Skip to main content
SpringerLink
Log in

On the early emergence of reverse transcription: Theoretical basis and experimental evidence

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Reverse transcriptase (RT) was first discovered as an essential catalyst in the biological cycle of retroviruses. However, in the past years evidence has accumulated showing that RTs are involved in a surprisingly large number of RNA-mediated transpositional events that include both viral and nonviral genetic entities. Although it is probable that some RT-bearing genetic elements like the different types of AIDS viruses and the mammalian LINE family have arisen in recent geological times, the possibility that reverse transcription first took place in the early Archean is supported by (1) the hypothesis that RNA preceded DNA as cellular genetic material; (2) the existence of homologous regions of the subunit tau of the E. coli DNA polymerase III with the simian immunodeficiency virus RT, the hepatitis B virus RT, and the β′ subunit of the E. coli RNA polymerase (McHenry et al. 1988); (3) the presence of several conserved motifs, including a 14-amino-acid segment that consists of an Asp-Asp pair flanked by hydrophobic amino acids, which are found in all RTs and in most cellular and viral RNA polymerases. However, whether extant RTs descend from the primitive polymerase involved in the RNA-to-DNA transition remains unproven. Substrate specificity of the AMV and HIV-1 RTs can be modified in the presence of Mn2+, a cation which allows them to add ribonucleotides to an oligo (dG) primer in a template-dependent reaction. This change in specificity is comparable to that observed under similar conditions in other nucleic acid polymerases. This experimentally induced change in RT substrate specificity may explain previous observations on the misincorporation of ribonucleotides by the Maloney murine sarcoma virus RT in the minus and plus DNA of this retrovirus (Chen and Temin 1980). Our results also suggest that HIV-infected macrophages and T-cell cells may contain mixed polynucleotides containing both ribo- and deoxyribonucleotides. The evolutionary significance of these changes in substrate specificities of nucleic acid polymerases is also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

RT:

reverse transcriptase

MMLV:

Moloney murine leukemia virus

MMTV:

mouse mammary tumor virus

HIV:

human immunodeficiency virus

SNV:

spleen necrosis virus

ASLV:

avian sarcoma leukosis virus

RSV:

Rous sarcoma virus

NTPs:

ribonucleotides

dNTPs:

deoxyribonucleotides

References

  • Alberts BM (1986) The function of the hereditary materials: biological catalyses reflect the cell's evolutionary history. Am Zool 26:781–796

    Google Scholar 

  • Argos P (1988) A sequence motif in many polymerases. Nucleic Acid Res 16:9909–9916

    Google Scholar 

  • Auld DS, Kawagachi H, Livingston DM, Vallee BL (1975) Reverse transcriptase from avian myeloblastosis virus: a zinc metalloenzyme. Biochem Biophys Res Comm 62:296–302

    Google Scholar 

  • Babiuk LA, Rouse BT (1976) Ribonucleotides in infectious bovine rhinotracheitis virus DNA. J Gen Virol 31:221–230

    Google Scholar 

  • Baltimore D (1970) RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 226:1209–1211

    Google Scholar 

  • Basu A, Nanduri VB, Gerard GF, Modak MJ (1988) Substrate binding domain of Murine leukemia virus reverse transcriptase. J Biol Chem 263:1648–1653

    Google Scholar 

  • Berg P, Fancher H, Chamberlin M (1963) The synthesis of mixed polynucleotides containing ribo- and deoxyribonucleotides by purified preparations of DNA polymerase from Escherichia coli. In: Vogel HJ, Bryson V, Lampen JO (eds) informational macromolecules. Academic Press, New York, pp 467–483

    Google Scholar 

  • Bernard A, Lazaro JM, Salas M, Blanco L (1990) The highly conserved amino acid sequence motif Tyr-Gly-Asp-Thr-Asp-Ser in alpha-like DNA polymerases is required by phage o 29 DNA polymerase for protein-primed initiation and polymerization. Proc Natl Acad Sci USA 87:4610–4614

    Google Scholar 

  • Biswal N, Benyesh-Melnick M (1969) Complementary nuclear RNAs of murine sarcoma-leukemia virus complex in transformed cells. Proc Natl Acad Sci USA 64:1372–1379

    Google Scholar 

  • Blanco L, Bernard A, Blasco MA, Salas M (1991) A general structure for DNA-dependent DNA polymerases. Gene 100: 27–38

    Google Scholar 

  • Bolden A, Fry M, Muller R, Citarella R, Weissbach A (1972) The presence of a polyriboadenylic acid-dependent DNA polymerase in eukaryotic cells. Arch Biochem Biophys 153:26–33

    Google Scholar 

  • Cech T (1989) Ribozyme self-replication? Nature 339:507–508

    Google Scholar 

  • Chen IS, Temin HE (1980) Ribonucleotides in unintegrated linear spleen necrosis virus DNA. J Virol 33:1058–1073

    Google Scholar 

  • Coffin JM (1986) Genetic variation in AIDS viruses. Cell 46:1–4

    Google Scholar 

  • Cove DJ (1974) Evolutionary significance of autogenous regulation. Nature 251:256

    Google Scholar 

  • Crick FHC (1968) The origin of the genetic code. J Mol Biol 38:367–379

    Google Scholar 

  • Darnell JE (1985) RNA. Sci Am 253:54–64

    Google Scholar 

  • Darnell JE, Doolittle WF (1986) Speculations on the early course of evolution. Proc Natl Sci USA 83:1271–1275

    Google Scholar 

  • Delarue M, Poch M, Tordo N, Moras D, Argos P (1990) An attempt to unify the structure of polymerases. Protein Engineering 3:461–467

    Google Scholar 

  • Domingo E, Martinez-Salas E, Sobrino F, de la Torre JC, Portela A, Ortin J, Lopez-Galindez C, Perez-Brena P, Villanueva N, Najera R, Van de Pol S, Steinhauer D, DePolo N, Holland JJ (1985) The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance—a review. Gene 40:1–8

    Google Scholar 

  • Doolittle RF (1989) Immunodeficiency viruses: the simian-human connection. Nature 339:338–339

    Google Scholar 

  • Doolittle RF, Feng DF, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Quart Rev Biol 64:1–30

    Google Scholar 

  • Edenberg HJ, Huberman JA (1975) Eukaryotic chromosome replication. Ann Rev Genet 9:245–284

    Google Scholar 

  • Fridlender B, Fry M, Bolden M, Weissbach A (1972) A new synthetic RNA-dependent DNA polymerase from human tissue culture cells. Proc Natl Acad Sci USA 69:452–455

    Google Scholar 

  • Fuetterer J, Hohn T (1987) Involvement of nucleocapsids in reverse transcription: a general phenomenon? Trends Biochem Sci 12:92–95

    Google Scholar 

  • Gerard GF, D'Alessio JM, Kotewicz ML, Noon MC (1986) Influence on stability in Escherichia coli of the carboxy-terminal structure of cloned Moloney murine leukemia virus reverse transcriptase. DNA 5:271–279

    Google Scholar 

  • Gerard GF, Rottman F, Green M (1976) Poly (2′-0-methylcytidylate) oligodeoxyguanylate as a template for the ribonucleic acid directed deoxyribonucleic acid polymerase in ribonucleic acid tumor virus particles and a specific probe for the ribonucleic acid directed enzyme in transformed murine cell. Biochemistry 13:1632–1641

    Google Scholar 

  • Gilbert W (1986) The RNA world. Nature 319:618

    Google Scholar 

  • Gillam S, Jahnke P, Smith M (1978) Enzymatic synthesis of oligodeoxyribonucleotides of defined sequence. J Biol Chem 253:2532–2539

    Google Scholar 

  • Goodman TC, Nagel L, Rappold W, Klotz G, Riesner D (1984) Viroid replication: equilibrium association constant and comparative activity measurements for the viroid-polymerase interaction. Nucleic Acid Res 12:6231–6246

    Google Scholar 

  • Grossman LI, Watson R, Vinograd J (1973) The presence of ribonucleotides in mature closed circular mitochondrial DNA. Proc Natl Acad Sci USA 70:3339–3343

    Google Scholar 

  • Helene C, Maurizot JC (1981) Interactions of oligopeptides with nucleic acids. CRC Critical Rev Biochem 10:213–258

    Google Scholar 

  • Hizi A, McGill C, Hughes SH (1988) Expression of soluble, enzymatically active, human immunodeficiency virus reverse transcriptase in Escherichia coli and analysis of mutants. Proc Natl Acad Sci USA 85:1218–1222

    Google Scholar 

  • Holland J, Spindler K, Horodyski F, Graban E, Nichols S, VandePol S (1982) Rapid evolution of RNA genomes. Science 215:1577–1585

    Google Scholar 

  • Horowitz NH (1945) On the evolution of biochemical syntheses. Proc Natl Acad Sci USA 31:153–157

    Google Scholar 

  • Horowitz NH (1965) The evolution of biochemical syntheses—retrospect and prospect. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 15–23

    Google Scholar 

  • Hsieh WT (1971) Polymerization of deoxyribonucleoside diphosphates from and Escherichia coli mutant lacking deoxyribonucleic acid polymerase activity. J Biol Chem 246:1780–1784

    Google Scholar 

  • Hull R, Covey SN (1983) Does cauliflower mosaic virus replicate by reverse transcription? Trends Biochem Sci 8:119–121

    Google Scholar 

  • Hull R, Sadler J, Longstaff M (1986) The sequence of carnation etched ring virus DNA: comparison with cauliflower mosaic virus and retroviruses. EMBO J 5:3083–3090

    Google Scholar 

  • Inokuchi Y, Hirashima A (1987) Interference with viral infection by defective RNA replicase. J Virol 61:3946–3949

    Google Scholar 

  • Inouye S, Hsu M-Y, Eagle S, Inouye M (1989) Reverse transcriptase associated with the biosynthesis of the branched RNA-linked ms DNA in Myxococcus xanthus. Cell 56:706–717

    Google Scholar 

  • Jensen RA (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol 30:409–425

    Google Scholar 

  • Jensen RA, Byng GS (1982) The partioning of biochemical pathways with isosymes systems. In: Rattazi MC, Scandalios JG, Whitt GS (eds) Isozymes: current topics in biological and medical research, vol 5. Alan R Liss, New York, pp 143–175

    Google Scholar 

  • Johnson MS, McClure MA, Feng DF, Gray J, Doolittle RF (1986) Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc Natl Acad Sci USA 83:7648–7652

    Google Scholar 

  • Joyce GF (1989) RNA evolution and the origins of life. Nature 338:217–224

    Google Scholar 

  • Joyce GF, Schwartz AW, Miller SL, Orgel LE (1987) The case for an ancestral genetic system involving simple analogues of the nucleotides. Proc Natl Acad Sci USA 84:4398–4402

    Google Scholar 

  • Kadama K, Ogasawara N, Yoshikawa H, Murakami S (1985) Nucleotide sequence of a cloned woodchuck hepatitis virus genome: evolutionary relationships between hepadnaviruses. J Virol 56:978–986

    Google Scholar 

  • Kamer G, Argos P (1984) Primary structural comparisons of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acid Res 12:7269–7282

    Google Scholar 

  • Kaplan PN, Greeman RL, Geirn JL, Purcell RH, Robinson WS (1973) DNA polymerase associated with human hepatitis B antigen. J Virol 12:995–1005

    Google Scholar 

  • Karkas JD (1973) Reverse transcription by Escherichia coli polymerase I. Proc Natl Acad Sci USA 70:3834–3838

    Google Scholar 

  • Karkas JD, Jannis GS, Chargaff E (1972) Action of DNA polymerase I of Escherichi coli with DNA-RNA hybrids as templates. Proc Natl Acad Sci USA 69:398–402

    Google Scholar 

  • Katz RA, Skalka AM (1988) A C-terminal domain in the Avian Sarcoma-Leukosis virus pol gene product is not essential for viral replication. J Virol 62:528–533

    Google Scholar 

  • Kiessling AA, Goulian M (1976) A comparison of the enzymatic responses of the DNA polymerases from four RNA tumor viruses. Biochem Biophys Res Comm 71:1069–1077

    Google Scholar 

  • Knesek JE, Nash MA, Chan JC, Bartlett RJ, Bowen JM, East JL (1980) Intracellular RNA complementary to the RNA genome of the Moloney murine sarcoma virus complex. Virology 100: 288–299

    Google Scholar 

  • Konarska MM, Sharp PA (1989) Replication of RNA by the DNA-dependent RNA polymerase of Phage T7. Cell 57:423–431

    Google Scholar 

  • Kornberg A (1977) Multiple stages in the enzymic replication of DNA. Biochem Soc Trans 5:359–374

    Google Scholar 

  • Koshland DE (1976) The evolution of function in enzymes. Fed Proc 35:2104–2111

    Google Scholar 

  • Lampson BC, Inouye M, Inouye S (1989a) Reverse transcriptase with concomitant ribonuclease H activity in the cell-free synthesis of branched RNA-linked msDNA of Myxococcus xanthus. Cell 56:701–707

    Google Scholar 

  • Lampson BC, Sun J, Hsu MY, Vallejo-Ramirez J, Inouye S, Inouye M (1989b) Reverse transcriptase in a clinical strain of Escherichia coli: production of branched RNA-linked msDNA. Science 243:1033–1037

    Google Scholar 

  • Larden BA, Purifoy DJM, Powell KL, Darby G (1987) Site specific mutagenesis of AIDS virus reverse transcriptase. Nature 327:716–717

    Google Scholar 

  • Lazcano A (1986) Prebiotic evolution and the organ of cells. Treballs Soc Cat Biol 39:73–103

    Google Scholar 

  • Lazcano A, Fastag J, Gariglio P, Ramirez C, Oro J (1988a) On the early evolution of RNA polymerase. J Mol Evol 27:365–376

    Google Scholar 

  • Lazcano A, Guerrero R, Margulis L, Oro J (1988b) The evolutionary transition from RNA to DNA in early cells. J Mol Evol 27:283–290

    Google Scholar 

  • Lazcano A, Gariglio P, Orozco E, Oro J (1989) On the early evolution of reverse transcriptase. Abstracts of the 6th Meeting of the International Society for the Study of the Origins of Life, Prague, Checoslovakia, July 3–8, 1989, 166–167

  • Lazcano A, Fox GE, Oro J (1992) Life before DNA: the origin and evolution of early Archean cells. In: Mortlock RP (ed) The evolution of metabolic function. CRC Press, Boca Raton, pp. 237–295

    Google Scholar 

  • Li WH (1983) Evolution of duplicate genes and pseudogenes. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer Press, Sunderland, MA, pp 14–37

    Google Scholar 

  • Li WH, Tanimura M, Sharp PM (1988) Rates and dates of divergence between AIDS virus nucleotide sequences. Mol Biol Evol 5:313–330

    Google Scholar 

  • Llaca V, Silva E, Lazcano A, Rangel LM, Gariglio P, Oro J (1987) In search of the ancestral RNA polymerase: an experimental approach. In: F Eirich, C Ponnamperuma (eds) Prebiological organization: proceedings of the VIII College Park Colloquium on Chemical Evolution. A Decker Publ, Hampton, VA, pp 247–260

    Google Scholar 

  • Loeb LA, Mildvan AS (1981) The role of metal ions in the fidelity of DNA and RNA synthesis. In: Eichhorn GL, Manzilli LG (eds) Metal ions in genetic information transfer. Elsevier/ North Holland, New York, pp 125–142

    Google Scholar 

  • Loeb LA, Tartof KD, Travaglini EC (1973) Copying natural RNAs with E. coli DNA polymerase I. Nature 242:66–69

    Google Scholar 

  • Mandart E, Kay A, Galibert F (1984) Nucleotide sequence of a cloned duck hepatitis B virus genome: comparison with woodchuck and human hepatitis B virus sequences. J Virol 49:782–792

    Google Scholar 

  • Marco Y, Howell SH (1984) Intracellular forms of viral DNA consistent with a model of reverse transcriptional replication of the cauliflower mosaic virus genome. Nucleic Acid Res 12:1517–1528

    Google Scholar 

  • Marcus SL, Modak MJ (1976) Observations on template specific conditions for DNA synthesis by avian myeloblastosis virus DNA polymerase. Nucleic Acid Res 3:1473–1486

    Google Scholar 

  • Matthews REF (1981) Plant virology. Academic Press, New York

    Google Scholar 

  • McHenry CS, Flower AM, Hawker JR (1988) Coordination of leading with lagging strand synthesis by the asymmetric dimeric DNA polymerase III holoenzyme of Escherichia coli. Cancer Cells 6:35–41

    Google Scholar 

  • McClure MA, Johnson MS, Feng DF, Doolittle RF (1988) Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci USA 85:2469–2473

    Google Scholar 

  • McMacken R, Kornberg A (1978) A multienzyme system for priming the replication of OX174 viral DNA. J Biol Chem 253:3313–3319

    Google Scholar 

  • Mildvan AS, Loeb LA (1979) The role of metal ions in the mechanisms of DNA and RNA polymerases. CRC Crit Rev Biochem 6:219–244

    Google Scholar 

  • Mildvan AS, Loeb LA (1981) The role of metal ions in the mechanism of DNA and RNA polymerases. In: Eichhorn GL, Marzilli LG (eds) Metal ions in genetic information transfer. Elsevier/North Holland, New York, pp 103–123

    Google Scholar 

  • Miller RH, Robinson WS (1986) Common evolutionary origin of hepatitis B virus and retroviruses. Proc Natl Acad Sci USA 83:2531–2535

    Google Scholar 

  • Modak MJ, Dumaswala UJ (1981) Divalent cation-dependent pyridoxal 5′-phosphate inhibition of Rauscher leukemia virus DNA polymerase. Biochem Biophys Acta 654:227–235

    Google Scholar 

  • Ono Y, Onda H, Sasada R, Igarashi K, Sugino Y, Nishioka K (1983) The complete nucleotide sequences of the cloned hepatitis B virus DNA: subtypes adr and adw. Nucleic Acid Res 11:1747–1757

    Google Scholar 

  • Orgel LE (1968) Evolution of the genetic apparatus. J Mol Biol 38:380–393

    Google Scholar 

  • Oro J, Lazcano-Araujo A (1984) A minimal living system and the origin of a protocell. Adv Space Res 4:167–176

    Google Scholar 

  • Oro J, Miller SL, Lazcano A (1990) The origin and early evolution of life on Earth. Annu Rev Earth Planet Sci 18:317–356

    Google Scholar 

  • Pace NR, Marsh TL (1985) RNA catalysis and the origin of life. Origins Life 16:97–116

    Google Scholar 

  • Pande S, Lemire EG, Nargang FE (1989) The mitochondrial plasmid from Neurospora intermedia strain LaBelle-1b contains a long open reading frame with blocks of amino acids characteristic of reverse transcriptases and related proteins. Nuclei Acid Res 17:2023–2042

    Google Scholar 

  • Pezzano H, Podo F (1980) Structure of binary complexes of mono- and polynucleotides with metal ions of the first transition group. Chem Rev 80:365–401

    Google Scholar 

  • Poch O, Sauvaget I, Delarue M, Tordo N (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8:3867–3874

    Google Scholar 

  • Poiesz BJ, Battula N, Loeb LA (1974) Zinc in reverse transcriptase. Biochem Biophys Res Comm 56:959–964

    Google Scholar 

  • Preston BD, Poiesz BJ, Loeb LA (1988) Fidelity of HIV-1 reverse transcriptase. Science 242:1168–1171

    Google Scholar 

  • Reanney DC (1982) The evolution of RNA viruses. Annu Rev Microbiol 36:47–73

    Google Scholar 

  • Roberts JD, Bebenek K, Kunkel TA (1988) The accuracy of reverse transcriptase from HIV-1. Science 242:1171–1173

    Google Scholar 

  • Rosenkranz HS (1973) RNA in coliphage T5. Nature 242:327–329

    Google Scholar 

  • Rowen L, Komberg A (1978) A ribo-deoxyribonucleotide primer synthesized by primase. J Biol Chem 253:770–774

    Google Scholar 

  • Sarngadharan MG, Allaudeen HS, Gallo RC (1976) Reverse transcriptase activity of RNA tumor viruses and animal cells. Methods Cancer Res 12:3–47

    Google Scholar 

  • Schulte U, Lambowitz AM (1991) The LaBelle mitochondrial plasmid of Neurospora intermedia encodes a novel DNA polymerase that may be derived from a reverse transcriptase. Mol Cell Biol 11:1696–1706

    Google Scholar 

  • Sharp PA (1985) On the origin of RNA splicing and introns. Cell 42:397–400

    Google Scholar 

  • Shen C, Lazcano A, Oro J (1989) Enhancing effects of histidylhistidine in some prebiotic reactions. J Mol Evol (submitted)

  • Shin Y (1973) Interaction of metal ions with polynucleotides and related compounds. XXII. Effect of divalent metal ions on the conformational changes of polyribonucleotides. Biopolymers 12:2459–2475

    Google Scholar 

  • Smith TF, Srinivasan A, Schochetman G, Marcus M, Myers G (1988) The phylogenetic history of immunodeficiency viruses. Nature 333:573–575

    Google Scholar 

  • Spadari S, Weissbach A (1974) HeLa cell R-deoxyribonucleic acid polymerase. J Biol Chem 249:5809–5815

    Google Scholar 

  • Speyer JF, Chao J, Chao L (1972) Ribonucleotides covalently linked to deoxyribonucleic acid in T4 bacteriophage. J Virol 10:902–908

    Google Scholar 

  • Stavnezer E, Ringold G, Varmus HE, Bishop M (1976) RNA complementary to the genome of RNA tumor viruses in virions and virus-producing cells. J Virol 20:342–347

    Google Scholar 

  • Steinhauer DA, Holland JJ (1987) Rapid evolution of RNA viruses. Annu Rev Microbiol 41:409–433

    Google Scholar 

  • Summers JA, Mason WS (1982) Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 29:403–415

    Google Scholar 

  • Summers JA, O'Connell A, Millman I (1975) Genome of hepatitis B virus: restriction enzyme cleavage and structure of DNA extracted from Dane particles. Proc Natl Acad Sci USA 72: 4597–4601

    Google Scholar 

  • Sundquist B, Oberg B (1979) Phosphonoformate inhibits reverse transcription. J Gen Virol 45:273–281

    Google Scholar 

  • Tanese N, Goff SP (1988) Domain structure of the Maloney murine leukemia virus reverse transcriptase: mutational analysis and separate expression of the DNA polymerase and RNAse H activities. Proc Natl Acad Sci USA 85:1777–1781

    Google Scholar 

  • Temin HM (1970) Malignant transformation of cells by viruses. Perspect Biol Med 14:11–26

    Google Scholar 

  • Temin HM (1971) The protovirus hypothesis. J Natl Cancer Inst 46:III-VII

    Google Scholar 

  • Temin HM (1985) Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol Biol Evol 2:455–468

    Google Scholar 

  • Temin HM (1989) Retrons in bacteria. Nature 339:254–255

    Google Scholar 

  • Temin HM, Mizutani M (1970) RNA-directed DNA polymerase in virions of Rous sarcoma virus. Nature 226:1211–1213

    Google Scholar 

  • Toh H, Hayashida H, Miyata T (1983) Homology of reverse transcriptase of retrovirus with putative polymerase gene products of hepatitis B virus and cauliflower mosaic virus. Nature 305:827–829

    Google Scholar 

  • Valverde V, Greco-Hernandez, Oro J, Gariglio P, Lazcano A (1989) Caracterizacion de la actividad de RNA replicasa que la reverso transcriptasa del VIH-1 presenta in vitro. Resumenes del II Congreso Nacional sobre SIDA. Mexico, DF, Noviembre 13–16, 1989

  • Vamvakopoulos NC, Vournakis JN, Marcus SL (1977) The effect of magnesium and manganese ions on the structure and template activity for reverse transcriptase of polyribocytidylate and its 2'-o-methyl derivative. Nucleic Acid Res 4: 3589–3597

    Google Scholar 

  • Varmus H (1987) Reverse transcription. Sci AM 257:56–64

    Google Scholar 

  • Varmus H (1989) Reverse transcription in bacteria. Cell 56:721–724

    Google Scholar 

  • Varmus HE, Swanstrom R (1982) Replication of retroviruses. In: Weiss R, Teich N, Varmus H, Coffin J (eds) RNA tumor viruses, vol 1. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 369–512

    Google Scholar 

  • Varmus H, Brown P (1989) Retroviruses. In: Howe M, Berg, D (s) Mobile DNA elements. American Society of Microbiology, Washington, DC, pp 53–108

    Google Scholar 

  • Velasco AM, Medrano L, Lazcano A, Oró J (1992) A redefinition of the Asp-Asp domain of reverse transcriptases. J Mol Evol 35:551–556

    Google Scholar 

  • Verma IM (1977) The reverse transcriptase. Biochem Biophys Acta 473:1–38

    Google Scholar 

  • Visscher J, Schwartz AW (1989) Manganese-catalyzed oligomerizations of nucleotide analogs. J Mol Evol 29:284–287

    Google Scholar 

  • Waley SG (1969) Some aspects of the evolution of metabolic pathways. Comp Biochem Physiol 30:1–11

    Google Scholar 

  • Wang TSF, Wong SW, Kom D (1989) Human DNA polymerase alpha: predicted functional domains and relationships with viral DNA polymerases. FASEB J 3:14–21

    Google Scholar 

  • Weiner AM (1987) The origins of life. In Watson JD, Hopkins NH, Roberts JW, Steitz JA, Weiner AM (eds) Molecular biology of the gene, vol II. Benjamin Cummings, Menlo Park CA, pp 1098–1160

    Google Scholar 

  • Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes and transposable elements generated by the reverse flow of genetic information. Ann Rev Biochem 55:631–661

    Google Scholar 

  • Wintersberger U, Wintersberger E (1987) RNA makes DNA: a speculative view of the evolution of DNA replication mechanisms. Trends Genet 3:198–202

    Google Scholar 

  • Woese CR (1967) The origins of the genetic code. Harper and Row, New York

    Google Scholar 

  • Wong SW, Wahl AF, Yuan MP, Arai N, Pearson BE, Arai K, Korn D, Hunkapiller MW, Wang TSF (1988) Human DNA polymerase alpha gene expression is cell proliferation dependent and its primary structure is similar to both prokaryotic and eukaryotic replicative DNA polymerases. EMBO J 7:37–47

    Google Scholar 

  • Xiong Y, Eickbush TH (1988) Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol 5:675–690

    Google Scholar 

  • Zavriev SK, Borisova OV (1987) Possible functional role of the “DD-domain” of RNA-dependent polymerases. Molekuyarnaya Biologiya 21:229–241 (English translation)

    Google Scholar 

  • Zuckerkandl E (1970) The cell machinery in its relation to biogenesis. Rev Eur Etud Clin Biol XV:369–374

    Google Scholar 

  • Zuckerkandl E (1975) The appearance of new structures and functions in proteins during evolution. J Mol Evol 7:1–57

    Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8:357–366

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Biología, Facultad de Ciencias-UNAM, Cd. Universitaria, Apartado Postal 70-407, 04511, D.F., México, México

    A. Lazcano, V. Valverde & G. Hernández

  2. Departamento de Genética y Biología Molecular, CINVESTAV-IPN, Apartado Postal 14-740, 07000, D.F., México, México

    P. Gariglio

  3. Departamento de Genética y Patología Experimental, Instituto Nacional de Salud Pública, CISEI, Cuernavaca, Morelos, México

    V. Valverde & P. Gariglio

  4. Department of Biochemical & Biophysical Sciences, University of Houston, 77204-5500, Houston, TX, USA

    G. E. Fox & J. Oró

Authors
  1. A. Lazcano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Valverde
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Gariglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. E. Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Oró
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Offprint requests to: A. Lazcano

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lazcano, A., Valverde, V., Hernández, G. et al. On the early emergence of reverse transcription: Theoretical basis and experimental evidence. J Mol Evol 35, 524–536 (1992). https://doi.org/10.1007/BF00160213

Download citation

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160213

Key words

Search

Navigation