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Splicing and editing of rps10 transcripts in potato mitochondria

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Abstract

The structure and expression of the potato mitochondrial gene rps10, encoding ribosomal protein S10, has been characterized. The RPS10 polypeptide of 129 amino acids is encoded by two exons of 307 bp and 80 bp respectively, which are separated by a 774-bp class-II intron. Editing of the complete rps10 coding region was studied by sequence analysis of spliced cDNAs. Four C residues are edited into U, resulting in the creation of a putative translational initiation codon, a new stop codon which eliminated ten carboxy-terminal residues, and two additional amino-acid alterations. All these changes increase the similarity between the potato and liverwort polypeptides. One additional C-to-U RNA editing event, observed in the intron sequence of unspliced cDNAs, improves the stability of the secondary structure in stem I (i) of domain I and may thus be required for the splicing reaction. All spliced cDNAs, and most unspliced cDNAs, were completely edited, suggesting that editing is an early step of rps10 mRNA processing and precedes splicing. Earlier work on potato rps10 (Zanlungo et al. 1994) is now known to comprise only a partial analysis of the gene, since the short downstream exon was not identified.

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References

  • Binder S, Marchfelder A, Brennicke A, Wissinger B (1992) RNA editing in trans-splicing intron sequences of nad2 mRNAs in Oenothera mitochondria. J Biol Chem 267:7615–7623

    Google Scholar 

  • Bonen L (1991) The mitochondrial genome: so simple yet so complex. Curr Opin Genet Dev 1:515–522

    Google Scholar 

  • Chapdelaine Y, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell 65:465–472

    Google Scholar 

  • Covello PS, Gray MW (1992) Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 11: 3815–3820

    Google Scholar 

  • Dell'Orto P, Moenne A, Graves PV, Jordana X (1993) The potato mitochondrial ATP synthase subunit 9: gene structure, RNA editing and partial protein sequence. Plant Sci 88:45–53

    Google Scholar 

  • Freyer R, Hoch B, Neckermann K, Maier RM, Kössel H (1993) RNA editing in maize chloroplasts is a processing step independent of splicing and cleavage to monocistronic mRNAs. Plant J 4:621–629

    Google Scholar 

  • González DH, Bonnard G, Grienenberger J-M (1993) A gene involved in the biogenesis of cytochromes is co-transcribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 24: 248–255

    Google Scholar 

  • Gray M, Hanic-Joyce PJ, Covello PS (1992) Transcription, processing and editing in plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol 43:145–175

    Google Scholar 

  • Grohmann L, Brennicke A, Schuster W (1992) The mitochondrial gene encoding ribosomal protein S12 has been translocated to the nuclear genome in Oenothera. Nucleic Acids Res 20:5641–5646

    Google Scholar 

  • Grohmann L, Brennicke A, Schuster W (1993) Genes for mitochondrial ribosomal proteins in plants. In: Nierhaus KH, Franceschi F, Subramanian AR, Erdmann VA, Wittmann-Liebold B (eds) The translational apparatus, structure, function, regulation, evolution. Plenum Press, New York London, p 599–607

    Google Scholar 

  • Gualberto JM, Bonnard G, Lamattina L, Grienenberger J-M (1991) Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3:1109–1120

    Google Scholar 

  • Hardy C, Clark-Walker GD (1991) Nucleotide sequence of the cox1 gene in Kluyveromyces lactis mitochondrial DNA: evidence for recent horizontal transfer of a group-II intron. Curr Genet 20: 99–114

    Google Scholar 

  • Hoch B, Maier RM, Appel K, Igloi GL, Kössel H (1991) Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353:178–180

    Google Scholar 

  • Hunt MD, Newton KJ (1991) The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. EMBO J 10:1045–1052

    Google Scholar 

  • Kemmerer EC, Kao T-H, Deng G-R, Wu R (1989) Isolation and nucleotide sequence of the pea cytochrome oxidase subunit I gene. Plant Mol Biol 13:121–124

    Google Scholar 

  • Knoop V, Schuster W, Wissinger B, Brennicke A (1991) Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J 10:3483–3493

    Google Scholar 

  • Knoop V, Ehrhardt T, Lättig K, Brennicke A (1995) The gene for ribosomal protein S10 is present in mitochondria of pea and potato but absent from those of Arabidopsis and Oenothera. Curr Genet 27:559–564

    Google Scholar 

  • Kudla J, Igloi GL, Metzlaff M, Hagemann R, Kössel H (1992) RNA editing in tobacco chloroplasts leads to the formation of a translatable psbL mRNA by a C to U substitution within the initiation codon. EMBO J 11:1099–1103

    Google Scholar 

  • Levings CS, Brown GG (1989) Molecular biology of plant mitochondria. Cell 56:171–179

    Google Scholar 

  • Lippok B, Brennicke A, Wissinger B (1994) Differential RNA editing in closely related introns in Oenothera mitochondria. Mol Gen Genet 243:39–46

    Google Scholar 

  • Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group-II catalytic introns — a review. Gene 82:5–30

    Google Scholar 

  • Nugent JM, Palmer JD (1991) RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering-plant evolution. Cell 66:473–481

    Google Scholar 

  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. J Mol Biol 223:1–7

    Google Scholar 

  • Ohta E, Oda K, Yamato K, Nakamura M, Takemura M, Nozato N, Akashi K, Ohyama K, Michel F (1993) Group-I introns in the liverwort mitochondrial genome: the gene coding for subunit I of cytochrome oxidase shares five intron positions with its fungal counterparts. Nucleic Acids Res 21:1297–1305

    Google Scholar 

  • Ruf S, Zeltz P, Kössel H (1994) Complete RNA editing of unspliced and dicistronic transcripts of the intron-containing reading frame IRF170 from maize chloroplasts. Proc Natl Acad Sci USA 91:2295–2299

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Sutton CA, Conklin PL, Pruitt KD, Hanson MR (1991) Editing of pre-mRNAs can occur before cis- and trans-splicing in Petunia mitochondrial. Mol Cell Biol 11:4274–4277

    Google Scholar 

  • Takemura M, Oda K, Yamato K, Ohta E, Nakamura Y, Nozato N, Akashi K, Ohyama K (1992) Gene clusters for ribosomal proteins in the mitochondrial genome of a liverwort, Marchantia polymorpha. Nucleic Acids Res 20:3199–3205

    Google Scholar 

  • Wissinger B, Schuster W, Brennicke A (1991) Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon- and trans-splicing group-II intron-sequences. Cell 65:473–482

    Google Scholar 

  • Yang AJ, Mulligan RM (1991) RNA editing intermediates of cox2 transcripts in maize mitochondria. Mol Cell Biol 11:4278–4281

    Google Scholar 

  • Zanlungo S, Bégu D, Quiñones V, Araya A, Jordana X (1993) RNA editing of apocytochrome b (cob) transcripts in mitochondria from two genera of plants. Curr Genet 24:344–348

    Google Scholar 

  • Zanlungo S, Quiñones V, Moenne A, Holuigue L, Jordana X (1994) A ribosomal protein S10 gene is found in the mitochondrial genome in Solanum tuberosum. Plant Mol Biol 25:743–749

    Google Scholar 

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Zanlungo, S., Quiñones, V., Moenne, A. et al. Splicing and editing of rps10 transcripts in potato mitochondria. Curr Genet 27, 565–571 (1995). https://doi.org/10.1007/BF00314449

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  • DOI: https://doi.org/10.1007/BF00314449

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