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Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses.
Gene. 2007 Apr 01; 390(1-2):3-17.GENE

Abstract

We previously identified a group of atypical mobile elements designated Mavericks from the nematodes Caenorhabditis elegans and C. briggsae and the zebrafish Danio rerio. Here we present the results of comprehensive database searches of the genome sequences available, which reveal that Mavericks are widespread in invertebrates and non-mammalian vertebrates but show a patchy distribution in non-animal species, being present in the fungi Glomus intraradices and Phakopsora pachyrhizi and in several single-celled eukaryotes such as the ciliate Tetrahymena thermophila, the stramenopile Phytophthora infestans and the trichomonad Trichomonas vaginalis, but not detectable in plants. This distribution, together with comparative and phylogenetic analyses of Maverick-encoded proteins, is suggestive of an ancient origin of these elements in eukaryotes followed by lineage-specific losses and/or recurrent episodes of horizontal transmission. In addition, we report that Maverick elements have amplified recently to high copy numbers in T. vaginalis where they now occupy as much as 30% of the genome. Sequence analysis confirms that most Mavericks encode a retroviral-like integrase, but lack other open reading frames typically found in retroelements. Nevertheless, the length and conservation of the target site duplication created upon Maverick insertion (5- or 6-bp) is consistent with a role of the integrase-like protein in the integration of a double-stranded DNA transposition intermediate. Mavericks also display long terminal-inverted repeats but do not contain ORFs similar to proteins encoded by DNA transposons. Instead, Mavericks encode a conserved set of 5 to 9 genes (in addition to the integrase) that are predicted to encode proteins with homology to replication and packaging proteins of some bacteriophages and diverse eukaryotic double-stranded DNA viruses, including a DNA polymerase B homolog and putative capsid proteins. Based on these and other structural similarities, we speculate that Mavericks represent an evolutionary missing link between seemingly disparate invasive DNA elements that include bacteriophages, adenoviruses and eukaryotic linear plasmids.

Authors+Show Affiliations

The University of Texas at Arlington, The Department of Biology, Arlington, TX 76019, United States. pritham@uta.eduNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

17034960

Citation

Pritham, Ellen J., et al. "Mavericks, a Novel Class of Giant Transposable Elements Widespread in Eukaryotes and Related to DNA Viruses." Gene, vol. 390, no. 1-2, 2007, pp. 3-17.
Pritham EJ, Putliwala T, Feschotte C. Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene. 2007;390(1-2):3-17.
Pritham, E. J., Putliwala, T., & Feschotte, C. (2007). Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene, 390(1-2), 3-17.
Pritham EJ, Putliwala T, Feschotte C. Mavericks, a Novel Class of Giant Transposable Elements Widespread in Eukaryotes and Related to DNA Viruses. Gene. 2007 Apr 1;390(1-2):3-17. PubMed PMID: 17034960.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. AU - Pritham,Ellen J, AU - Putliwala,Tasneem, AU - Feschotte,Cédric, Y1 - 2006/08/23/ PY - 2006/07/14/received PY - 2006/08/02/accepted PY - 2006/10/13/pubmed PY - 2007/5/3/medline PY - 2006/10/13/entrez SP - 3 EP - 17 JF - Gene JO - Gene VL - 390 IS - 1-2 N2 - We previously identified a group of atypical mobile elements designated Mavericks from the nematodes Caenorhabditis elegans and C. briggsae and the zebrafish Danio rerio. Here we present the results of comprehensive database searches of the genome sequences available, which reveal that Mavericks are widespread in invertebrates and non-mammalian vertebrates but show a patchy distribution in non-animal species, being present in the fungi Glomus intraradices and Phakopsora pachyrhizi and in several single-celled eukaryotes such as the ciliate Tetrahymena thermophila, the stramenopile Phytophthora infestans and the trichomonad Trichomonas vaginalis, but not detectable in plants. This distribution, together with comparative and phylogenetic analyses of Maverick-encoded proteins, is suggestive of an ancient origin of these elements in eukaryotes followed by lineage-specific losses and/or recurrent episodes of horizontal transmission. In addition, we report that Maverick elements have amplified recently to high copy numbers in T. vaginalis where they now occupy as much as 30% of the genome. Sequence analysis confirms that most Mavericks encode a retroviral-like integrase, but lack other open reading frames typically found in retroelements. Nevertheless, the length and conservation of the target site duplication created upon Maverick insertion (5- or 6-bp) is consistent with a role of the integrase-like protein in the integration of a double-stranded DNA transposition intermediate. Mavericks also display long terminal-inverted repeats but do not contain ORFs similar to proteins encoded by DNA transposons. Instead, Mavericks encode a conserved set of 5 to 9 genes (in addition to the integrase) that are predicted to encode proteins with homology to replication and packaging proteins of some bacteriophages and diverse eukaryotic double-stranded DNA viruses, including a DNA polymerase B homolog and putative capsid proteins. Based on these and other structural similarities, we speculate that Mavericks represent an evolutionary missing link between seemingly disparate invasive DNA elements that include bacteriophages, adenoviruses and eukaryotic linear plasmids. SN - 0378-1119 UR - https://www.unboundmedicine.com/medline/citation/17034960/Mavericks_a_novel_class_of_giant_transposable_elements_widespread_in_eukaryotes_and_related_to_DNA_viruses_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0378-1119(06)00537-3 DB - PRIME DP - Unbound Medicine ER -