Evolution and differential expression of a vertebrate vitellogenin gene cluster
© Finn et al; licensee BioMed Central Ltd. 2009
Received: 23 July 2008
Accepted: 05 January 2009
Published: 05 January 2009
The multiplicity or loss of the vitellogenin (vtg) gene family in vertebrates has been argued to have broad implications for the mode of reproduction (placental or non-placental), cleavage pattern (meroblastic or holoblastic) and character of the egg (pelagic or benthic). Earlier proposals for the existence of three forms of vertebrate vtgs present conflicting models for their origin and subsequent duplication.
By integrating phylogenetics of novel vtg transcripts from old and modern teleosts with syntenic analyses of all available genomic variants of non-metatherian vertebrates we identify the gene orthologies between the Sarcopterygii (tetrapod branch) and Actinopterygii (fish branch). We argue that the vertebrate vtg gene cluster originated in proto-chromosome m, but that vtg genes have subsequently duplicated and rearranged following whole genome duplications. Sequencing of a novel fourth vtg transcript in labrid species, and the presence of duplicated paralogs in certain model organisms supports the notion that lineage-specific gene duplications frequently occur in teleosts. The data show that the vtg gene cluster is more conserved between acanthomorph teleosts and tetrapods, than in ostariophysan teleosts such as the zebrafish. The differential expression of the labrid vtg genes are further consistent with the notion that neofunctionalized Aa-type vtgs are important determinants of the pelagic or benthic character of the eggs in acanthomorph teleosts.
The vertebrate vtg gene cluster existed prior to the separation of Sarcopterygii from Actinopterygii >450 million years ago, a period associated with the second round of whole genome duplication. The presence of higher copy numbers in a more highly expressed subcluster is particularly prevalent in teleosts. The differential expression and latent neofunctionalization of vtg genes in acanthomorph teleosts is an adaptive feature associated with oocyte hydration and spawning in the marine environment.
A defining feature of the early development of non-eutherian vertebrates is a cleidoic egg endowed with variable amounts of yolk. Until very recently, the major products of the vitellogenin (vtg) genes that encode yolk proteins have been considered to be simple precursors of the energy reserve of vertebrate eggs, but the latest studies have demonstrated several non-nutritional roles for Vtg [1, 2]. Similarly, the recent observation that remnants of vtg genes exist in Eutheria, including humans, but have sequentially been lost through co-evolution with casein genes  elegantly demonstrated that the three known vtg genes in birds represent a conserved gene complement. In a previous study, Finn & Kristoffersen  proposed a model for the evolution and neofunctionalization of vtg genes in acanthomorph teleosts. We identified vtgC as an ancestral gene, and argued that the dual vtgAa/vtgAb system, first noted by La Fleur et al.  was derived from a single form, the A-type vtg. In this model, the separation of the vtgC- and vtgA-type genes occurred following the second round (R2) of whole genome duplication (WGD). Subsequently vtgA duplicated and formed paragolous vtgAa and vtgAb genes in acanthomorph teleosts. This phylogenetic model has been corroborated by other investigators . Most recently however, Babin  has provided a syntenic map of vertebrate vtg genes, which shows that the three forms of vtg are encoded in a vtg gene cluster (VGC) in non-eutherian vertebrates. A major goal of the present study was to integrate the statistical, biochemical and physical models of vtg gene evolution in vertebrates.
Through a series of studies, we and other laboratories have shown that the pelagic nature of a marine teleost egg is an evolved feature  that primarily results from the maturational influx of water due to differential degradation of VtgAa-type yolk proteins (Yp), and the temporal insertion of novel aquaporins (Aqp1b) in the microvillous portion of the plasmalemma [8–10]. The neofunctionalization of the vtgAa form in acanthomorph teleosts, has sensitized the heavy chain domain (LvH-Aa) to catheptic proteolysis that generates a large organic osmolyte pool of free amino acids (FAA) in the ovulated egg [1, 9, 11–19]. In contrast the LvH domains derived from vtgAb and vtgC genes may be partially cleaved, but remain mostly intact following the maturational proteolytic event, and thus contribute minimally to oocyte hydration [1, 12, 14, 17, 18]. In teleosts that spawn benthic eggs (benthophils), a character that we have argued to be the ancestral condition due to an ancient freshwater heritage (Finn & Kristoffersen, 2007), Yps may be cleaved or partially processed to generate a small pool of FAA during oocyte hydration [6, 20–24].
In order to reconcile the differences in the phylogenetic, biochemical and syntenic models we have examined the evolution and expression of the vtg gene complement in modern (Perciformes: Labridae) and old (Clupeocephala: Clupeidae) teleosts that spawn pelagic and benthic eggs. We were interested in determining how the expression of different vtg transcripts relates to the character of the egg in a single family of closely related teleosts, and whether lineage-specific gene duplication resulted in neofunctionalization of the Aa-type vtgs. To determine the orthologies and ancestry of the novel labrid vtg genes cloned in the present study, we anchored the results of phylogenetic inference with the syntenic arrangement of genomic vtgs in model vertebrates. This approach allowed us to identify the proto-chromosomal origin of the VGC that is conserved between the Actinopterygii (fish branch) and the Sarcopterygii (tetrapod branch). It further allowed us to conclude that neofunctionalization of the vtgAa genes in acanthomorph teleosts occurred long after the duplication event.
Results and discussion
Within the labrid species, sequences had highest identities to their homologs in closely related goldsinny wrasse. Since only a single Ab-type transcript was detected in cuckoo wrasse, and it showed 100% identity to the novel cevtgAb2 and crvtgAb2 sequences over the ~250 aligned aa and ~750 aligned nt (Fig. 3), we named the cuckoo wrasse Ab-type sequence lmvtgAb2.
The present analyses thus fully corroborate our earlier study of vertebrate vtgs  wherein the major and minor transcripts cluster according to taxonomic group. We further verified the inferred duplication of the vtgAa and vtgAb clusters using the method of Zmasek and Eddy . Hence the tree topology is inconsistent with the syntenic arrangement of vertebrate vtg genes, and suggests that different functions have evolved within the major clades. Specifically for acanthomorph teleosts, the LvH-Aa domains have evolved a sensitivity to acidic degradation following activation of V-class proton pumps during oocyte maturation [1, 9, 11–13, 15, 17, 18]. The data for labrid teleosts that spawn benthic and pelagic eggs support this view [[19, 20], see below].
In order to understand the disparity between the phylogenetic and syntenic arrangement of vertebrate vtg genes, we increased the phylogenetic data set to include all known sarcopterygian vtgs (108 sequences, containing ~370 k nt), including amphibian, bird, reptile and platypus variants. In addition we examined the syntenic positions of vtg genes within non-metatherian vertebrates. The larger data set did not affect the topology of the teleost branches, but did place ggvtgI and the partial platypus transcript (ENSOANT00000031211) at the base of the tetrapoda and closer to, but on a separate branch to teleost vtgC variants (data not shown). Similarly, two further partial platypus transcripts (ENSOANT00000008462 and a construct of ENSOANT00000013101-ENSOANT00000013100) clustered as a basal node to ggvtgIII and ggvtgII, but after amphibian variants. These findings agree with the recent studies of Brawand et al.  and Babin  who demonstrated that three genes exist in monotremata and are putative orthologs of the three bird genes. Since these latter platypus genes are not yet localized to any chromosome, but are annotated in contigs 49.51 and 49.49, respectively, it was not possible to discern their true orthology, or syntenic arrangement in relation to chicken. However, by combining the results of the present phylogenetic data with the syntenic positions of the chicken and teleost vtgs, it can be stated that teleost vtgC genes are the putative orthologs of ggvtgI, and that teleost vtgAa and vtgAb genes are the putative orthologs of ggvtgII and ggvtgIII, respectively.
Previously we showed that the evolution of Vtg sub-domains is neither clock-like, nor under strong functional constraint . We further highlighted the disparate retention of the sub-domain structures of the mature proteins. Teleost VtgC proteins have all lost the highly phosphorylated polyserine Pv region and the C-terminal domains that are homologous to human VWFD. In chicken, however, all three Vtgs, including GgvtgI, are complete type proteins containing all encoded domains. The same appears to be true for other tetrapod Vtgs, exemplified by amphibia and the platypus, although Brawand et al.  have shown that premature stop codons or indels have led to loss of function in ggvtgII/III orthologs in the platypus. The loss of sub-domains in teleosts is not restricted to the VtgC class. Amongst all ostariophysan teleosts, which represent the second largest superorder of fishes [31–33], the major gene expressed encodes a truncated form of Vtg that lacks the Vwfd region [26, 27, 34–36]. However, a complete-type gene is present in zebrafish as vtg2, and a novel juxtaposed gene (vtg8) encodes a protein that lacks the Pv and CT domains, i.e. a tripartite protein (NH2-LvH-LvL-β'-COOH). To address the vtg orthologies in Ostariophysi, we thus included all known zebrafish coding variants in the phylogenetic data set and examined their loci.
To ascertain the local cis-duplication events, we integrated the results of the phylogentic analyses. The topology of the ZfVTG1-8 shown in Fig. 4 precisely replicates the chromosomal loci of each gene in the genome shown in Fig. 5. This is also true for the meadaka VGC, where olvtgAa2 represents an internal duplication of the independently sequenced olvtgAa1 (Q8UW88_ORYLA). In fact each of the major genes that are expressed in vertebrates are located at the outer edge of the ggvtgII/III and vtgAa/Ab VGC. This arrangement appears to have implications for the differential expression of the cluster, where cis-regulatory elements associated with estrogen induction [43, 44] and recruitment of the transcription initiation complexes are concerned.
The selected model of labrid teleosts are best known for their cleaning behaviour, a character that is currently being exploited as an environmentally-friendly means of biological control of ectopic parasites in mariculture. Members of this family, the third largest of vertebrates  with more than 600 species in 82 genera  are also known for their remarkable sex lives , where sex change, transvestitism and male-dominated parental care is prevalent. Although only one species spawns pelagic eggs in the temperate coastal waters of our Norwegian study area, it is noteworthy that all labrid teleosts are marine species, with the vast majority spawning pelagic eggs in a subtropical environment . An understanding of the differential expression in the non-disrupted vtg-gene complement in this family of fishes is an important step towards development of sex-specific molecular markers for this group.
Probes were designed from the highly conserved N-terminal area of each cDNA sequence and their gene specificity verified by subsequent cloning and sequencing. With the exception of crvtgAb2, a single band of relevant size was detected after hybridization in each species. Although several levels of regulation lie between an expressed hepatic transcript and deposited Yp product in the growing oocyte, it is noteworthy that vtg band intensities were highly correlated to the type of Yp deposited in the oocytes and the pelagic or benthic nature of the spawned egg. For the goldsinny wrasse, which spawns pelagic eggs and generates the largest pool of FAA during oocyte hydration, an exceptional level of vtgAa is expressed in the liver compared to the other vtg transcripts. These data strongly support our earlier findings where virtually all of the oocyte Yps are maturationally proteolysed to FAA that subsequently drive the osmotic flow of water into the highly hydrated egg . In the benthophil rock cook, more even band intensities of the four vtg transcripts are found, although higher levels of vtgAa are also expressed in this species. The rock cook is a close relative of the corkwing wrasse (Crenilabrus melops), which generates a small pool of FAA from partial Yp proteolysis during oocyte hydration . We have recently conducted a proteomic analysis of the oocyte and egg Yps in the rock cook and cuckoo wrasse and found that moderate oocyte hydration is associated with proteolysis of mainly vtgAa derived Yp products (Kolarevic unpublished data). In cuckoo wrasse, a species that spawns benthic eggs and shows very limited maturational proteolysis, higher levels of VtgAb-type Yps are deposited in the oocyte. These latter observations are further supported by the fact that although greater amounts of RNA were inadvertently loaded in the vtgAa lane, the vtgAb2 band had the highest intensity. The significance of higher expression levels of Ab-type vtgs relates to the fact that these genes have not neofunctionalized  and their Yp products remain mostly intact in the hydrated egg as the major protein reserve for the developing embryo. Taken together, these data are in line with the notion that differential expression of non-neofunctionalized and neofunctionalized vtgs in acanthomorph teleosts is related to the benthic or pelagic character of the spawned egg.
We find that labrid teleosts differentially express up to four vtg genes that are orthologous to an ancient vtg gene cluster that existed prior to the separation of Actinopterygii from Sarcopterygii. With the exception of zebrafish, the vertebrate vtg gene cluster remains linked on single chromosomes that arose in close association with the second round of whole genome duplication (WGD) >450 million years ago. Our model for lineage-specific duplication of the major vtg genes in teleosts shows that they comprise a variable subcluster. The copy number of this variable subcluster, which comprises the ggvtgIII/vtgAb and ggvtgII/vtgAa orthologs, is likely to be the combined result of the third round of WGD in teleosts with subsequent gene loss due to chromosomal rearrangements followed by lineage-specific gene duplications. The topology of the phylogenetic tree for the 8 zebrafish vtg genes precisely replicates their chromosomal loci in the genome and suggests that lineage-specific duplications can occur within the teleost subcluster. The expression data for the labrid transcripts demonstrated that the more ancestral vtgC genes that are orthologous to chicken ggvtgI are the least expressed and we argue that these minor genes have functionally diverged in the teleost lineage due to loss of the Pv and C-terminal domains. In the closely related family of labrid teleosts, the expression ratios of the major vtgAb and neofunctionalized vtgAa transcripts reflect the benthic or pelagic character of the spawned egg.
Mature female cuckoo wrasse (Labrus mixtus), rock cook (Crenilabrus exoletus) and goldsinny wrasse (Ctenolabrus rupestris) were collected using traps and gill nets in the costal waters near Bergen, Norway. Fish were transported live to the laboratory and maintained in fish tanks. Later they where euthanized in accordance with the International Guiding Principles for Biomedical Research Involving Animals as promulgated by the Society for the Study of Reproduction. Subsequent sampling of livers and ovaries was performed in a cold room (4°C). Pre-hydrated oocytes (PH ooc) and ovulated eggs (OV egg) were dissected from the ovaries and processed as described previously .
Total RNA was isolated from vitellogenic livers of three rock cook females using RNAeasy kit (Qiagen). Extracts were subsequently mixed together for single strand 3' and 5'-cDNA synthesis using Smart Race cDNA Amplification kit (Clonetech, http://www.clonetech.com). The alignment of Finn & Kristoffersen  was used to select areas that were specific to each form of vtg. Gene specific primers (GSP) (see Additional file 2) subsequently designed from nt sequences of red seabream vtgAa, vtgAb and vtgC (primers P1, P11 and P21) were then used to run 3' and 5'-RACE polymerase chain reactions (PCR) as recommended by the manufacturer.
A PCR product of approximately 4000 bp was amplified using sense primer P1. It was cloned and sequenced as described previously . Three sense primers (P2–P4) designed from a partial rock cook sequence were used in addition to M13 vector primers to obtain the sequence of the cloned product. In order to sequence the remaining N-terminal area of this gene, a new antisense GSP (P5) was constructed from the aforementioned sequence. The RACE PCR product (~1300 bp) was cloned and bi-directionally sequenced.
An antisense GSP for red seabream vtgAb (P11) was used in a 5'-RACE PCR together with single stranded rock cook 5'-cDNA giving ~800 bp long PCR product. After cloning and sequencing, two different ESTs were identified to match the N-terminal end of vtgAb in other teleost species using BLAST. To verify that the ESTs represent two novel products, the same experiment was conducted with new total RNAs that were extracted from two females and independently used for single strand cDNA synthesis. PCR products from both reactions were gel-purified, cloned and sequenced giving the same two distinct vtgAb sequences. Full sequence of vtgAb1 was achieved by primer walking with five sense rock cook GSPs (P12–P16). An additional sense GSP (P17) was used to obtain the remaining part of the partial vtgAb2 sequence.
Cloning of vtgC was accomplished using an antisense GSP made from red seabream nt sequence (P21) and a sense primer (P22) designed from rock cook ESTs. A PCR product of approximately 3500 bp was amplified using the latter primer and was sequenced with M13 vector primers and three additional sense primers (P23–P25).
The same extraction procedures and sequencing strategies were employed to retrieve full-length sequences of three different vtg forms in cuckoo wrasse. Cloning of PCR products amplified with the same red seabream GSPs (P1, P11 and P21) as for rock cook, gave partial sequences that were used to construct new vtgAa (P6–P10), vtgAb (P18–P20) and vtgC (P26–P29) primers. Subsequent PCR reactions, cloning and sequencing of new PCR products were done as described above. Despite using GSPs for both vtgAb types in rock cook wrasse (P12 and P13), only a single vtgAb2 transcript was obtained.
Total RNA was extracted from each of the labrid teleost livers, as described above, and electrophoretically fractioned in 1% agarose gels containing formaldehyde (6.7%), stained with ethidium bromide solution to visualize rRNAs and blotted onto a Hybond-N nylon membrane (Amersham) by capillary transfer in 10 × SSC and covalently linked to the membrane by exposure to the UV light. Membranes were prehybridized in hybridization buffer (PerfectHyb™ Plus, Sigma) at 68°C for 60 min before being hybridized with denatured and labeled 32P-cDNA probes (Strip-EZ DNA, Ambion) overnight as described previously .
Four vtg gene specific probes for rock cook and three for cuckoo and goldsinny wrasse ranging is size from 602 to 736 nt were constructed from the N-terminal regions. To verify probe specificity, each was sequenced following amplification, gel purification, and excision. Blots were rinsed two times with 2 × SSC/0.1% SDS for 5 min and once with 1 × SSC/0.1% SDS for 15 min at the room temperature. Additional washing was done with 0.1 × SSC/0.1% SDS twice for 10 min at 68°C. In order to detect the signals, membranes were exposed to Kodak's BioMax MS film for 2 hr.
Multiple sequence alignments of the deduced amino acids were used to generate codon alignments of the sequenced transcripts as described previously . In order to determine gene orthologies, vtg genes from each of the currently sequenced teleost genomes were accessed from the ensembl servers (zebrafish, medaka, 3-spined stickleback, torafugu and spotted green pufferfish: ensembl release 49, May 2008). For zebrafish, 8 genes were identified using the graphical view and contiguous alignments of transcripts, of which 2 are located in genbank (see Additional file 1 for accession numbers). For medaka, Babin  annoted 5 genes on chromosome 4, however, we only found evidence of 4 vtg genes, 3 of which are located between bp 9,868,166 – 9,974,743. A novel construct (olvtgAa2) was assembled from transcripts: ENSORLESTT00000013001, ENSORLT00000007668, ENSORLESTT00000012994, ENSORLESTT00000012967, ENSORLESTT00000012953 that encoded a protein of 1671 aa. Similarly, a novel construct for 3-spined stickleback (gavtgAb) was assembled from transcripts ENSGACT00000012852 and ENSGACT00000012880 located between bp 12,491,853 – 12,515,240 in group VIII. To provide greater statistical support, the novel sequences from the labrid species were aligned with the genomic variants and other vertebrate taxa for which vtg sequences are known (see Additional file 1).
Phylogenetic reconstruction was performed using Bayesian (Mr Bayes 3.1.2: 4 × mcmc chains, 1,000,00 generations, sample frequency 100, burnin 3500; , maximum parsimony and neighbour joining (PAUP 4.0b10: 1,000 bootstraps; ) analyses of the amino acid and codon alignments, and maximum likelihood analyses of the codon alignments as described by Finn & Kristoffersen .
The Research Council of Norway (project #178837/40), the University of Bergen and the Norwegian Ministry of Education (JK: Quota Program) are thanked for their financial support.
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