Evolution and differential expression of a vertebrate vitellogenin gene cluster (original) (raw)
Related papers
Molecular Biology and Evolution, 2009
Oocyte hydration is a unique event in oviparous marine teleosts that provides the single-celled egg with an essential pool of water for survival during early development in the saline oceanic environment. A conserved mechanism of maturational yolk proteolysis of a neofunctionalized vitellogenin (VtgAa) has been shown to underlie the hydration event in all teleosts that spawn pelagic eggs (pelagophils), and is argued to be a key adaptation for teleost radiation in the oceanic environment 55 Ma. We have recently shown that a small pool of free amino acids (FAAs) significantly contributes to the osmolarity of the ovulated egg in an ancestral marine teleost, the Atlantic herring that spawns benthic eggs (benthophil). To determine whether multiple forms of vtg exist and whether neofunctionalization of the gene products are related to the egg FAA pool in this species, genomic sequences conserved between the exons of Atlantic herring and zebrafish were amplified. This approach identified a small polymorphic intron between exons 9 and 10 in Atlantic herring and demonstrated that two closely related major vtg transcripts (chvtgAc1 and chvtgAc2) are expressed during oogenesis. A separate polymerase chain reaction-based approach identified a more ancestral phosvitinless transcript (chvtgC). Proteomic analyses of the translated products of the major vtg forms demonstrated that the yolk proteins are similarly processed during deposition, and oocyte maturation and reveal that vtgs have duplicated but not neofunctionalized in this species. Phylogenetic analyses consistently clustered the transcripts and proteins as the basal sister group to the Ostariophysi in full congruence with the Clupeocephalan rank, and suggest that expansion of ostariophysan vtgAo1 and vtgAo2 genes occurred in a lineage-specific manner after separation from the Clupeiformes. Three-dimensional modeling of the ChvtgAc1 sequence against the resolved lamprey lipovitellin module revealed that the tertiary structure is highly conserved, with most substitutions occurring on the outside of the molecule. The data indicate that the phosvitin domain, the smallest yet reported for teleosts, and an N-terminal fragment of the lipovitellin light chain contribute to the FAA pool. The present findings thus show that yolk proteolysis and the generation of an organic osmolyte pool of FAAs was an adaptive response to spawning in seawater also for the Clupeiformes, but that this process was not evolutionarily successful in terms of biodiversity until vtg gene neofunctionalization occurred in the Acanthomorpha.
Whole-genome duplication in teleost fishes and its evolutionary consequences
Molecular Genetics and Genomics, 2014
Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change.
New perspectives on the evolutionary history of vitellogenin gene family in vertebrates
Genome biology and evolution, 2018
Vitellogenin (Vtg) is a glycolipophosphoprotein produced by oviparous and ovoviviparous species and is the precursor protein of the yolk, an essential nutrient reserve for embryonic development and early larval stages. Vitellogenin is encoded by a family of paralog genes whose number varies in the different vertebrate lineages. Its evolution has been the subject of considerable analyses but it remains still unclear.In this work, microsyntenic and phylogenetic analyses were performed in order to increase our knowledge on the evolutionary history of this gene family in vertebrates. Our results support the hypothesis that the vitellogenin gene family is expanded from two genes both present at the beginning of vertebrate radiation through multiple independent duplication events occurred in the diverse lineages.
Sequence analysis of a fish vitellogenin cDNA with a large phosvitin domain
Gene, 2001
Vitellogenins (Vtg) are egg-yolk precursor proteins crucial for reproductive success in oviparous animals. We have cloned the first complete cichlid Vtg cDNA from the tilapia fish, Oreochromis aureus. This cDNA has the largest phosvitin (PV) domain amongst piscine Vtgs, being comparable to those of lamprey, Xenopus, and chicken. Thus, the size of PV is independent of the evolutionary advancement of a species. The closer interspecific relationship between O. aureus Vtg1 and Fundulus VtgII than the intraspecific relationship between Fundulus VtgI and II isoforms suggests that teleost ancestors had at least two Vtg isoforms. Contrary to the results of previous phylogenetic inference using Vtgs which indicate that insect lineage is most diverged and nematodes are closer to vertebrate lineage, our results show that nematodes and hexapods form two monophyletic sister groups. Another arthropod taxon, represented by a malacostracan crustacean, Penaeus japonicus, appears to be more closely related to the vertebrates than the hexapods. q
Molecular Biology and Evolution, 2002
It has been proposed that two events of duplication of the entire genome occurred early in vertebrate history (2R hypothesis). Several phylogenetic studies with a few gene families (mostly Hox genes and proteins from the MHC) have tried to confirm these polyploidization events. However, data from a single locus cannot explain the evolutionary history of a complete genome. To study this 2R hypothesis, we have taken advantage of the phylogenetic position of the lamprey to study the history of gene duplications in vertebrates. We selected most gene families that contain several paralogous genes in vertebrates and for which lamprey genes and an out-group are known in databases. In addition, we isolated members of the nuclear receptor superfamily in lamprey. Hagfish genes were also analyzed and found to confirm the lamprey gene analysis. Consistent with the 2R hypothesis, the phylogenetic analysis of 33 selected gene families, dispersed through the whole genome, revealed that one period of gene duplication arose before the lamprey-gnathostome split and this was followed by a second period of gene duplication after the lamprey-gnathostome split. Nevertheless, our analysis suggests that numerous gene losses and other genegenome duplications occurred during the evolution of the vertebrate genomes. Thus, the complexity of all the paralogy groups present in vertebrates should be explained by the contribution of genome duplications (2R hypothesis), extra gene duplications, and gene losses. cation was proposed to have occurred on the vertebrate lineage after the divergence of cephalochordates and the second after the divergence of jawless vertebrates (hagfish and lampreys; Holland et al. 1994; ). It has
Vitellogenin gene family in vertebrates: evolution and functions
The European Zoological Journal
The vitellogenin gene family is constituted of variable gene numbers encoding for polypeptides that are precursors of yolk proteins and derivatives in oviparous and ovoviviparous vertebrates. The comprehension of which mechanisms have shaped the evolution of vtg gene family represents an attractive field of research. The primary intent of this review is to summarize the evolutionary hypotheses that have been proposed over recent decades, highlighting the differences between the proposed models. Overall in vertebrates the evolutionary history of this gene family is the result of complex modifications deeply influenced by events such as Whole Genome Duplications (WGDs), lineage-specific gene losses and duplications. Interestingly the last hypothesis allowed to date the vitellogenin gene cluster origin in the common ancestor of gnathostomes. In addition, in the last decades, several works evidenced non-nutritional functions such as antibacterial, immunological and antioxidant activities overcoming its classical view as a simple source of nourishment for the developing embryos.
Nature, 2004
Tetraodon nigroviridis is a freshwater puffer fish with the smallest known vertebrate genome. Here, we report a draft genome sequence with long-range linkage and substantial anchoring to the 21 Tetraodon chromosomes. Genome analysis provides a greatly improved fish gene catalogue, including identifying key genes previously thought to be absent in fish. Comparison with other vertebrates and a urochordate indicates that fish proteins have diverged markedly faster than their mammalian homologues. Comparison with the human genome suggests ,900 previously unannotated human genes. Analysis of the Tetraodon and human genomes shows that whole-genome duplication occurred in the teleost fish lineage, subsequent to its divergence from mammals. The analysis also makes it possible to infer the basic structure of the ancestral bony vertebrate genome, which was composed of 12 chromosomes, and to reconstruct much of the evolutionary history of ancient and recent chromosome rearrangements leading to the modern human karyotype.
Gene duplications and the origins of vertebrate development
Development (Cambridge, England). Supplement, 1994
All vertebrates possess anatomical features not seen in their closest living relatives, the protochordates (tunicates and amphioxus). Some of these features depend on developmental processes or cellular behaviours that are again unique to vertebrates. We are interested in the genetic changes that may have permitted the origin of these innovations. Gene duplication, followed by functional divergence of new genes, may be one class of mutation that permits major evolutionary change. Here we examine the hypothesis that gene duplication events occurred close to the origin and early radiation of the vertebrates. Genome size comparisons are compatible with the occurrence of duplications close to vertebrate origins; more precise insight comes from cloning and phylogenetic analysis of gene families from amphioxus, tunicates and vertebrates. Comparisons of Hox gene clusters, other homeobox gene families, Wnt genes and insulin-related genes all indicate that there was a major phase of gene dup...
The "Fish-Specific" Hox Cluster Duplication Is Coincident with the Origin of Teleosts
Molecular Biology and Evolution, 2005
The Hox gene complement of zebrafish, medaka, and fugu differs from that of other gnathostome vertebrates. These fishes have seven to eight Hox clusters compared to the four Hox clusters described in sarcopterygians and shark. The clusters in different teleost lineages are orthologous, implying that a Òfish specificÓ Hox cluster duplication has occurred in the stem lineage leading to the most recent common ancestor of zebrafish and fugu. The timing of this event, however, is unknown. To address this question, we sequenced four Hox genes from taxa representing basal actinopterygian and teleost lineages, and compared them to known sequences from shark, coelacanth, zebrafish and other teleosts. The resulting gene genealogies suggest that the Òfish specificÓ Hox cluster duplication occurred coincident with the origin of crown group teleosts. In addition, we obtained evidence for an independent Hox cluster duplication in the sturgeon lineage (Acipenserifornes). Finally, results from HoxA11 and HoxB5 suggest that duplicated Hox genes have experienced strong diversifying selection immediately after the duplication event. Taken together, these results support the notion that the duplicated Hox genes of teleosts were causally relevant to adaptive evolution during the initial teleost radiation.
Crustaceana, 2019
Crustacean vitellogenesis is a process that involves Vitellin, produced via endoproteolysis of its precursor, which is designated as Vitellogenin (Vtg). The Vtg gene, mRNA and protein regulation involve several environmental factors and physiological processes, including gonadal maturation and moult stages, among others. Once the Vtg gene, mRNAs and protein are obtained, it is possible to establish the relationship between the elements that participate in their regulation, which could either be species-specific, or tissue-specific. This work is a systematic analysis that compares the similarities and differences of Vtg genes, mRNA and Vtg between the crustacean species reported in databases with respect to that obtained from the transcriptome of Callinectes arcuatus, C. toxotes, Penaeus stylirostris and P. vannamei obtained with MiSeq sequencing technology from Illumina. Those analyses confirm that the Vtg obtained from selected species will serve to understand the process of vitellogenesis in crustaceans that is important for fisheries and aquaculture. RESUMEN La vitelogénesis de los crustáceos es un proceso que involucra la vitelina, producida a través de la endoproteólisis de su precursor llamado Vitelogenina (Vtg). La regulación del gen Vtg, los ARNm y la Vtg involucra factores ambientales y procesos fisiológicos, incluyendo: maduración gonadal, etapas de muda, entre otros. Con el gen Vtg, los ARNm y la proteína obtenidos, es posible correlacionar los elementos que participan en su regulación, pudiendo ser especie-específicos o tejido-específicos. Este trabajo es un análisis sistemático que compara las similitudes y diferencias