Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera: is genetic information transferred between organelles via RNA? (original) (raw)

Abstract

We describe an open reading frame (ORF) with high homology to reverse transcriptase in the mitochondrial genome of Oenothera. This ORF displays all the characteristics of an active plant mitochondrial gene with a possible ribosome binding site and 39% T in the third codon position. It is located between a sequence fragment from the plastid genome and one of nuclear origin downstream from the gene encoding subunit 5 of the NADH dehydrogenase. The nuclear derived sequence consists of 528 nucleotides from the small ribosomal RNA and contains an expansion segment unique to nuclear rRNAs. The plastid sequence contains part of the ribosomal protein S4 and the complete tRNA(Ser). The observation that only transcribed sequences have been found i more than one subcellular compartment in higher plants suggests that interorganellar transfer of genetic information may occur via RNA and subsequent local reverse transcription and genomic integration.

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Selected References

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  1. Bertrand H., Chan B. S., Griffiths A. J. Insertion of a foreign nucleotide sequence into mitochondrial DNA causes senescence in Neurospora intermedia. Cell. 1985 Jul;41(3):877–884. doi: 10.1016/s0092-8674(85)80068-4. [DOI] [PubMed] [Google Scholar]
  2. Bibb M. J., Van Etten R. A., Wright C. T., Walberg M. W., Clayton D. A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981 Oct;26(2 Pt 2):167–180. doi: 10.1016/0092-8674(81)90300-7. [DOI] [PubMed] [Google Scholar]
  3. Brennicke A. Mitochondrial DNA from Oenothera berteriana: PURIFICATION AND PROPERTIES. Plant Physiol. 1980 Jun;65(6):1207–1210. doi: 10.1104/pp.65.6.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chang D. D., Clayton D. A. A mammalian mitochondrial RNA processing activity contains nucleus-encoded RNA. Science. 1987 Mar 6;235(4793):1178–1184. doi: 10.1126/science.2434997. [DOI] [PubMed] [Google Scholar]
  5. Chomyn A., Mariottini P., Cleeter M. W., Ragan C. I., Matsuno-Yagi A., Hatefi Y., Doolittle R. F., Attardi G. Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature. 1985 Apr 18;314(6012):592–597. doi: 10.1038/314592a0. [DOI] [PubMed] [Google Scholar]
  6. Clayton D. A. Transcription of the mammalian mitochondrial genome. Annu Rev Biochem. 1984;53:573–594. doi: 10.1146/annurev.bi.53.070184.003041. [DOI] [PubMed] [Google Scholar]
  7. Dawson A. J., Jones V. P., Leaver C. J. The apocytochrome b gene in maize mitochondria does not contain introns and is preceded by a potential ribosome binding site. EMBO J. 1984 Sep;3(9):2107–2113. doi: 10.1002/j.1460-2075.1984.tb02098.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fox T. D., Leaver C. J. The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell. 1981 Nov;26(3 Pt 1):315–323. doi: 10.1016/0092-8674(81)90200-2. [DOI] [PubMed] [Google Scholar]
  9. Gardner R. C., Howarth A. J., Hahn P., Brown-Luedi M., Shepherd R. J., Messing J. The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by M13mp7 shotgun sequencing. Nucleic Acids Res. 1981 Jun 25;9(12):2871–2888. doi: 10.1093/nar/9.12.2871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gray M. W., Doolittle W. F. Has the endosymbiont hypothesis been proven? Microbiol Rev. 1982 Mar;46(1):1–42. doi: 10.1128/mr.46.1.1-42.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hiesel R., Schobel W., Schuster W., Brennicke A. The cytochrome oxidase subunit I and subunit III genes in Oenothera mitochondria are transcribed from identical promoter sequences. EMBO J. 1987 Jan;6(1):29–34. doi: 10.1002/j.1460-2075.1987.tb04714.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Isaac P. G., Brennicke A., Dunbar S. M., Leaver C. J. The mitochondrial genome of fertile maize (Zea mays L.) contains two copies of the gene encoding the alpha-subunit of the F1-ATPase. Curr Genet. 1985;10(4):321–328. doi: 10.1007/BF00365628. [DOI] [PubMed] [Google Scholar]
  13. Lang B. F., Burger G. A collection of programs for nucleic acid and protein analysis, written in FORTRAN 77 for IBM-PC compatible microcomputers. Nucleic Acids Res. 1986 Jan 10;14(1):455–465. doi: 10.1093/nar/14.1.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Leaver C. J., Harmey M. A. Higher-plant mitochondrial ribosomes contain a 5S ribosomal ribonucleic acid component. Biochem J. 1976 Jul 1;157(1):275–277. doi: 10.1042/bj1570275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lonsdale D. M., Hodge T. P., Howe C. J., Stern D. B. Maize mitochondrial DNA contains a sequence homologous to the ribulose-1,5-bisphosphate carboxylase large subunit gene of chloroplast DNA. Cell. 1983 Oct;34(3):1007–1014. doi: 10.1016/0092-8674(83)90558-5. [DOI] [PubMed] [Google Scholar]
  16. Mahler H. R., Raff R. A. The evolutionary origin of the mitochondrion: a nonsymbiotic model. Int Rev Cytol. 1975;43:1–124. doi: 10.1016/s0074-7696(08)60067-4. [DOI] [PubMed] [Google Scholar]
  17. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  18. Michel F., Lang B. F. Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature. 1985 Aug 15;316(6029):641–643. doi: 10.1038/316641a0. [DOI] [PubMed] [Google Scholar]
  19. Russell D., Bogorad L. Transcription analysis of the maize chloroplast gene for the ribosomal protein S4. Nucleic Acids Res. 1987 Feb 25;15(4):1853–1867. doi: 10.1093/nar/15.4.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Saigo K., Kugimiya W., Matsuo Y., Inouye S., Yoshioka K., Yuki S. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature. 1984 Dec 13;312(5995):659–661. doi: 10.1038/312659a0. [DOI] [PubMed] [Google Scholar]
  21. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  22. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  23. Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986 Sep;5(9):2043–2049. doi: 10.1002/j.1460-2075.1986.tb04464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stern D. B., Lonsdale D. M. Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature. 1982 Oct 21;299(5885):698–702. doi: 10.1038/299698a0. [DOI] [PubMed] [Google Scholar]
  25. Strittmatter G., Kössel H. Cotranscription and processing of 23S, 4.5S and 5S rRNA in chloroplasts from Zea mays. Nucleic Acids Res. 1984 Oct 25;12(20):7633–7647. doi: 10.1093/nar/12.20.7633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Subramanian A. R., Steinmetz A., Bogorad L. Maize chloroplast DNA encodes a protein sequence homologous to the bacterial ribosome assembly protein S4. Nucleic Acids Res. 1983 Aug 11;11(15):5277–5286. doi: 10.1093/nar/11.15.5277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wong T. W., Clayton D. A. DNA primase of human mitochondria is associated with structural RNA that is essential for enzymatic activity. Cell. 1986 Jun 20;45(6):817–825. doi: 10.1016/0092-8674(86)90556-8. [DOI] [PubMed] [Google Scholar]