Molecular Biology and Evolution, Vol 16, 793-805, Copyright © 1999 by Society for Molecular Biology and Evolution
HS Malik, WD Burke and TH Eickbush
A comprehensive phylogenetic analysis was conducted of non-long-
terminal-repeat (non-LTR) retrotransposons based on an extended sequence
alignment of their reverse transcriptase (RT) domain. The 440 amino acid
positions used included a region proposed to be similar to the "thumb" of
the right-handed RT structure found in retroviruses. All identified non-LTR
elements could be grouped into 11 distinct clades. Using the rates of
sequence change derived from studies of the vertical inheritance of R1 and
R2 elements in arthropods as a comparison, we found no evidence for the
horizontal transmission of non-LTR elements. Assuming vertical descent, the
phylogeny suggested that non-LTR elements are as old as eukaryotes, with
each of the 11 clades dating back to the Precambrian era. The analysis
enabled us to propose a simple chronology for the acquisition of different
enzymatic domains in the evolution of the non-LTR class of
retrotransposons. The first non- LTR elements were sequence specific by
virtue of a restriction-enzyme- like endonuclease located downstream of the
RT domain. Evolving from this original group were elements (eight clades)
that acquired an apurinic-apyrimidic endonuclease-like domain upstream of
the RT domain. Finally, four of these clades have inherited an RNase H
domain downstream of the RT domain. The phylogenies of the AP endonuclease
and RNase H domains were also determined for this report and are consistent
with the monophyletic acquisition of these domains. These studies represent
the most comprehensive effort to date to trace the evolution of a major
class of transposable elements.
ORIGINAL ARTICLE
The age and evolution of non-LTR retrotransposable elements
Department of Biology, University of Rochester, New York 14627, USA.
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
D. G. Eickbush, J. Ye, X. Zhang, W. D. Burke, and T. H. Eickbush Epigenetic Regulation of Retrotransposons within the Nucleolus of Drosophila Mol. Cell. Biol., October 15, 2008; 28(20): 6452 - 6461. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Ichiyanagi and N. Okada Mobility Pathways for Vertebrate L1, L2, CR1, and RTE Clade Retrotransposons Mol. Biol. Evol., June 1, 2008; 25(6): 1148 - 1157. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Zhang, J. Zhou, and T. H. Eickbush Rapid R2 Retrotransposition Leads to the Loss of Previously Inserted Copies via Large Deletions of the rDNA Locus Mol. Biol. Evol., January 1, 2008; 25(1): 229 - 237. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Chung, O. Siol, T. Dingermann, and T. Winckler Protein Interactions Involved in tRNA Gene-Specific Integration of Dictyostelium discoideum Non-Long Terminal Repeat Retrotransposon TRE5-A Mol. Cell. Biol., December 15, 2007; 27(24): 8492 - 8501. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Villasante, J. P. Abad, R. Planello, M. Mendez-Lago, S. E. Celniker, and B. de Pablos Drosophila telomeric retrotransposons derived from an ancestral element that was recruited to replace telomerase Genome Res., December 1, 2007; 17(12): 1909 - 1918. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. E. Stage and T. H. Eickbush Sequence variation within the rRNA gene loci of 12 Drosophila species Genome Res., December 1, 2007; 17(12): 1888 - 1897. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Ichiyanagi, H. Nishihara, D. D. Duvernell, and N. Okada Acquisition of Endonuclease Specificity during Evolution of L1 Retrotransposon Mol. Biol. Evol., September 1, 2007; 24(9): 2009 - 2015. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Matveev, H. Nishihara, and N. Okada Novel SINE Families from Salmons Validate Parahucho (Salmonidae) as a Distinct Genus and Give Evidence that SINEs Can Incorporate LINE-related 3'-Tails of Other SINEs Mol. Biol. Evol., August 1, 2007; 24(8): 1656 - 1666. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. Piskurek and N. Okada Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals PNAS, July 17, 2007; 104(29): 12046 - 12051. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Casacuberta, F. A. Marin, and M.-L. Pardue Intracellular targeting of telomeric retrotransposon Gag proteins of distantly related Drosophila species PNAS, May 15, 2007; 104(20): 8391 - 8396. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. H. Eickbush and D. G. Eickbush Finely Orchestrated Movements: Evolution of the Ribosomal RNA Genes Genetics, February 1, 2007; 175(2): 477 - 485. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Ichiyanagi, R. Nakajima, M. Kajikawa, and N. Okada Novel retrotransposon analysis reveals multiple mobility pathways dictated by hosts Genome Res., January 1, 2007; 17(1): 33 - 41. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Ye and T. H. Eickbush Chromatin Structure and Transcription of the R1- and R2-Inserted rRNA Genes of Drosophila melanogaster Mol. Cell. Biol., December 1, 2006; 26(23): 8781 - 8790. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. H. Maxwell, J. M. Belote, and R. W. Levis Identification of multiple transcription initiation, polyadenylation, and splice sites in the Drosophila melanogaster TART family of telomeric retrotransposons Nucleic Acids Res., November 14, 2006; 34(19): 5498 - 5507. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. S. Dolgin and B. Charlesworth The Fate of Transposable Elements in Asexual Populations Genetics, October 1, 2006; 174(2): 817 - 827. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Kojima, K.-i. Kuma, H. Toh, and H. Fujiwara Identification of rDNA-Specific Non-LTR Retrotransposons in Cnidaria Mol. Biol. Evol., October 1, 2006; 23(10): 1984 - 1993. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Matsumoto, M. Hamada, M. Osanai, and H. Fujiwara Essential Domains for Ribonucleoprotein Complex Formation Required for Retrotransposition of Telomere-Specific Non-Long Terminal Repeat Retrotransposon SART1. Mol. Cell. Biol., July 1, 2006; 26(13): 5168 - 5179. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. d. C. Seleme, M. R. Vetter, R. Cordaux, L. Bastone, M. A. Batzer, and H. H. Kazazian Jr. Extensive individual variation in L1 retrotransposition capability contributes to human genetic diversity PNAS, April 25, 2006; 103(17): 6611 - 6616. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Lucchinetti, J. Feng, R. d. Silva, G. V. Tolstonog, M. C. Schaub, G. G. Schumann, and M. Zaugg Inhibition of LINE-1 expression in the heart decreases ischemic damage by activation of Akt/PKB signaling Physiol Genomics, April 13, 2006; 25(2): 314 - 324. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. T. Averbeck and T. H. Eickbush Monitoring the Mode and Tempo of Concerted Evolution in the Drosophila melanogaster rDNA Locus Genetics, December 1, 2005; 171(4): 1837 - 1846. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. M. Christensen, A. Bibillo, and T. H. Eickbush Role of the Bombyx mori R2 element N-terminal domain in the target-primed reverse transcription (TPRT) reaction Nucleic Acids Res., November 10, 2005; 33(20): 6461 - 6468. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. R. Heras, M. C. Lopez, J. L. Garcia-Perez, S. L. Martin, and M. C. Thomas The L1Tc C-Terminal Domain from Trypanosoma cruzi Non-Long Terminal Repeat Retrotransposon Codes for a Protein That Bears Two C2H2 Zinc Finger Motifs and Is Endowed with Nucleic Acid Chaperone Activity Mol. Cell. Biol., November 1, 2005; 25(21): 9209 - 9220. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Kojima and H. Fujiwara Long-Term Inheritance of the 28S rDNA-Specific Retrotransposon R2 Mol. Biol. Evol., November 1, 2005; 22(11): 2157 - 2165. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. L. Crainey, C. F. Garvey, and C. A. Malcolm The Origin and Evolution of Mosquito APE Retroposons Mol. Biol. Evol., November 1, 2005; 22(11): 2190 - 2197. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Kojima, T. Matsumoto, and H. Fujiwara Eukaryotic Translational Coupling in UAAUG Stop-Start Codons for the Bicistronic RNA Translation of the Non-Long Terminal Repeat Retrotransposon SART1 Mol. Cell. Biol., September 1, 2005; 25(17): 7675 - 7686. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. M. Christensen and T. H. Eickbush R2 Target-Primed Reverse Transcription: Ordered Cleavage and Polymerization Steps by Protein Subunits Asymmetrically Bound to the Target DNA Mol. Cell. Biol., August 1, 2005; 25(15): 6617 - 6628. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Kojima and H. Fujiwara An extraordinary retrotransposon family encoding dual endonucleases Genome Res., August 1, 2005; 15(8): 1106 - 1117. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Zingler, U. Willhoeft, H.-P. Brose, V. Schoder, T. Jahns, K.-M. O. Hanschmann, T. A. Morrish, J. Lower, and G. G. Schumann Analysis of 5' junctions of human LINE-1 and Alu retrotransposons suggests an alternative model for 5'-end attachment requiring microhomology-mediated end-joining Genome Res., June 1, 2005; 15(6): 780 - 789. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Anzai, M. Osanai, M. Hamada, and H. Fujiwara Functional roles of 3'-terminal structures of template RNA during in vivo retrotransposition of non-LTR retrotransposon, R1Bm Nucleic Acids Res., April 6, 2005; 33(6): 1993 - 2002. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Kajikawa, K. Ichiyanagi, N. Tanaka, and N. Okada Isolation and Characterization of Active LINE and SINEs from the Eel Mol. Biol. Evol., March 1, 2005; 22(3): 673 - 682. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. d. C. Seleme, O. Disson, S.ép. Robin, C. Brun, D. Teninges, and A. Bucheton In vivo RNA localization of I factor, a non-LTR retrotransposon, requires a cis-acting signal in ORF2 and ORF1 protein Nucleic Acids Res., February 1, 2005; 33(2): 776 - 785. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. J.H. BLOCKER, G. MOHR, L. H. CONLAN, L. QI, M. BELFORT, and A. M. LAMBOWITZ Domain structure and three-dimensional model of a group II intron-encoded reverse transcriptase RNA, January 1, 2005; 11(1): 14 - 28. [Abstract] [Full Text] [PDF] |
||||
![]() |
J.-N. Volff, H. Lehrach, R. Reinhardt, and D. Chourrout Retroelement Dynamics and a Novel Type of Chordate Retrovirus-like Element in the Miniature Genome of the Tunicate Oikopleura dioica Mol. Biol. Evol., November 1, 2004; 21(11): 2022 - 2033. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Maita, T. Anzai, H. Aoyagi, H. Mizuno, and H. Fujiwara Crystal Structure of the Endonuclease Domain Encoded by the Telomere-specific Long Interspersed Nuclear Element, TRAS1 J. Biol. Chem., September 24, 2004; 279(39): 41067 - 41076. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Osanai, H. Takahashi, K. K. Kojima, M. Hamada, and H. Fujiwara Essential Motifs in the 3' Untranslated Region Required for Retrotransposition and the Precise Start of Reverse Transcription in Non-Long-Terminal-Repeat Retrotransposon SART1 Mol. Cell. Biol., September 15, 2004; 24(18): 7902 - 7913. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. H. Penton and T. J. Crease Evolution of the Transposable Element Pokey in the Ribosomal DNA of Species in the Subgenus Daphnia (Crustacea: Cladocera) Mol. Biol. Evol., September 1, 2004; 21(9): 1727 - 1739. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Ergun, C. Buschmann, J. Heukeshoven, K. Dammann, F. Schnieders, H. Lauke, F. Chalajour, N. Kilic, W. H. Stratling, and G. G. Schumann Cell Type-specific Expression of LINE-1 Open Reading Frames 1 and 2 in Fetal and Adult Human Tissues J. Biol. Chem., June 25, 2004; 279(26): 27753 - 27763. [Abstract] [Full Text] [PDF] |
||||
![]() |
Macroevolution, hierarchy theory, and the C-value enigma Paleobiology, June 1, 2004; 30(2): 179 - 202. |
||||
![]() |
A. M. RUSCHAK, D. H. MATHEWS, A. BIBILLO, S. L. SPINELLI, J. L. CHILDS, T. H. EICKBUSH, and D. H. TURNER Secondary structure models of the 3' untranslated regions of diverse R2 RNAs RNA, June 1, 2004; 10(6): 978 - 987. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. J. D. Goodwin and R. T. M. Poulter A New Group of Tyrosine Recombinase-Encoding Retrotransposons Mol. Biol. Evol., April 1, 2004; 21(4): 746 - 759. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. DeMarco, A. T. Kowaltowski, A. A. Machado, M. B. Soares, C. Gargioni, T. Kawano, V. Rodrigues, A. M. B. N. Madeira, R. A. Wilson, C. F. M. Menck, et al. Saci-1, -2, and -3 and Perere, Four Novel Retrotransposons with High Transcriptional Activities from the Human Parasite Schistosoma mansoni J. Virol., March 15, 2004; 78(6): 2967 - 2978. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. H. Kazazian Jr. Mobile Elements: Drivers of Genome Evolution Science, March 12, 2004; 303(5664): 1626 - 1632. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Bringaud, N. Biteau, E. Zuiderwijk, M. Berriman, N. M. El-Sayed, E. Ghedin, S. E. Melville, N. Hall, and T. Baltz The ingi and RIME non-LTR Retrotransposons Are Not Randomly Distributed in the Genome of Trypanosoma brucei Mol. Biol. Evol., March 1, 2004; 21(3): 520 - 528. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. S. Fillingham, T. A. Thing, N. Vythilingum, A. Keuroghlian, D. Bruno, G. B. Golding, and R. E. Pearlman A Non-Long Terminal Repeat Retrotransposon Family Is Restricted to the Germ Line Micronucleus of the Ciliated Protozoan Tetrahymena thermophila Eukaryot. Cell, February 1, 2004; 3(1): 157 - 169. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. K. Mandal, A. Bagchi, A. Bhattacharya, and S. Bhattacharya An Entamoeba histolytica LINE/SINE Pair Inserts at Common Target Sites Cleaved by the Restriction Enzyme-Like LINE-Encoded Endonuclease Eukaryot. Cell, February 1, 2004; 3(1): 170 - 179. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Kojima and H. Fujiwara Cross-Genome Screening of Novel Sequence-Specific Non-LTR Retrotransposons: Various Multicopy RNA Genes and Microsatellites Are Selected as Targets Mol. Biol. Evol., February 1, 2004; 21(2): 207 - 217. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Matsumoto, H. Takahashi, and H. Fujiwara Targeted Nuclear Import of Open Reading Frame 1 Protein Is Required for In Vivo Retrotransposition of a Telomere-Specific Non-Long Terminal Repeat Retrotransposon, SART1 Mol. Cell. Biol., January 1, 2004; 24(1): 105 - 122. [Abstract] [Full Text] [PDF] |
||||
![]() |
H.-R. Huang, M. Y. Chao, B. Armstrong, Y. Wang, A. M. Lambowitz, and P. S. Perlman The DIVa Maturase Binding Site in the Yeast Group II Intron aI2 Is Essential for Intron Homing but Not for In Vivo Splicing Mol. Cell. Biol., December 1, 2003; 23(23): 8809 - 8819. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Martin, D. Branciforte, D. Keller, and D. L. Bain Trimeric structure for an essential protein in L1 retrotransposition PNAS, November 25, 2003; 100(24): 13815 - 13820. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Biedler and Z. Tu Non-LTR Retrotransposons in the African Malaria Mosquito, Anopheles gambiae: Unprecedented Diversity and Evidence of Recent Activity Mol. Biol. Evol., November 1, 2003; 20(11): 1811 - 1825. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. E. Perez-Gonzalez, W. D. Burke, and T. H. Eickbush R1 and R2 Retrotransposition and Deletion in the rDNA Loci on the X and Y Chromosomes of Drosophila melanogaster Genetics, October 1, 2003; 165(2): 675 - 685. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Wickstead, K. Ersfeld, and K. Gull Repetitive Elements in Genomes of Parasitic Protozoa Microbiol. Mol. Biol. Rev., September 1, 2003; 67(3): 360 - 375. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. D. Boeke The Unusual Phylogenetic Distribution of Retrotransposons: A Hypothesis Genome Res., September 1, 2003; 13(9): 1975 - 1983. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. D. Burke, D. Singh, and T. H. Eickbush R5 Retrotransposons Insert into a Family of Infrequently Transcribed 28S rRNA Genes of Planaria Mol. Biol. Evol., August 1, 2003; 20(8): 1260 - 1270. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Bouneau, C. Fischer, C. Ozouf-Costaz, A. Froschauer, O. Jaillon, J.-P. Coutanceau, C. Korting, J. Weissenbach, A. Bernot, and J.-N. Volff An Active Non-LTR Retrotransposon With Tandem Structure in the Compact Genome of the Pufferfish Tetraodon nigroviridis Genome Res., July 1, 2003; 13(7): 1686 - 1695. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. S. Copeland, P. J. Brindley, O. Heyers, S. F. Michael, D. A. Johnston, D. L. Williams, A. C. Ivens, and B. H. Kalinna Boudicca, a Retrovirus-Like Long Terminal Repeat Retrotransposon from the Genome of the Human Blood Fluke Schistosoma mansoni J. Virol., June 1, 2003; 77(11): 6153 - 6166. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Rashkova, A. Athanasiadis, and M.-L. Pardue Intracellular Targeting of Gag Proteins of the Drosophila Telomeric Retrotransposons J. Virol., June 1, 2003; 77(11): 6376 - 6384. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. A. Petrov, Y. T. Aminetzach, J. C. Davis, D. Bensasson, and A. E. Hirsh Size Matters: Non-LTR Retrotransposable Elements and Ectopic Recombination in Drosophila Mol. Biol. Evol., June 1, 2003; 20(6): 880 - 892. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Casacuberta and M.-L. Pardue Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group PNAS, March 18, 2003; 100(6): 3363 - 3368. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Kojima and H. Fujiwara Evolution of Target Specificity in R1 Clade Non-LTR Retrotransposons Mol. Biol. Evol., March 1, 2003; 20(3): 351 - 361. [Abstract] [Full Text] |













