vitellogenesis. This article is protected by copyright. All rights reserved
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The observed oogenesis impairment in greater amberjack Seriola dumerili (Risso, 1810) reared in captivity is not related to an insufficient liver transcription or oocyte uptake of vitellogenin
Article
The greater amberjack Seriola dumerili is an excellent candidate for the Mediterranean aquaculture, due to its large body size and high growth rate, as well as its high flesh quality and commercial value worldwide. For its successful incorporation in the aquaculture industry, an in-depth understanding of the reproductive function of the species under rearing conditions is necessary, since completion of oogenesis in captivity is currently a bottleneck for the commercial production of the species. Liver and ovary samples from wild and captive-reared greater amberjack females were collected at three different phases of the reproductive cycle: early gametogenesis (EARLY, late April-early May), advanced gametogenesis (ADVANCED, late May-early June) and spawning (SPAWNING, late June-July). The cDNAs of three vitellogenins (VtgA, VtgB and VtgC) were partially sequenced and a qRT-PCR for their expression was used to compare ovarian maturity stage and liver vitellogenin transcript levels between wild and captive-reared individuals. An extensive atresia of late vitellogenic follicles, which prevented any further oocyte development and spawning was observed in captive-reared individuals during the ADVANCED phase. The expression levels of the three vitellogenins, as well as the amount of yolk globules in vitellogenic oocytes, did not differ significantly between captive-reared and wild females, indicating that the observed oogenesis impairment in greater amberjack reared in captivity was not related to an insufficient liver synthesis or a reduced oocyte uptake of vitellogenin.
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Vitellogenesis in Fishes
Chapter
  • Jan 2017
Developing offspring of oviparous animals are entirely dependent on stored egg yolk for nutritional sustenance. The nutrients stored in the ovulated egg must be sufficient to sustain progeny development from the time of fertilization to the onset of exogenous feeding. Vitellogenesis is the process whereby the required yolk nutrients are deposited into growing oocytes, which eventually give rise to eggs. These nutrients consist of maternally derived substances, including proteins, carbohydrates, lipids, vitamins, minerals, and ions that are collectively transported from the liver to the ovary in the form of circulating yolk precursors called vitellogenins.
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Maternal investment in fish oocytes and eggs: The molecular cargo and its contributions to fertility and early development
Article
  • Oct 2016
  • AQUACULTURE
The production of fertile eggs with the capacity to develop into larvae and subsequently into marketable fish is centrally important to the aquaculture industry. This entails not only the programmed production of large numbers of eggs, but also high quality eggs with the potential to support normal development and high survival of offspring to juvenile and later stages of development and growth. Numerous studies highlight the maternal contributions to the development of embryos, including transcripts that regulate cell division and determine oocyte polarity, pattern development during early and late embryonic stages and the transition from maternal to zygotic gene expression and translation. Since most fish embryos develop independently within an enclosed egg envelope, they rely on compounds deposited within the oocytes during their various stages of development. In addition to regulatory nucleic acids (maternal DNA and RNA), these include proteins and other compounds that contribute to the structure and function of the egg envelope and the bulk molecular cargo that will be used as a source of cellular energy and structural components for formation of embryos and larvae. These latter components notably include yolk lipids and proteins deposited during oocyte growth and water acquired at the same time and during cytoplasmic maturation. In this review we highlight recent advances made in revealing the transcripts deposited within the oocyte that contribute to the structural and morphological development of the embryo, and to the regulation of gene expression and translation during oocyte development. Significant advances have been made in revealing the molecular mechanisms of lipid accumulation and metabolism within the oocyte, the intricacies of yolk protein formation via endocytosis of multiple yolk precursor proteins by multiple oocyte receptors, and the complex machinery supporting massive accumulation of water by maturing oocytes of many species. Additionally, many advances have been made in our understanding of the endocrine regulation of all of these processes during oogenesis. We provide here an overview of recent advances in our knowledge on these various aspects of oogenesis and identify several gaps in our knowledge for future studies.
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