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BACKGROUND: DNA transposons are generally destroyed by mutations and have short lifespans in hosts, as they are neutral or harmful to the host and therefore not conserved by natural selection. The clawed frog Xenopus harbors many DNA transposons and certain families, such as T2-MITE, have extremely long lives. These have ancient origins, but have shown recent transposition activity. In addition, certain transposase genes may have been "domesticated" by Xenopus and conserved over long time periods by natural selection. The aim of this study was to elucidate the evolutionary interactions between the host and the long-lived DNA transposon family it contains. Here, we investigated the molecular evolution of the Kolobok DNA transposon superfamily. Kolobok is thought to contribute to T2-MITE transposition.
RESULTS: In the diploid western clawed frog Xenopus tropicalis and the allotetraploid African clawed frog Xenopus laevis, we searched for transposase genes homologous to those in the Kolobok superfamily. To determine the amplification and domestication of these genes, we used molecular phylogenetics and analyses of copy numbers, conserved motifs, orthologous gene synteny, and coding sequence divergence between the orthologs of X. laevis and X. tropicalis, or between those of two distant X. tropicalis lineages. Among 38 X. tropicalis and 24 X. laevis prospective transposase genes, 10 or more in X. tropicalis and 14 or more in X. laevis were apparently domesticated. These genes may have undergone multiple independent domestications from before the divergence of X. laevis and X. tropicalis. In contrast, certain other transposases may have retained catalytic activity required for transposition and could therefore have been recently amplified.
CONCLUSION: Multiple domestication of certain transposases and prolonged conservation of the catalytic activity in others suggest that Kolobok superfamily transposons were involved in complex, mutually beneficial relationships with their Xenopus hosts. Some transposases may serve to activate long-lived T2-MITE subfamilies.
Fig. 1. Conserved regions of prospective XKol transposase CDSs. Conserved regions in a multiple alignment of prospective transposases predicted from the putative CDSs of XKol-Tpase genes with three outgroup transposases (Danio rerio Kolobok-1_DR, Capitella teleta Kolobok-1_CTe, and Branchiostoma floridae Kolobok-2_BF). Numbers above the alignment indicate the position of the amino acids in it (Additional file 1: Figure S1). Numbers in square brackets are the abbreviated amino acids. Consensus residues of conserved domains (DDE, THAP, and H2CH) are shown below the alignment. Nonconserved amino acid residues in conserved motifs are marked by gray shading
Fig. 2. Molecular phylogeny of prospective XKol transposases. Molecular phylogenetic trees of XKol-Tpase amino acid sequences inferred using the neighbor-joining method. Each operational taxonomic unit is represented by the names of the CDS and a chromosome or scaffold on which the CDS is located. The number of blastn hits to truncated transposase sequences are shown as numerals following the vertical bar. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are shown next to the branches. The symbol “+” on the branches indicates domestication events. Asterisks indicate transpositional amplification events. Subfamilies of putative domesticated transposase orthologs are grouped by black bars and named D1–D9. CDS subfamilies that may have been duplicated by recent transposition and amplification are grouped by gray bars and designated A1–A6
Fig. 3. Dot plot analysis of XKol-Tpase gene CDSs. All-to-all comparisons of XKol-Tpase CDSs (upper right) and proteins (lower left) performed by dot plot analyses. D1–D9 and A1–A6 are grouped in the same way as in Fig. 2
Fig. 4. Synteny of XKol-Tpase genes. Conserved synteny around putative domesticated orthologs of subfamily D1–D7. Xenopus laevis homeologous chromosomes L and S and Xenopus tropicalis homologous chromosome (T) are indicated by arrows. The orientation of each arrow indicates the 5′ to 3′ direction. XKol-Tpase CDSs are represented by white triangles on the chromosomes, and their names are shown below the chromosomes. Gray triangles indicate truncated XKol-Tpase sequences. Gene models around the CDSs are represented by black bars
Altschul,
Basic local alignment search tool.
1990, Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Alzohairy,
Transposable elements domesticated and neofunctionalized by eukaryotic genomes.
2013,
Pubmed
Avramova,
Matrix attachment regions and structural colinearity in the genomes of two grass species.
1998,
Pubmed
Bao,
Repbase Update, a database of repetitive elements in eukaryotic genomes.
2015,
Pubmed
Brookfield,
The ecology of the genome - mobile DNA elements and their hosts.
2005,
Pubmed
Chuong,
Regulatory activities of transposable elements: from conflicts to benefits.
2017,
Pubmed
Edgar,
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
2004,
Pubmed
El Amrani,
Genome-wide distribution and potential regulatory functions of AtATE, a novel family of miniature inverted-repeat transposable elements in Arabidopsis thaliana.
2002,
Pubmed
Finnegan,
Eukaryotic transposable elements and genome evolution.
1989,
Pubmed
Hellsten,
The genome of the Western clawed frog Xenopus tropicalis.
2010,
Pubmed
,
Xenbase
Hikosaka,
Evolution of the Xenopus piggyBac transposon family TxpB: domesticated and untamed strategies of transposon subfamilies.
2007,
Pubmed
,
Xenbase
Hikosaka,
Extensive amplification and transposition of a novel repetitive element, xstir, together with its terminal inverted repeat in the evolution of Xenopus.
2000,
Pubmed
,
Xenbase
Hikosaka,
Recent transposition activity of Xenopus T2 family miniature inverted-repeat transposable elements.
2011,
Pubmed
,
Xenbase
Hikosaka,
Distribution of the T2-MITE Family Transposons in the Xenopus (Silurana) tropicalis Genome.
2015,
Pubmed
,
Xenbase
Hikosaka,
A systematic search and classification of T2 family miniature inverted-repeat transposable elements (MITEs) in Xenopus tropicalis suggests the existence of recently active MITE subfamilies.
2010,
Pubmed
,
Xenbase
Hikosaka,
Lineage-specific tandem repeats riding on a transposable element of MITE in Xenopus evolution: a new mechanism for creating simple sequence repeats.
2004,
Pubmed
,
Xenbase
Izsvák,
Short inverted-repeat transposable elements in teleost fish and implications for a mechanism of their amplification.
1999,
Pubmed
,
Xenbase
Jangam,
Transposable Element Domestication As an Adaptation to Evolutionary Conflicts.
2017,
Pubmed
Jones,
The rapid generation of mutation data matrices from protein sequences.
1992,
Pubmed
Kashiwagi,
Xenopus tropicalis: an ideal experimental animal in amphibia.
2010,
Pubmed
,
Xenbase
Kumar,
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.
2016,
Pubmed
Lohe,
Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements.
1995,
Pubmed
Meng,
A systematic identification of Kolobok superfamily transposons in Trichomonas vaginalis and sequence analysis on related transposases.
2011,
Pubmed
Rice,
EMBOSS: the European Molecular Biology Open Software Suite.
2000,
Pubmed
Roussigne,
The THAP domain: a novel protein motif with similarity to the DNA-binding domain of P element transposase.
2003,
Pubmed
Saitou,
The neighbor-joining method: a new method for reconstructing phylogenetic trees.
1987,
Pubmed
Session,
Genome evolution in the allotetraploid frog Xenopus laevis.
2016,
Pubmed
,
Xenbase
Sinzelle,
Molecular domestication of transposable elements: from detrimental parasites to useful host genes.
2009,
Pubmed
Ugarkovic,
Functional elements residing within satellite DNAs.
2005,
Pubmed
Unsal,
A novel group of families of short interspersed repetitive elements (SINEs) in Xenopus: evidence of a specific target site for DNA-mediated transposition of inverted-repeat SINEs.
1995,
Pubmed
,
Xenbase
Volff,
Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes.
2006,
Pubmed
Wicker,
A unified classification system for eukaryotic transposable elements.
2007,
Pubmed
Yang,
PAML 4: phylogenetic analysis by maximum likelihood.
2007,
Pubmed
Yang,
Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.
2000,
Pubmed
