Abstract
The proposal that RNA preceded DNA in evolution is more than 15 years old. In light of recent studies on RNA processing (including protein-free reactions), present knowledge about eukaryotic gene structure, and studies comparing ribosomal RNA sequences, we propose a train of events for precellular and early cellular evolution.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anson D. S., Choo K. H., Rees D. J., Giannelli F., Gould K., Huddleston J. A., Brownlee G. G. The gene structure of human anti-haemophilic factor IX. EMBO J. 1984 May;3(5):1053–1060. doi: 10.1002/j.1460-2075.1984.tb01926.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baltimore D. RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature. 1970 Jun 27;226(5252):1209–1211. doi: 10.1038/2261209a0. [DOI] [PubMed] [Google Scholar]
- Baltimore D. Retroviruses and retrotransposons: the role of reverse transcription in shaping the eukaryotic genome. Cell. 1985 Mar;40(3):481–482. doi: 10.1016/0092-8674(85)90190-4. [DOI] [PubMed] [Google Scholar]
- Bargiello T. A., Young M. W. Molecular genetics of a biological clock in Drosophila. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2142–2146. doi: 10.1073/pnas.81.7.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Belfort M., Pedersen-Lane J., West D., Ehrenman K., Maley G., Chu F., Maley F. Processing of the intron-containing thymidylate synthase (td) gene of phage T4 is at the RNA level. Cell. 1985 Jun;41(2):375–382. doi: 10.1016/s0092-8674(85)80010-6. [DOI] [PubMed] [Google Scholar]
- Berget S. M., Moore C., Sharp P. A. Spliced segments at the 5' terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3171–3175. doi: 10.1073/pnas.74.8.3171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blake C. Exons--present from the beginning? Nature. 1983 Dec 8;306(5943):535–537. doi: 10.1038/306535a0. [DOI] [PubMed] [Google Scholar]
- Blanchetot A., Wilson V., Wood D., Jeffreys A. J. The seal myoglobin gene: an unusually long globin gene. Nature. 1983 Feb 24;301(5902):732–734. doi: 10.1038/301732a0. [DOI] [PubMed] [Google Scholar]
- Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
- Brändén C. I., Eklund H., Cambillau C., Pryor A. J. Correlation of exons with structural domains in alcohol dehydrogenase. EMBO J. 1984 Jun;3(6):1307–1310. doi: 10.1002/j.1460-2075.1984.tb01967.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burke J. M., RajBhandary U. L. Intron within the large rRNA gene of N. crassa mitochondria: a long open reading frame and a consensus sequence possibly important in splicing. Cell. 1982 Dec;31(3 Pt 2):509–520. doi: 10.1016/0092-8674(82)90307-5. [DOI] [PubMed] [Google Scholar]
- Cech T. R. RNA splicing: three themes with variations. Cell. 1983 Oct;34(3):713–716. doi: 10.1016/0092-8674(83)90527-5. [DOI] [PubMed] [Google Scholar]
- Craik C. S., Buchman S. R., Beychok S. Characterization of globin domains: heme binding to the central exon product. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1384–1388. doi: 10.1073/pnas.77.3.1384. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crick F. H., Brenner S., Klug A., Pieczenik G. A speculation on the origin of protein synthesis. Orig Life. 1976 Dec;7(4):389–397. doi: 10.1007/BF00927934. [DOI] [PubMed] [Google Scholar]
- Crick F. H. The origin of the genetic code. J Mol Biol. 1968 Dec;38(3):367–379. doi: 10.1016/0022-2836(68)90392-6. [DOI] [PubMed] [Google Scholar]
- Darnell J. E., Jr Implications of RNA-RNA splicing in evolution of eukaryotic cells. Science. 1978 Dec 22;202(4374):1257–1260. doi: 10.1126/science.364651. [DOI] [PubMed] [Google Scholar]
- Darnell J. E., Jr The processing of RNA. Sci Am. 1983 Oct;249(4):90–100. doi: 10.1038/scientificamerican1083-90. [DOI] [PubMed] [Google Scholar]
- Doolittle R. F. Proteins. Sci Am. 1985 Oct;253(4):88–99. doi: 10.1038/scientificamerican1085-88. [DOI] [PubMed] [Google Scholar]
- Folk W. R., Berg P. Duplication of the structural gene for glycyl-transfer RNA synthetase in Escherichia coli. J Mol Biol. 1971 Jun 14;58(2):595–610. doi: 10.1016/0022-2836(71)90374-3. [DOI] [PubMed] [Google Scholar]
- Gilbert W. Genes-in-pieces revisited. Science. 1985 May 17;228(4701):823–824. doi: 10.1126/science.4001923. [DOI] [PubMed] [Google Scholar]
- Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
- Go M. Correlation of DNA exonic regions with protein structural units in haemoglobin. Nature. 1981 May 7;291(5810):90–92. doi: 10.1038/291090a0. [DOI] [PubMed] [Google Scholar]
- Guerrier-Takada C., Gardiner K., Marsh T., Pace N., Altman S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 1983 Dec;35(3 Pt 2):849–857. doi: 10.1016/0092-8674(83)90117-4. [DOI] [PubMed] [Google Scholar]
- Hand R. Eucaryotic DNA: organization of the genome for replication. Cell. 1978 Oct;15(2):317–325. doi: 10.1016/0092-8674(78)90001-6. [DOI] [PubMed] [Google Scholar]
- Hitzeman R. A., Hagie F. E., Hayflick J. S., Chen C. Y., Seeburg P. H., Derynck R. The primary structure of the Saccharomyces cerevisiae gene for 3-phosphoglycerate kinase. Nucleic Acids Res. 1982 Dec 11;10(23):7791–7808. doi: 10.1093/nar/10.23.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holland J. P., Holland M. J. Structural comparison of two nontandemly repeated yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem. 1980 Mar 25;255(6):2596–2605. [PubMed] [Google Scholar]
- Inoue T., Orgel L. E. A nonenzymatic RNA polymerase model. Science. 1983 Feb 18;219(4586):859–862. doi: 10.1126/science.6186026. [DOI] [PubMed] [Google Scholar]
- Jaenisch R. Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1260–1264. doi: 10.1073/pnas.73.4.1260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jagadeeswaran P., Forget B. G., Weissman S. M. Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse transcription of RNA pol III transcripts? Cell. 1981 Oct;26(2 Pt 2):141–142. doi: 10.1016/0092-8674(81)90296-8. [DOI] [PubMed] [Google Scholar]
- Jelinek W. R., Schmid C. W. Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem. 1982;51:813–844. doi: 10.1146/annurev.bi.51.070182.004121. [DOI] [PubMed] [Google Scholar]
- Konarska M. M., Padgett R. A., Sharp P. A. Trans splicing of mRNA precursors in vitro. Cell. 1985 Aug;42(1):165–171. doi: 10.1016/s0092-8674(85)80112-4. [DOI] [PubMed] [Google Scholar]
- Kruger K., Grabowski P. J., Zaug A. J., Sands J., Gottschling D. E., Cech T. R. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell. 1982 Nov;31(1):147–157. doi: 10.1016/0092-8674(82)90414-7. [DOI] [PubMed] [Google Scholar]
- Lonberg N., Gilbert W. Intron/exon structure of the chicken pyruvate kinase gene. Cell. 1985 Jan;40(1):81–90. doi: 10.1016/0092-8674(85)90311-3. [DOI] [PubMed] [Google Scholar]
- Löhler J., Timpl R., Jaenisch R. Embryonic lethal mutation in mouse collagen I gene causes rupture of blood vessels and is associated with erythropoietic and mesenchymal cell death. Cell. 1984 Sep;38(2):597–607. doi: 10.1016/0092-8674(84)90514-2. [DOI] [PubMed] [Google Scholar]
- Michelson A. M., Blake C. C., Evans S. T., Orkin S. H. Structure of the human phosphoglycerate kinase gene and the intron-mediated evolution and dispersal of the nucleotide-binding domain. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6965–6969. doi: 10.1073/pnas.82.20.6965. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nikolaev N., Silengo L., Schlessinger D. Synthesis of a large precursor to ribosomal RNA in a mutant of Escherichia coli. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3361–3365. doi: 10.1073/pnas.70.12.3361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orgel L. E. Evolution of the genetic apparatus. J Mol Biol. 1968 Dec;38(3):381–393. doi: 10.1016/0022-2836(68)90393-8. [DOI] [PubMed] [Google Scholar]
- Pfeiffer P., Hohn T. Involvement of reverse transcription in the replication of cauliflower mosaic virus: a detailed model and test of some aspects. Cell. 1983 Jul;33(3):781–789. doi: 10.1016/0092-8674(83)90020-x. [DOI] [PubMed] [Google Scholar]
- Reanney D. C. On the origin of prokaryotes. J Theor Biol. 1974 Nov;48(1):243–251. doi: 10.1016/0022-5193(74)90194-5. [DOI] [PubMed] [Google Scholar]
- Reanney D. RNA splicing and polynucleotide evolution. Nature. 1979 Feb 22;277(5698):598–600. doi: 10.1038/277598b0. [DOI] [PubMed] [Google Scholar]
- Rigby P. W., Burleigh B. D., Jr, Hartley B. S. Gene duplication in experimental enzyme evolution. Nature. 1974 Sep 20;251(5472):200–204. doi: 10.1038/251200a0. [DOI] [PubMed] [Google Scholar]
- Rossmann M. G., Argos P. Protein folding. Annu Rev Biochem. 1981;50:497–532. doi: 10.1146/annurev.bi.50.070181.002433. [DOI] [PubMed] [Google Scholar]
- Rossmann M. G., Moras D., Olsen K. W. Chemical and biological evolution of nucleotide-binding protein. Nature. 1974 Jul 19;250(463):194–199. doi: 10.1038/250194a0. [DOI] [PubMed] [Google Scholar]
- Russell D. W., Smith M., Williamson V. M., Young E. T. Nucleotide sequence of the yeast alcohol dehydrogenase II gene. J Biol Chem. 1983 Feb 25;258(4):2674–2682. [PubMed] [Google Scholar]
- Sharp P. A. Conversion of RNA to DNA in mammals: Alu-like elements and pseudogenes. Nature. 1983 Feb 10;301(5900):471–472. doi: 10.1038/301471a0. [DOI] [PubMed] [Google Scholar]
- Sharp P. A. On the origin of RNA splicing and introns. Cell. 1985 Sep;42(2):397–400. doi: 10.1016/0092-8674(85)90092-3. [DOI] [PubMed] [Google Scholar]
- Solnick D. Trans splicing of mRNA precursors. Cell. 1985 Aug;42(1):157–164. doi: 10.1016/s0092-8674(85)80111-2. [DOI] [PubMed] [Google Scholar]
- Stark B. C., Kole R., Bowman E. J., Altman S. Ribonuclease P: an enzyme with an essential RNA component. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3717–3721. doi: 10.1073/pnas.75.8.3717. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stone E. M., Rothblum K. N., Schwartz R. J. Intron-dependent evolution of chicken glyceraldehyde phosphate dehydrogenase gene. Nature. 1985 Feb 7;313(6002):498–500. doi: 10.1038/313498a0. [DOI] [PubMed] [Google Scholar]
- Südhof T. C., Goldstein J. L., Brown M. S., Russell D. W. The LDL receptor gene: a mosaic of exons shared with different proteins. Science. 1985 May 17;228(4701):815–822. doi: 10.1126/science.2988123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Südhof T. C., Russell D. W., Goldstein J. L., Brown M. S., Sanchez-Pescador R., Bell G. I. Cassette of eight exons shared by genes for LDL receptor and EGF precursor. Science. 1985 May 17;228(4701):893–895. doi: 10.1126/science.3873704. [DOI] [PubMed] [Google Scholar]
- Temin H. M., Mizutani S. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature. 1970 Jun 27;226(5252):1211–1213. doi: 10.1038/2261211a0. [DOI] [PubMed] [Google Scholar]
- Tonegawa S., Maxam A. M., Tizard R., Bernard O., Gilbert W. Sequence of a mouse germ-line gene for a variable region of an immunoglobulin light chain. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1485–1489. doi: 10.1073/pnas.75.3.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Arsdell S. W., Denison R. A., Bernstein L. B., Weiner A. M., Manser T., Gesteland R. F. Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell. 1981 Oct;26(1 Pt 1):11–17. doi: 10.1016/0092-8674(81)90028-3. [DOI] [PubMed] [Google Scholar]
- Waring R. B., Scazzocchio C., Brown T. A., Davies R. W. Close relationship between certain nuclear and mitochondrial introns. Implications for the mechanism of RNA splicing. J Mol Biol. 1983 Jul 5;167(3):595–605. doi: 10.1016/s0022-2836(83)80100-4. [DOI] [PubMed] [Google Scholar]
- Watson N., Gurevitz M., Ford J., Apirion D. Self cleavage of a precursor RNA from bacteriophage T4. J Mol Biol. 1984 Jan 25;172(3):301–323. doi: 10.1016/s0022-2836(84)80028-5. [DOI] [PubMed] [Google Scholar]
- Wilde C. D., Crowther C. E., Cripe T. P., Gwo-Shu Lee M., Cowan N. J. Evidence that a human beta-tubulin pseudogene is derived from its corresponding mRNA. Nature. 1982 May 6;297(5861):83–84. doi: 10.1038/297083a0. [DOI] [PubMed] [Google Scholar]
- Woese C. R. A comment on methanogenic bacteria and the primitive ecology. J Mol Evol. 1977 Aug 5;9(4):369–371. doi: 10.1007/BF01796101. [DOI] [PubMed] [Google Scholar]
- Woese C. R., Gutell R., Gupta R., Noller H. F. Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev. 1983 Dec;47(4):621–669. doi: 10.1128/mr.47.4.621-669.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang D., Oyaizu Y., Oyaizu H., Olsen G. J., Woese C. R. Mitochondrial origins. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4443–4447. doi: 10.1073/pnas.82.13.4443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zaug A. J., Cech T. R. Oligomerization of intervening sequence RNA molecules in the absence of proteins. Science. 1985 Sep 13;229(4718):1060–1064. doi: 10.1126/science.2412290. [DOI] [PubMed] [Google Scholar]
- Zaug A. J., Cech T. R. The intervening sequence RNA of Tetrahymena is an enzyme. Science. 1986 Jan 31;231(4737):470–475. doi: 10.1126/science.3941911. [DOI] [PubMed] [Google Scholar]
- van Roode J. H., Orgel L. E. Template-directed synthesis of oligoguanylates in the presence of metal ions. J Mol Biol. 1980 Dec 25;144(4):579–585. doi: 10.1016/0022-2836(80)90338-1. [DOI] [PubMed] [Google Scholar]
- van der Horst G., Tabak H. F. Self-splicing of yeast mitochondrial ribosomal and messenger RNA precursors. Cell. 1985 Apr;40(4):759–766. doi: 10.1016/0092-8674(85)90335-6. [DOI] [PubMed] [Google Scholar]