Trends in Genetics
Reconstruction of a 450-My-old ancestral vertebrate protokaryotype
Introduction
The genomes of different mammalian species are far more similar than has been expected from their karyotypic diversity. Overall these genomes share a similar number of ∼24 500–26 000 genes [1]. Mapping of orthologous genes and comparative painting techniques using DNA probes from single chromosomes has enabled the reconstruction of an ancestral eutherian founder karyotype from ∼100 million years ago (Mya) 2, 3, 4, 5, 6. These reconstructions are based on ancestral chromosome characteristics shared between extant mammalian species. Most informative for these reconstructions are genomes from species with highly conserved karyotypes [4]. It was surprising to realize that the human karyotype is similar to this ancestral karyotype, implying that no major karyotype change occurred during the evolution of humans in the past 100 My.
Similar comparisons have also been performed between the karyotypes of different fish species and human 7, 8, 9, 10, 11. With the availability of the chicken genome [12] as a connecting link between mammals and fish, it is now possible to reconstruct the protokaryotype of a common vertebrate ancestor that lived 450 Mya. Because of the greater DNA divergence rate, chromosomal painting techniques are not applicable when comparing different vertebrate genomes. For karyotype reconstructions one has to switch to in silico analysis and search for shared ancestral syntenies of genes across multiple species. To do this, we established a gene orthology database containing ∼3300 genes at a density of one gene per Mb along all human (Homo sapiens, HSA) chromosomes. This database contains human genes and their orthologous genes together with their chromosomal assignment from chicken (Gallus gallus, GGA), green spotted pufferfish (Tetraodon nigrovirides, TNI) and zebrafish (Danio rerio, DRE). This database is an extension of the one we used previously to reconstruct the ancestor of the mammalian X chromosome [13]. Genes from chicken and fish were considered to be orthologous to the respective human gene if reciprocal BLAST best-hit searches identified them as such in the Ensembl database (Table S1 in supplementary online material). Another 801 genes were added from a third fish species, medaka (Oryzias latipes, OLA) [9]. Table 1 shows the numbers of orthologous genes that could be unequivocally identified in each genome. Because the chicken [12], pufferfish [10] and zebrafish genome analyses are still incomplete, the number of orthologous genes retrieved for each species differs. This database, which is described in more detail in Box 1, can be used for electronic chromosome painting (E-painting), which is highly informative. By E-painting conserved syntenies (for a definition, see Box 1) are identified and used to reconstruct the ancestral vertebrate protokaryotype. For the comparison only synteny groups with three or more genes in the sample were considered. First, the karyotype of the early tetrapod (TET), which is ancestral to both birds and mammals, was reconstructed. Second, a reconstruction was performed of the karyotype of an ancestral teleost fish (TEL), which lived before the extra whole-genome duplication that is characteristic for the teleost fish genomes 10, 14. Finally, a common early vertebrate (VER) protokaryotype from 450 Mya was established.
Section snippets
Reconstruction of the ancestral tetrapod protokaryotype
The reconstruction of the tetrapod karyotype was based on chicken and human genome data including the conserved chromosome characteristics that had already guided the reconstruction of the ancestral eutherian karyotype (e.g. Refs 2, 6). The following syntenic associations of neighboring chromosomal segments of the ancestral eutherian karyotype are also present in the chicken genome: 1/19p, 3/21, 4/8p, 7/16p, 12/22 (2 chromosomes), 14/15, 16q/19q (Table 2). Therefore, these associations and the
Reconstruction of the teleost protokaryotype
Next we deduced the protokaryotype of an ancestral teleost fish that lived before the third and extra round of whole-genome duplication 10, 14. Again, only synteny segments with three or more genes in the sample were considered. Genome data from pufferfish [10] and medaka [9] provided most of the information.
The principle used to reconstruct the teleost protokaryotype is illustrated in Figure 2 (Table 2, and Table S2 in supplementary online material). For simplicity, chromosomes are presented
Reconstruction of the vertebrate protokaryotype
For the final reconstruction of the 450-My-old ancestral vertebrate protokaryotype (VER) no outgroup species is available to date. Two slightly different procedures, not independent of each other, were followed.
To begin we went back to the original mapping data in human, chicken, pufferfish and zebrafish as given in Table S1 in supplementary online material. The map positions of ∼1500 genes were available in all four species and the reconstruction is based on this data set. The genes and their
Comparison of the vertebrate protokaryotype with the teleost and tetrapod karyotypes
In most cases the teleost protochromosomes were shown to represent ancestral vertebrate protochromosomes (Figure 2, Figure 4). However, some fissions and fusions must have occurred. The largest chromosome, TEL 1, is composed of genes from TNI 2 and 3 and is the fusion product of the protochromosomes VER 4 and 11 (Figure 2). In zebrafish, chicken and human the genes of these two protochromosomes are separated on different sets of chromosomes (Table S3d,k in supplementary online material). In the
Concluding remarks
There are several initiatives underway to use the genome data from mammalian and vertebrate species to reconstruct by in silico analysis an ancestral founder genome 10, 11, 15, 16, 17. An approach similar to that proposed here was taken by Jaillon et al. [10]. Data from 6684 genes with proven orthology in pufferfish and human were combined to reconstruct a protokaryotype with 12 chromosome pairs. Similar to the procedure used here, the genes were assembled in synteny segments, and only 110
References (32)
Wide genome comparisons reveal the origins of the human X chromosome
Trends Genet.
(2004)Visualization of the conservation of synteny between humans and pigs by heterologous chromosomal painting
Genomics
(1995)The evolution of eutherian chromosomes
Curr. Opin. Genet. Dev.
(2004)- et al.
Vertebrate genomes compared
Science
(2002) Emerging patterns of comparative genome organization in some mammalian species as revealed by Zoo-FISH
Genome Res.
(1998)- Murphy, W.J. et al. (2001) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome...
Reciprocal chromosome painting among human, aardvark and elephant (superorder Afrotheria) reveals the likely eutherian ancestral karyotype
Proc. Natl. Acad. Sci. U. S. A.
(2003)Reconstruction of the ancestral karyotype of eutherian mammals
Chromosome Res.
(2003)Origins of primate chromosomes as delineated by Zoo-FISH and alignments of human and mouse draft sequences
Cytogenet. Genome Res.
(2005)Zebrafish hox clusters and vertebrate genome evolution
Science
(1998)
A comparative map of the zebrafish genome
Genome Res.
A medaka gene map: The trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping
Genome Res.
Genome duplication in the teleost fish Tetraodon nigrovirides reveals the early vertebrate proto-karyotype
Nature
The zebrafish gene map defines ancestral vertebrate chromosomes
Genome Res.
Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution
Nature
Major events in the genome evolution of vertebrates: Paranome age and size differ considerably between ray-finned fishes and land vertebrates
Proc. Natl. Acad. Sci. U. S. A.
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These authors contributed equally to this article.