Dataset Information

Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins.

ABSTRACT: The centromere is a chromatin region that is required for accurate inheritance of eukaryotic chromosomes during cell divisions. Among the different centromere-associated proteins (CENP) identified, CENP-B has been independently domesticated from a pogo-like transposase twice: Once in mammals and once in fission yeast. Recently, a third independent domestication restricted to holocentric lepidoptera has been described. In this work, we take advantage of the high-quality genome sequence and the wealth of functional information available for Drosophila melanogaster to further investigate the possibility of additional independent domestications of pogo-like transposases into host CENP-B related proteins. Our results showed that CENP-B related genes are not restricted to holocentric insects. Furthermore, we showed that at least three independent domestications of pogo-like transposases have occurred in metazoans. Our results highlight the importance of transposable elements as raw material for the recurrent evolution of important cellular functions.

SUBMITTER: Mateo L

PROVIDER: S-EPMC4231638 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins.

Mateo Lidia L González Josefa J

Genome biology and evolution 20140724 8

The centromere is a chromatin region that is required for accurate inheritance of eukaryotic chromosomes during cell divisions. Among the different centromere-associated proteins (CENP) identified, CENP-B has been independently domesticated from a pogo-like transposase twice: Once in mammals and once in fission yeast. Recently, a third independent domestication restricted to holocentric lepidoptera has been described. In this work, we take advantage of the high-quality genome sequence and the we ...[more]

PMID: 25062917

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Project description:Proteins encoded by transposable elements (TEs) play a vital role in their proliferation in host genomes. In recent years, an increasing number of studies have shown that TE proteins have contributed to the emergence of novel host proteins. In Drosophila, there are several proteins derived from the PIF/Harbinger transposase superfamily called Drosophila PIF Like Genes (DPLGs). Here, we investigated the function of four DPLGs (DPLG1-4) in D. melanogaster that are highly conserved and present across Drosophila but are deeply diverged from each other, and likely originated through independent domestication of the transposase from distinct PIF-like TE families. We have analyzed transcript localization of DPLG 1-4, tagged DPLG3 and DPLG4 and studied their protein localization and, produced null alleles for DPLG1 and DPLG4. RNA in situ hybridization reveals that DPLG1-4 have strikingly similar pattern of transcript localization in the gonads, and in the nervous system during embryogenesis, suggesting their domestication for related functions. DPLGs show co-expression enrichment with transcription factors in ovaries and during embryogenesis supporting that they may be domesticated as regulatory proteins in flies. DPLG3 and DPLG4 tagged proteins localize with DNA in the nucleus of the ovaries consistent with this hypothesis. Loss of DPLG1 or DPLG4 results in viability and/or fertility effects, while loss of both DPLG1 and DPLG4 resulted in no effect in viability or fertility suggesting genetic interaction between these two genes. Further, loss of DPLG4 showed increased survival in flies, and increased fertility in older females indicating its involvement in the process of ageing. Transcriptional analyses in the ovaries showed that the loss of either DPLG1 or DPLG4 protein leads to modest changes in transcription of a large and significantly overlapping set of genes, and also affects transposable elements activity. The observed functional overlap of independently domesticated transposases from the same TE family and genetic interaction between them suggests a stepping stone model in which domestication of a PIF/Harbinger transposase might promote the domestication of related transposases for gonad and nervous system regulatory functions.

Dataset Information

Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins.

Publications

Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins.

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