Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals - PubMed (original) (raw)

Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals

Claudio Casola et al. Mol Biol Evol. 2008 Jan.

Abstract

The mammalian centromere-associated protein B (CENP-B) shares significant sequence similarity with 3 proteins in fission yeast (Abp1, Cbh1, and Cbh2) that also bind centromeres and have essential function for chromosome segregation and centromeric heterochromatin formation. Each of these proteins displays extensive sequence similarity with pogo-like transposases, which have been previously identified in the genomes of various insects and vertebrates, in the protozoan Entamoeba and in plants. Based on this distribution, it has been proposed that the mammalian and fission yeast centromeric proteins are derived from "domesticated" pogo-like transposons. Here we took advantage of the vast amount of sequence information that has become recently available for a wide range of fungal and animal species to investigate the origin of the mammalian CENP-B and yeast CENP-B-like genes. A highly conserved ortholog of CENP-B was detected in 31 species of mammals, including opossum and platypus, but was absent from all nonmammalian species represented in the databases. Similarly, no ortholog of the fission yeast centromeric proteins was identified in any of the various fungal genomes currently available. In contrast, we discovered a plethora of novel pogo-like transposons in diverse invertebrates and vertebrates and in several filamentous fungi. Phylogenetic analysis revealed that the mammalian and fission yeast CENP-B proteins fall into 2 distinct monophyletic clades, each of which includes a different set of pogo-like transposons. These results are most parsimoniously explained by independent domestication events of pogo-like transposases into centromeric proteins in the mammalian and fission yeast lineages, a case of "convergent domestication." These findings highlight the propensity of transposases to give rise to new host proteins and the potential of transposons as sources of genetic innovation.

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Figures

Figure 1

Figure 1

Distribution of CENP-B and related _pogo_-derived genes. Solid figures indicate apparent extant genes, as evidenced by the presence of uninterrupted ORFs and dN/dS <0.5 and significantly <1. Unshaded figures indicate putative genes exhibiting dN/dS <0.5 and significantly <1, which contain one or more apparent frameshift and/or nonsense mutations. The Greek letter ψ indicates probable pseudogenes, which, in addition to harboring apparent frameshift and nonsense mutations, exhibit dN/dS >0.5 and not significantly <1. Assembled, high coverage genomes (NHGRI, NIH,

http://www.genome.gov/10002154

) are in bold print. A dash indicates the absence of a detected ortholog in an assembled, high coverage genome.

Figure 2

Figure 2

Phylogenetic tree of _pogo_-like transposases and _pogo_-derived genes. Protein sequences were aligned using the MAFFT package and the alignment refined manually with Bioedit to produce a final multialignment of about 310 residues. The tree shown here was inferred using the Bayesian algorithms implemented in MrBayes as described in Methods. Numbers in the nodes show posterior probabilities. _pogo_-derived genes and _pogo_-like transposons are highlighted in red and blue, respectively. Detailed information about each sequence are reported in table 1 and table 2. CR: CENP-B-related clade; AR:Abp1-related clade; JR: JERKY-related clade: TC2: TC2-related clade. Fot1, Cirt1 and Tan1 belong to the Fot1 clade.

Figure 3

Figure 3

Terminal inverted repeats of _pogo_-like transposons. Multialignments of TIR sequences of transposons belonging to the three clades of pogo-like elements identified in this study: CENP-B-related (CR), Abp1-related (AR) and JERKY-related (JR). Nucleotides conserved in at least 50% of sequences are shaded.

Figure 4

Figure 4

Convergent domestication of pogo-like transposases in fission yeast and mammals. A star indicates the presence of _pogo_-derived centromere-binding protein. A circle indicates the presence of _pogo_-like transposons. Under an orthology model, arrowheads indicate inferred gene loss events following a single domestication event indicated by the arrow. Representative taxa for which whole-genome sequencing is complete are shown. The cladogram has been inferred using the Tree of Life Web Project (Maddison and Schulz 1996–2006) and the fungi phylogeny described in James et al. (2006).

References

    1. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 2005;21:2104–2105. - PubMed
    1. Amor DJ, Kalitsis P, Sumer H, Choo KH. Building the centromere: from foundation proteins to 3D organization. Trends Cell Biol. 2004;14:359–368. - PubMed
    1. Aravind L, Watanabe H, Lipman DJ, Koonin EV. Lineage-specific loss and divergence of functionally linked genes in eukaryotes. Proc Natl Acad Sci U S A. 2000;97:11319–11324. - PMC - PubMed
    1. Baum M, Clarke L. Fission yeast homologs of human CENP-B have redundant functions affecting cell growth and chromosome segregation. Mol Cell Biol. 2000;20:2852–2864. - PMC - PubMed
    1. Bejarano LA, Valdivia MM. Molecular cloning of an intronless gene for the hamster centromere antigen CENP-B. Biochim Biophys Acta. 1996;1307:21–25. - PubMed

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