Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals.
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.
Casola
Claudio
C
Department of Biology, University of Texas, Arlington, USA.
Hucks
Donald
D
Feschotte
Cédric
C
D000818:Animals; D051936:Centromere Protein B / Q000235:genetics*; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics*; D030541:Databases, Genetic; D019143:Evolution, Molecular; D006801:Humans; D010802:Phylogeny; D012568:Schizosaccharomyces / Q000235:genetics*; D029702:Schizosaccharomyces pombe Proteins / Q000235:genetics*; D017422:Sequence Analysis, DNA; D013045:Species Specificity; D019895:Transposases / Q000235:genetics*
C427236:Cbh2 protein, S pombe; D051936:Centromere Protein B; D002868:Chromosomal Proteins, Non-Histone; D004268:DNA-Binding Proteins; D029702:Schizosaccharomyces pombe Proteins; C097691:cbp1 protein, S pombe; D019895:Transposases