An evolutionary hypothesis suggested by studies of the genome of the tiger pufferfish Takifugu rubripes has now been confirmed by comparison with the genome of a close relative, the spotted green pufferfish Tetraodon nigroviridis. Ray-finned fish underwent a whole-genome duplication some 350 million years ago that might explain their evolutionary success

Van de Peer, Yves

English

PubMed

Ghent University Academic Bibliography

Genome Biology 2004, 5:250commentreviewsreportsdeposited researchinteractionsinformationrefereed researchMinireviewTetraodon genome confirms Takifugu findings: most fish areancient polyploids Yves Van de PeerAddress: Bioinformatics and Evolutionary Genomics, Vlaams Interuniversitair Instituut voor Biotechnologie (VIB), Ghent University,Technologiepark 927, B-9052 Ghent, Belgium. E-mail: yves.vandepeer@psb.ugent.beAbstractAn evolutionary hypothesis suggested by studies of the genome of the tiger pufferfish Takifugurubripes has now been confirmed by comparison with the genome of a close relative, the spottedgreen pufferfish Tetraodon nigroviridis. Ray-finned fish underwent a whole-genome duplicationsome 350 million years ago that might explain their evolutionary success. Published: 25 November 2004Genome Biology 2004, 5:250The electronic version of this article is the complete one and can befound online at http://genomebiology.com/2004/5/12/250© 2004 BioMed Central Ltd In 1993, Sydney Brenner and colleagues [1] proposedsequencing the pufferfish genome as a cost-effective way toidentify and characterize human genes. The genome of thepufferfish is only about one-eighth of the size of that ofhuman but was expected to contain a similar gene reper-toire. Ten years later, not only has a draft genomesequence been released for Takifugu rubripes (Fugu, alsoknown as the Japanese or tiger pufferfish) [2], but also forTetraodon nigroviridis (green spotted pufferfish) [3], aclose relative that diverged from Takifugu 18-30 millionyears ago (Mya). By comparing the two pufferfish genomeswith that of human, several hundred novel human geneshave already been uncovered, as was predicted by Brennerand colleagues [1]. But the pufferfish genome sequencingprojects have also yielded a surprising finding: ray-finnedfish (Actinopterygii), such as pufferfish might have moregenes than lobe-finned fish (coelacanths and lungfish) andland vertebrates, because of additional gene-duplicationevents [4]. The recent release of the Tetraodon genomesequence [3] provides overwhelming evidence that agenome-duplication event did indeed occur early in theevolution of ray-finned fish.A fish-specific genome duplication Some of the first data pointing to a possible genome duplica-tion in fish came from Hox genes and Hox gene clusters. Hoxgenes encode DNA-binding proteins that specify cell fatealong the anterior-posterior axis of bilaterian animalembryos and occur in one or more clusters of up to 13 genes.Whereas lobe-finned fish, amphibians, reptiles, birds andmammals have four clusters, extra Hox gene clusters havebeen discovered in zebrafish, Medaka, Nile tilapia andpufferfish [4]. The observation that such distantly relatedspecies [5] all have seven or eight Hox gene clusters sug-gested the occurrence of an additional genome-duplicationevent in the ray-finned fish lineage before the divergence ofmost teleost (bony fish) species. More recent comparativegenomic studies have turned up many more genes and geneclusters for which there are two copies in fish but one inother vertebrates [6]. The findings that different paralogouspairs seem to have originated at about the same time, thatdifferent fish species seem to share ancient gene duplica-tions, and that different paralogs are found on differentlinkage groups in the same order as other duplicated genes,all support the hypothesis that these genes arose through alarge-scale gene-duplication event. It is worth noting,however, that some authors have argued that an ancestralwhole-genome-duplication event was not responsible for theabundance of duplicated fish genes [7]. Additional evidence for a genome duplication in ray-finnedfish was provided by analyzing the complete Takifugugenome, a draft sequence of which was published in 2002[2]. Two recent studies identified duplicated genes in thisgenome and used phylogenetic trees to estimate the ages ofthese duplicates [8,9]. Vandepoele et al. [8] constructedphylogenetic trees for all gene families containing betweentwo and ten duplicated Takifugu genes, which amounts to atotal of 3,077 families. For each gene family, the relativedate of duplication events was determined to test whethergene duplications occurred before or after the split betweenfish and land vertebrates. To this end, neighbor-joiningtrees were created for each of the Takifugu gene familieswith homologous sequences from mouse and human.Absolute dating of duplication events was achieved throughinference from linearized trees [10]. In such trees - wherebranch length is directly proportional to time - the splitbetween ray-finned fish and land vertebrates, dated at 450Mya, was used as a calibration point for the dating of gene-duplication events. A major fraction (about one-third) ofthe duplicated genes in Takifugu could be ascribed to alarge-scale gene-duplication event specific to the fishlineage, which was estimated to have occurred about 320Mya (Figure 1). A very similar approach was followed for the analysis of theTakifugu genome by Christoffels et al. [9], who obtainedessentially the same result: by constructing linearized trees,the whole-genome-duplication event was estimated to haveoccurred approximately 350 Mya. To test whether thesudden increase in the number of duplicated genes in theTakifugu genome was the result of an entire-genomeduplication rather than an increased rate of independenttandem-duplication events, both Vandepoele et al. [8] andChristoffels et al. [9] investigated the appearance of dupli-cated genes in duplicated blocks on chromosomes. Statisti-cally significant regions of micro-colinearity were identifiedwithin the complete Takifugu genome, showing the samegene content and gene order. Indeed, both studies reported alarge number of duplicated genes in so-called paralogons -homologous genomic segments that can be proved to havebeen created by duplication [11] - and concluded that mostfindings were congruent with a large-scale, probably whole-genome duplication event in a ray-finned ancestor that gaverise to the Takifugu and other fish lineages.Comparing genomes Because of the highly fragmented nature of the initial Takifugugenome assembly, it was difficult to prove that the large-scale gene-duplication event had indeed affected the wholegenome. The recent release of the well-assembledTetraodon genome [3] seems to have settled this issue intwo ways. First, Jaillon et al. [3] analyzed the chromoso-mal distribution of ancient duplicates and observed thatgenes on one chromosome have a strong tendency to haveduplicate copies on a single other chromosome. As wouldbe expected from a whole-genome-duplication event, allchromosomes are involved. Second, by using a compara-tive approach in which they compared the Tetraodongenome with that of human, which has not undergone thegenome-duplication event (Figure 1), Jaillon et al. [3]showed that almost every region in the human genomeclearly corresponds to two regions in the Tetraodongenome. This type of comparative analysis (Figure 2) hasproved very powerful for unveiling genome-duplicationevents. Recently, such an approach provided overwhelmingevidence for the long-suggested [12], but contested (see,for example, [13]) ancient whole-genome duplication in theyeast Saccharomyces cerevisiae, by comparing its genomewith that of different relatives that diverged prior to theduplication events [14,15]. A comparative analysis between the human and Tetraodongenomes has also allowed inference of the basic structure ofthe ancestral bony vertebrate genome, and the reconstruc-tion of much of the evolutionary history of ancient andrecent chromosomal rearrangements leading to the modernhuman karyotype. By matching up the genes on theTetraodon chromosomes with homologs on human chromo-somes, Jaillon et al. [3] inferred that the ancestor of bothfish and land vertebrates had no more than 12 chromo-somes, a number that has been previously suggested on thebasis of linkage relationships between zebrafish, Medaka,and human [16]. Comparison of the genomes of Tetraodonand human also showed that chromosome evolution in both250.2 Genome Biology 2004, Volume 5, Issue 12, Article 250 Van de Peer http://genomebiology.com/2004/5/12/250Genome Biology 2004, 5:250Figure 1A phylogenetic tree showing the vertebrate phylogenetic relationshipsand superimposed pufferfish gene-duplication events. (a) A generallyaccepted tree illustrating the relationships between several vertebratespecies. The gray horizontal bar denotes the fish-specific genome-duplication event inferred from absolute dating of Takifugu paralogs. Thebroken line indicates the position of the duplicated copy of the Takifugugenome that originated between the divergence of gar and the bonytongues. (b) The bar chart shows the number of paralogous genes thatcould be dated through the construction of linearized trees. Modifiedfrom [8,9].MouseChickenFrogZebrafishTakifuguHumanTakifuguGar (Semionotiformes)Sturgeon (Acipenseriformes)Bony tongues (Osteoglossiformes)Bichir (Polypteriformes)Lobe-finned fish Land vertebrates andlobe-finned fishRay-finned fishTime (millions of years ago)Number of duplicates30252015105025 75 125175225275 325 375 425 475 525(a)(b)lineages differed considerably. Whereas all but one ofthe ancestral Tetraodon chromosomes had not undergoneinterchromosomal exchange for 450 Mya, only one humanchromosome was similarly undisturbed. A possible explana-tion for the difference in genome evolution might be themassive integration of transposable elements in the humangenome, with an increased overall frequency of chromosomebreaks as a result [3].Evolutionary implications As mentioned above, on the basis of previous analyses ofthe Takifugu genome, the whole-genome-duplication eventin fish is thought to have occurred somewhere between300 and 350 Mya [8,9]. An interesting question is whetherthis date correlates with a decisive period in the evolutionof the fish. For instance, if the genome duplication hadbeen responsible for the biological diversification and largenumber of ray-finned fish, as suggested previously [4,17], itmust have occurred prior to the radiation of most fish lin-eages. The class Actinopterygii includes more than 23,500species [18], of which the vast majority are teleosts or ray-finned fish. Interestingly, all older, more basal groups ofray-finned fish, namely Polypteriformes (bichirs),Acipenseriformes (sturgeons and paddlefish), Semionoti-formes (gars), and Amiformes (bowfin), have only a fewextant species (Figure 1). Most members of these basalactinopterygian lineages are considered to be ‘livingcommentreviewsreportsdeposited researchinteractionsinformationrefereed researchhttp://genomebiology.com/2004/5/12/250                                                     Genome Biology 2004, Volume 5, Issue 12, Article 250 Van de Peer  250.3Genome Biology 2004, 5:250Figure 2 Uncovering genome duplications through comparative analysis with related sequences. The hypothetical genomes of two related organisms are shown,each containing the same set of genes. Both genomes are initially identical, but the genome of Organism 1 is duplicated, resulting in a second identical setof chromosomes and genes. After some time, homologous chromosomes lose a different set of genes, keeping two copies for only a minority of theduplicated genes. For the sake of simplicity, the genome of Organism 2 is assumed to remain unchanged. Within Organism 1, the only evidence for aduplication event comes from the conserved order of the anchor points formed by genes 1 and 11 (indicated by boxed regions). Comparison with thegenome of Organism 2, however, shows a pattern of so-called ‘double conserved synteny’ where the duplicated nature of Organism 1 is revealed. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 151 2 3 4 5 6 7 8 9 10 11 12 13 14 151 2 3 4 5 6 7 8 9 10 11 12 13 14 15Organism 1 Organism 2Common ancestorSpeciationGenome duplicationGene loss1 2 3 4 5 6 7 8 9 10 11 12 13 14 151 4 5 7 9 11 12 142 3 61 8 10 11 13 151 2 3 4 5 6 7 8 9 10 11 12 13 141 4 5 7 9 11 12 14151 2 3 6 8 10 11 13 15fossils’, because their morphology has remainedunchanged over very long evolutionary time periods. In a recent study, Hoegg et al. [19] have tried to determinethe timing of the duplication event in relation to the origin oflineages of teleost and ‘nonteleost’ fish by sequencing threenuclear genes - fzd8, sox11 and tyrosinase - from sturgeons,gars, bony tongues, and a tenpounder. For these three genes,two copies have been described previously in derived teleostmodel species, such as zebrafish and pufferfish, but only oneorthologous copy has been found in tetrapods. The specificclustering of the genes in individual gene trees for thesethree genes and a dataset of concatenated genes support thehypothesis that the fish-specific genome-duplication eventtook place after the split of the Acipenseriformes and theSemionotiformes from the lineage leading to teleost fish, butbefore the divergence of Osteoglossiformes (bony tongues)and the other more derived groups of fish (Figure 1). This isin good agreement with the recent analyses of the Takifugugenome, as fossil data age the Semionotiformes at between245 and 286 million years, whereas molecular estimates forthe Amiiformes, which are of approximately the same age asthe Semionotiformes, hint at a separation from the Teleosteistem lineage about 367-404 Mya. Likewise, molecular datasuggest an age of 335 million years for the Osteoglossiformes[19]. The inferred relative and absolute dates for the fish-specific genome duplication event seem to separate thespecies-poor branching lineages from the species-richteleost lineages, providing evidence that the fish-specificgenome duplication might be related causally to an increasein species and morphological diversity. On the basis of isozyme studies, Werth and Windham [20]developed a model in which the ‘reciprocal silencing’ ofgenes in geographically separated populations wouldpromote speciation. A few years ago, this idea was revivedin a model called ‘divergent resolution’, in which the loss orsilencing of gene duplicates was postulated to be moreimportant for the evolution of species diversity than theacquisition of new functions by duplicated genes. Diver-gent resolution occurs when different copies of a dupli-cated gene are lost on different chromosomes in differentpopulations, thereby creating genetic barriers for repro-duction between them [21,22]. Divergent resolution andlineage-specific subfunction partitioning [17] can promoteincompatibility among populations within a species, andthus might facilitate evolutionary radiation. Gene duplica-tions might, therefore, bring about rapid speciation in pop-ulations fixed for different copies of a duplicated locus. Thefish-specific genome duplication has created many dupli-cates that could be divergently resolved. Potentially, suchgenes have played a prominent role in the radiation of theteleosts. Further studies of the genes encoded in these fishgenomes may shed light on how important the fish-specificwhole-genome duplication has been in the evolution of theray-finned fish.References1. Brenner S, Elgar G, Sandford R, Macrae A, Venkatesh B, Aparicio S:Characterization of the pufferfish (Fugu) genome as acompact model vertebrate genome. Nature 1993, 366:265-268.2. Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, Dehal P,Christoffels A, Rash S, Hoon S, Smit A, et al.: Whole-genomeshotgun assembly and analysis of the genome of Fugurubripes. Science 2002, 297:1301-1310.3. Jaillon O, Aury J-M, Brinet F, Petit J-L, Stange-Thomann N, MauceliE, Bouneau L, Fischer C, Ozoef-Costaz C, Bernot A, et al.:Genome duplication in the teleost fish Tetraodonnigroviridis reveals the early vertebrate proto-karyotype.Nature 2004, 431:946-957.4. Meyer A, Schartl M: Gene and genome duplications in verter-brates: the one-to-four (-to-eight in fish) rule and the evo-lution of novel gene functions. Curr Opin Cell Biol 1999,11:699-704.5. Chen W-J, Orti G, Meyer A: Novel evolutionary relationshipsamong four fish model systems. Trends Genet 2004, 20:424-431.6. Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer, Y: Genomeduplication, a trait shared by 22,000 species of ray-finnedfish. Genome Res 2003, 13:382-390.7. Robinson-Rechavi M, Marchand O, Escriva H, Laudet V: An ances-tral whole-genome duplication may not have been respon-sible for the abundance of duplicated fish genes. Curr Biol2001, 11:R458-R459.8. Vandepoele K, De Vos W, Taylor JS, Meyer A, Van de Peer Y:Major events in the genome evolution of vertebrates:paranome age and size differs considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci USA2004, 101:1638-1643.9. Christoffels A, Koh EG, Brenner S, Aparicio S, Venkatesh B: Fugugenome analysis provides evidence for a whole-genomeduplication early during the evolution of ray-finned fishes.Mol Biol Evol 2004, 21:1146-1151.10. Takezaki N, Rzhetsky A, Nei M: Phylogenetic test of the molecu-lar clock and linearized trees. Mol Biol Evol 1995, 12:823-833.11. Van de Peer Y: Computational approaches to unveilingancient genome duplications. Nat Rev Genet 2004, 5:752-763.12. Wolfe KH, Shields DC: Molecular evidence for an ancientduplication of the entire yeast genome. Nature 1997,387:708-713. 13. Llorente B, Durrens P, Malpertuy A, Aigle M, Artiguenave F, BlandinG, Bolotin-Fukuhara M, Bon E, Brottier P, Casaregola S, et al.:Genomic exploration of the hemiascomycetous yeasts: 20.Evolution of redundancy compared to Saccharomyces cere-visiae. FEBS Lett 2000, 487:122-133.14. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, MohrC, Pohlmann R, Luedi P, Choi S, et al.: The Ashbya gossypiigenome as a tool for mapping the ancient Saccharomycescerevisiae genome. Science 2004, 304:304-307.15. Kellis M, Birren BW, Lander ES: Proof and evolutionary analy-sis of ancient genome duplication in the yeast Saccha-romyces cerevisiae. Nature 2004, 428:617-624. 16. Naruse K, Tanaka M, Mita K, Shima A, Postlethwait J, Mitani H: AMedaka gene map: the trace of ancestral vertebrateproto-chromosomes revealed by comparative genemapping. Genome Res 2004, 14:820-828.17. Postlethwait P, Amores A, Cresco W, Singer A, Yan Y-L: Subfunc-tion partitioning, the teleost radiation and the annotationof the human genome. Trends Genet 2004, 20:481-490.18. Nelson J: Fishes of the World. New York: Wiley; 1994.19. Hoegg S, Brinkmann H, Taylor JS, Meyer A: Phylogenetic timingof the fish-specific genome duplication correlates withphenotypic and taxonomic diversification in fishes. J MolEvol 2004, 59:190-203.20. Werth CR, Windham MD: A model for divergent allopatricspeciation of polyploid pteridophytes resulting fromsilencing of duplicate gene expression. Am Nat 1991,137:515-526.21. Lynch M, Force A: The origin of interspecific genomic incom-patibility via gene duplication. Am Nat 2000, 156:590-605.22. Taylor JS, Van de Peer Y, Meyer A: Genome duplication,divergent resolution and speciation. Trends Genet 2001,17:299-301.250.4 Genome Biology 2004, Volume 5, Issue 12, Article 250 Van de Peer http://genomebiology.com/2004/5/12/250Genome Biology 2004, 5:250

Tetraodon genome confirms Takifugu findings : most fish are ancient polyploids

A: Genome duplication, divergent resolution and speciation. Trends Genet

A: Novel evolutionary relationships among four fish model systems. Trends Genet

A: Phylogenetic timing of the fish-specific genome duplication correlates with phenotypic and taxonomic diversification in fishes.

An ancestral whole-genome duplication may not have been responsible for the abundance of duplicated fish genes. Curr Biol

Aparicio S: Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature

Computational approaches to unveiling ancient genome duplications. Nat Rev Genet

DC: Molecular evidence for an ancient duplication of the entire yeast genome. Nature

ES: Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature

et al.: Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature

Fishes of the World.

Force A: The origin of interspecific genomic incompatibility via gene duplication. Am Nat

Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol Biol Evol

Gene and genome duplications in verterbrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol

Genomic exploration of the hemiascomycetous yeasts: 20. Evolution of redundancy compared to Saccharomyces cerevisiae. FEBS Lett

H: A Medaka gene map: the trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping. Genome Res

Major events in the genome evolution of vertebrates: paranome age and size differs considerably between rayfinned fishes and land vertebrates. Proc Natl Acad Sci USA

MD: A model for divergent allopatric speciation of polyploid pteridophytes resulting from silencing of duplicate gene expression. Am Nat

Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol

The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science

Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science

Y-L: Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet

Y: Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res

http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=545788

Tetraodon genome confirms Takifugu findings : most fish are ancient polyploids

Abstract

Similar works

Full text

Available Versions

Ghent University Academic Bibliography