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. 1997 Jun 2;16(11):3282–3288. doi: 10.1093/emboj/16.11.3282

Extraplastidic site-specific factors mediate RNA editing in chloroplasts.

R Bock 1, H U Koop 1
PMCID: PMC1169944  PMID: 9214643

Abstract

Single nucleotides in higher plant organellar mRNAs are subject to post-transcriptional alterations by RNA editing, typically resulting in changes of the encoded protein sequence. Although some information has been acquired on the general features of the editing processes in both plastids and plant mitochondria, the mechanisms and factors involved in the selective recognition of the nucleotide to be edited are still unknown. To gain a better understanding of how an editing site is specifically selected by the organellar RNA editing machinery, we have attempted to rescue a previously generated tobacco plastid editing mutant. Using an interspecific protoplast fusion approach, we were able to restore RNA editing activity for a specific site in the psbF transcript that otherwise remained unedited. Our results suggest (i) that site-specific trans-acting factors mediate chloroplast editing site recognition and (ii) that these factors are of extraplastidic origin.

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Selected References

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  1. Akagi H., Shimada H., Fujimura T. High-frequency inter-parental recombination between mitochondrial genomes of rice cybrids. Curr Genet. 1995 Dec;29(1):58–65. doi: 10.1007/BF00313194. [DOI] [PubMed] [Google Scholar]
  2. Araya A., Domec C., Begu D., Litvak S. An in vitro system for the editing of ATP synthase subunit 9 mRNA using wheat mitochondrial extracts. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1040–1044. doi: 10.1073/pnas.89.3.1040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bachmann B., Lüke W., Hunsmann G. Improvement of PCR amplified DNA sequencing with the aid of detergents. Nucleic Acids Res. 1990 Mar 11;18(5):1309–1309. doi: 10.1093/nar/18.5.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benne R. RNA editing: how a message is changed. Curr Opin Genet Dev. 1996 Apr;6(2):221–231. doi: 10.1016/s0959-437x(96)80054-2. [DOI] [PubMed] [Google Scholar]
  5. Benne R., Van den Burg J., Brakenhoff J. P., Sloof P., Van Boom J. H., Tromp M. C. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 1986 Sep 12;46(6):819–826. doi: 10.1016/0092-8674(86)90063-2. [DOI] [PubMed] [Google Scholar]
  6. Birky C. W., Jr Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11331–11338. doi: 10.1073/pnas.92.25.11331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bock R., Hagemann R., Kössel H., Kudla J. Tissue- and stage-specific modulation of RNA editing of the psbF and psbL transcript from spinach plastids--a new regulatory mechanism? Mol Gen Genet. 1993 Aug;240(2):238–244. doi: 10.1007/BF00277062. [DOI] [PubMed] [Google Scholar]
  8. Bock R., Hermann M., Kössel H. In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J. 1996 Sep 16;15(18):5052–5059. [PMC free article] [PubMed] [Google Scholar]
  9. Bock R., Kössel H., Maliga P. Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. EMBO J. 1994 Oct 3;13(19):4623–4628. doi: 10.1002/j.1460-2075.1994.tb06784.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bock R., Maliga P. In vivo testing of a tobacco plastid DNA segment for guide RNA function in psbL editing. Mol Gen Genet. 1995 May 20;247(4):439–443. doi: 10.1007/BF00293145. [DOI] [PubMed] [Google Scholar]
  11. Carrillo N., Seyer P., Tyagi A., Herrmann R. G. Cytochrome b-559 genes from Oenothera hookeri and Nicotiana tabacum show a remarkably high degree of conservation as compared to spinach. The enigma of cytochrome b-559: highly conserved genes and proteins but no known function. Curr Genet. 1986;10(8):619–624. doi: 10.1007/BF00418129. [DOI] [PubMed] [Google Scholar]
  12. Chaudhuri S., Carrer H., Maliga P. Site-specific factor involved in the editing of the psbL mRNA in tobacco plastids. EMBO J. 1995 Jun 15;14(12):2951–2957. doi: 10.1002/j.1460-2075.1995.tb07295.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chaudhuri S., Maliga P. Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. EMBO J. 1996 Nov 1;15(21):5958–5964. [PMC free article] [PubMed] [Google Scholar]
  14. Chen K., Wildman S. G., Smith H. H. Chloroplast DNA distribution in parasexual hybrids as shown by polypeptide composition of fraction I protein. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5109–5112. doi: 10.1073/pnas.74.11.5109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chiu W. L., Sears B. B. Recombination between chloroplast DNAs does not occur in sexual crosses of Oenothera. Mol Gen Genet. 1985;198(3):525–528. doi: 10.1007/BF00332951. [DOI] [PubMed] [Google Scholar]
  16. Covello P. S., Gray M. W. RNA editing in plant mitochondria. Nature. 1989 Oct 19;341(6243):662–666. doi: 10.1038/341662a0. [DOI] [PubMed] [Google Scholar]
  17. Eigel L., Oelmüller R., Koop H. U. Transfer of defined numbers of chloroplasts into albino protoplasts using an improved subprotoplast/protoplast microfusion procedure: transfer of only two chloroplasts leads to variegated progeny. Mol Gen Genet. 1991 Jul;227(3):446–451. doi: 10.1007/BF00273936. [DOI] [PubMed] [Google Scholar]
  18. Gualberto J. M., Weil J. H., Grienenberger J. M. Editing of the wheat coxIII transcript: evidence for twelve C to U and one U to C conversions and for sequence similarities around editing sites. Nucleic Acids Res. 1990 Jul 11;18(13):3771–3776. doi: 10.1093/nar/18.13.3771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Haley J., Bogorad L. Alternative promoters are used for genes within maize chloroplast polycistronic transcription units. Plant Cell. 1990 Apr;2(4):323–333. doi: 10.1105/tpc.2.4.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hiesel R., Wissinger B., Schuster W., Brennicke A. RNA editing in plant mitochondria. Science. 1989 Dec 22;246(4937):1632–1634. doi: 10.1126/science.2480644. [DOI] [PubMed] [Google Scholar]
  21. Koop H. U., Steinmüller K., Wagner H., Rössler C., Eibl C., Sacher L. Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta. 1996;199(2):193–201. doi: 10.1007/BF00196559. [DOI] [PubMed] [Google Scholar]
  22. Maier R. M., Neckermann K., Igloi G. L., Kössel H. Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol. 1995 Sep 1;251(5):614–628. doi: 10.1006/jmbi.1995.0460. [DOI] [PubMed] [Google Scholar]
  23. Maier R. M., Zeltz P., Kössel H., Bonnard G., Gualberto J. M., Grienenberger J. M. RNA editing in plant mitochondria and chloroplasts. Plant Mol Biol. 1996 Oct;32(1-2):343–365. doi: 10.1007/BF00039390. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Svab Z., Hajdukiewicz P., Maliga P. Stable transformation of plastids in higher plants. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8526–8530. doi: 10.1073/pnas.87.21.8526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yu W., Schuster W. Evidence for a site-specific cytidine deamination reaction involved in C to U RNA editing of plant mitochondria. J Biol Chem. 1995 Aug 4;270(31):18227–18233. doi: 10.1074/jbc.270.31.18227. [DOI] [PubMed] [Google Scholar]

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