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PMID: 1698615 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Origin and evolution of retroelements based upon their reverse transcriptase sequences.

The EMBO journal ·Vol. 9 ·No. 10 ·1990-10-00 ·Pages 3353-62

Xiong Y, Eickbush TH

Abstract

To study the evolutionary relationship of reverse transcriptase (RT) containing genetic elements, a phylogenetic tree of 82 retroelements from animals, plants, protozoans and bacteria was constructed. The tree was based on seven amino acid domains totalling 178 residues identified in all RTs. We have also identified these seven domains in the RNA-directed RNA polymerases from various plus-strand RNA viruses. The sequence similarity of these RNA polymerases to RT suggests that these two enzymes evolved from a common ancestor, and thus RNA polymerase can be used as an outgroup to root the RT tree. A comparison of the genetic organization of the various RT containing elements and their position on the tree allows several inferences concerning the origin and evolution of these elements. The most probable ancestor of current retroelements was a retrotransposable element with both gag-like and pol-like genes. On one major branch of the tree, organelle and bacterial sequences (e.g. group II introns and bacterial msDNA) appear to have captured the RT sequences from retrotransposons which lack long terminal repeats (LTRs). On the other major branch, acquisition of LTRs gave rise to two distinct groups of LTR retrotransposons and three groups of viruses: retroviruses, hepadnaviruses and caulimoviruses.

MeSH Terms
Amino Acid Sequence Animals Biological Evolution DNA Transposable Elements DNA-Directed RNA Polymerases/genetics Humans Introns Molecular Sequence Data Phylogeny RNA-Directed DNA Polymerase/genetics Sequence Homology, Nucleic Acid
Chemicals
DNA Transposable Elements RNA-Directed DNA Polymerase DNA-Directed RNA Polymerases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Xiong Y
Department of Biology, University of Rochester, NY 14627.
Eickbush T H
References (71)
71 references, click to expand
  1. Genetic organization of gibbon ape leukemia virus.
    Virology. 1989 Nov;173(1):205-13 PMID: 2683360
  2. Sequence of a novel simian immunodeficiency virus from a wild-caught African mandrill.
    Nature. 1989 Oct 12;341(6242):539-41 PMID: 2797181
  3. Nucleotide sequence analysis of feline immunodeficiency virus: genome organization and relationship to other lentiviruses.
    Proc Natl Acad Sci U S A. 1989 Oct;86(20):8088-92 PMID: 2813380
  4. Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses.
    J Virol. 1988 Mar;62(3):722-31 PMID: 2828667
  5. Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses.
    Mol Cell Biol. 1988 Dec;8(12):5245-56 PMID: 2854194
  6. A copia-like transposable element family in Arabidopsis thaliana.
    Nature. 1988 Nov 17;336(6196):242-4 PMID: 2904123
  7. Complete nucleotide sequence of a molecular clone of woodchuck hepatitis virus that is infectious in the natural host.
    Proc Natl Acad Sci U S A. 1989 Mar;86(6):1846-9 PMID: 2928306
  8. L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein.
    Nature. 1986 Jun 5-11;321(6070):625-8 PMID: 2423883
  9. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information.
    Annu Rev Biochem. 1986;55:631-61 PMID: 2427017
  10. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs.
    Cell. 1986 Dec 26;47(6):1007-15 PMID: 2430722
  11. Sequence relationships of type D retroviruses which cause simian acquired immunodeficiency syndrome.
    Virology. 1987 Apr;157(2):317-29 PMID: 2435057
  12. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons.
    Mol Cell Biol. 1988 Jan;8(1):114-23 PMID: 2447482
  13. Primary structure and functional organization of Drosophila 1731 retrotransposon.
    Nucleic Acids Res. 1988 Jul 11;16(13):6113-25 PMID: 2456522
  14. A sequence motif in many polymerases.
    Nucleic Acids Res. 1988 Nov 11;16(21):9909-16 PMID: 2461550
  15. Two independent retrons with highly diverse reverse transcriptases in Myxococcus xanthus.
    Proc Natl Acad Sci U S A. 1990 Feb;87(3):942-5 PMID: 1689062
  16. A retrotransposable element from the mosquito Anopheles gambiae .
    Mol Cell Biol. 1990 Mar;10(3):863-71 PMID: 1689457
  17. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori.
    J Mol Biol. 1990 Mar 5;212(1):37-52 PMID: 1690812
  18. A rapidly rearranging retrotransposon within the miniexon gene locus of Crithidia fasciculata.
    Mol Cell Biol. 1990 Feb;10(2):615-24 PMID: 2153919
  19. The complete sequence of mag, a new retrotransposon in Bombyx mori.
    Nucleic Acids Res. 1990 Feb 11;18(3):674 PMID: 2155411
  20. SLACS retrotransposon from Trypanosoma brucei gambiense is similar to mammalian LINEs.
    Nucleic Acids Res. 1990 Feb 25;18(4):785-92 PMID: 2156231
  21. Nucleotide sequence and genome organization of biologically active proviruses of the bovine immunodeficiency-like virus.
    Virology. 1990 Apr;175(2):391-409 PMID: 2183467
  22. Close structural resemblance between putative polymerase of a Drosophila transposable genetic element 17.6 and pol gene product of Moloney murine leukaemia virus.
    EMBO J. 1985 May;4(5):1267-72 PMID: 2408886
  23. The origin and evolution of retroposons.
    Int Rev Cytol. 1985;93:187-279 PMID: 2409043
  24. Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins.
    Mol Cell Biol. 1985 Jul;5(7):1630-8 PMID: 2410772
  25. Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses.
    Nature. 1985 Aug 15-21;316(6029):641-3 PMID: 2412125
  26. Sequence of Dictyostelium DIRS-1: an apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence.
    Cell. 1985 Nov;43(1):105-15 PMID: 2416457
  27. Genes encoding a subunit of respiratory NADH dehydrogenase (ND1) and a reverse transcriptase-like protein (RTL) are linked to ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA.
    EMBO J. 1988 Nov;7(11):3501-8 PMID: 2463163
  28. The Drosophila mobile element jockey belongs to LINEs and contains coding sequences homologous to some retroviral proteins.
    Gene. 1988 Oct 30;70(2):253-62 PMID: 2463954
  29. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns.
    Mol Biol Evol. 1988 Nov;5(6):675-90 PMID: 2464735
  30. Reverse transcriptase associated with the biosynthesis of the branched RNA-linked msDNA in Myxococcus xanthus.
    Cell. 1989 Feb 24;56(4):709-17 PMID: 2465092
  31. Reverse transcriptase in a clinical strain of Escherichia coli: production of branched RNA-linked msDNA.
    Science. 1989 Feb 24;243(4894 Pt 1):1033-8 PMID: 2466332
  32. Transposable elements in eukaryotes.
    Int Rev Cytol. 1985;93:281-326 PMID: 2989205
  33. Nucleotide sequence of human endogenous retrovirus genome related to the mouse mammary tumor virus genome.
    J Virol. 1986 Nov;60(2):589-98 PMID: 3021993
  34. The sequence of a large L1Md element reveals a tandemly repeated 5' end and several features found in retrotransposons.
    Mol Cell Biol. 1986 Jan;6(1):168-82 PMID: 3023821
  35. Nucleotide sequence of a complete mouse intracisternal A-particle genome: relationship to known aspects of particle assembly and function.
    J Virol. 1987 Oct;61(10):3020-9 PMID: 3041022
  36. Progressive sequence alignment as a prerequisite to correct phylogenetic trees.
    J Mol Evol. 1987;25(4):351-60 PMID: 3118049
  37. On the early evolution of RNA polymerase.
    J Mol Evol. 1988;27(4):365-76 PMID: 3146647
  38. Alteration of T-state binding properties of naturally glycated hemoglobin, HbA1c.
    J Mol Biol. 1988 Sep 5;203(1):233-9 PMID: 3184188
  39. Molecular cloning, complete nucleotide sequence, and gene structure of the provirus genome of a retrovirus produced in a human lymphoblastoid cell line.
    Virology. 1988 Dec;167(2):468-76 PMID: 3201749
  40. Sequence of simian immunodeficiency virus from African green monkey, a new member of the HIV/SIV group.
    Nature. 1988 Jun 2;333(6172):457-61 PMID: 3374586
  41. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  42. Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses.
    Nature. 1987 Aug 6-12;328(6130):543-7 PMID: 3649576
  43. The complete nucleotide sequence of tobacco rattle virus RNA-1.
    J Gen Virol. 1987 Oct;68 ( Pt 10):2563-75 PMID: 3668507
  44. Sequence of figwort mosaic virus DNA (caulimovirus group).
    Nucleic Acids Res. 1987 Oct 26;15(20):8451-66 PMID: 3671088
  45. Structure and genomic organization of a new family of murine retrovirus-related DNA sequences (MuRRS).
    Nucleic Acids Res. 1985 May 24;13(10):3461-70 PMID: 4011431
  46. RNA-dependent DNA polymerase in virions of RNA tumour viruses.
    Nature. 1970 Jun 27;226(5252):1209-11 PMID: 4316300
  47. RNA-dependent DNA polymerase in virions of Rous sarcoma virus.
    Nature. 1970 Jun 27;226(5252):1211-3 PMID: 4316301
  48. The DNA sequence and genetic organization of a Neurospora mitochondrial plasmid suggest a relationship to introns and mobile elements.
    Cell. 1984 Sep;38(2):441-53 PMID: 6088081
  49. Sequence homology between retroviral reverse transcriptase and putative polymerases of hepatitis B virus and cauliflower mosaic virus.
    Nature. 1983 Oct 27-Nov 2;305(5937):827-9 PMID: 6195530
  50. Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses.
    Nucleic Acids Res. 1984 Sep 25;12(18):7269-82 PMID: 6207485
  51. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster.
    Nature. 1984 Dec 13-19;312(5995):659-61 PMID: 6209583
  52. Origin of retroviruses from cellular moveable genetic elements.
    Cell. 1980 Oct;21(3):599-600 PMID: 6254661
  53. Retroviruses and transposable elements--which came first?
    Nature. 1983 Mar 10;302(5904):105-6 PMID: 6298639
  54. The sequence of carnation etched ring virus DNA: comparison with cauliflower mosaic virus and retroviruses.
    EMBO J. 1986 Dec 1;5(12):3083-90 PMID: 16453731
  55. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons.
    EMBO J. 1987 Dec 20;6(13):3873-80 PMID: 16453815
  56. Amino acid sequence homology in gag region of reverse transcribing elements and the coat protein gene of cauliflower mosaic virus.
    Nucleic Acids Res. 1986 Jan 24;14(2):623-33 PMID: 2418414
  57. Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus.
    Cell. 1986 May 9;45(3):375-85 PMID: 2421920
  58. Reverse transcriptase-dependent synthesis of a covalently linked, branched DNA-RNA compound in E. coli B.
    Cell. 1989 Mar 10;56(5):891-904 PMID: 2466573
  59. Origins and evolutionary relationships of retroviruses.
    Q Rev Biol. 1989 Mar;64(1):1-30 PMID: 2469098
  60. Reverse transcriptases. Retrons in bacteria.
    Nature. 1989 May 25;339(6222):254-5 PMID: 2471077
  61. The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme.
    Mol Gen Genet. 1989 Aug;218(2):257-65 PMID: 2476655
  62. Potential structural motifs for reverse transcriptases.
    Mol Biol Evol. 1989 May;6(3):317-20 PMID: 2482917
  63. A group II intron in the Neurospora mitochondrial coI gene: nucleotide sequence and implications for splicing and molecular evolution.
    Nucleic Acids Res. 1989 Nov 25;17(22):9087-99 PMID: 2531370
  64. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics.
    Nature. 1989 Jan 26;337(6205):376-80 PMID: 2536143
  65. Infectious introns.
    Cell. 1989 Feb 10;56(3):323-6 PMID: 2536590
  66. Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5015-9 PMID: 2544887
  67. Composite transposable elements in the Xenopus laevis genome.
    Mol Cell Biol. 1989 Jul;9(7):3018-27 PMID: 2550791
  68. Transcription and reverse transcription of retrotransposons.
    Annu Rev Microbiol. 1989;43:403-34 PMID: 2552899
  69. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements.
    EMBO J. 1989 Dec 1;8(12):3867-74 PMID: 2555175
  70. Evolutionary relationship between luteoviruses and other RNA plant viruses based on sequence motifs in their putative RNA polymerases and nucleic acid helicases.
    Nucleic Acids Res. 1989 Dec 11;17(23):9543-55 PMID: 2557586
  71. Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression.
    Proc Natl Acad Sci U S A. 1985 May;82(9):2829-33 PMID: 2581255
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1990-10-00
Pages
3353-62
Language
English
Region
England
NLM ID
8208664
PMCID
PMC552073
Subset
IM
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