Abstract
The mitochondrial ribosomal protein L2 gene (rpl2) is coded by two exons of 840 and 669 bp separated by an intron sequence of 1481 bp in the rice mitochondrial genome. The rpl2 gene is located three nucleotides upstream of the ribosomal protein S19 gene (rps19) and both genes are co-transcribed. cDNA sequence analysis indentified splicing of the intron sequence from the rpl2 mRNA as well as RNA editing events. The deduced secondary structure of the rpl2 intron sequence shows the characteristic features of a group-II intron. A single RNA editing site is identified in rpl2 and six editing sites in rps19 transcripts. In addition, one editing site is observed in the 3 nucleotide intergenic region. Analysis of individual cDNA clones showed a different extent of RNA editing. The rice rpl2 intron is located at a different site and shows no significant nucleotide sequence similarity with the rpl2 intron of liverwort. However, 60% nucleotide sequence identity is observed between the rice rpl2 intron and the Oenothera nad5 intron in a 234 nucleotide region. The mitochondrial rpl2 sequence is absent from the pea mitochondrial genome and we consequently propose that the mitochondrial RPL2 protein is encoded by a nuclear gene in pea.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bland MM, Levings CS III, Matzinger DF: The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet 204: 8–16 (1986).
Bonen L: The mitochondrial S13 ribosomal protein gene is silent in wheat embryos and seedlings. Nucl Acids Res 15: 10393–10404 (1987).
Brennicke A, Grohmann L, Hiesel R, Knoop V, Schuster W: The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Lett 325: 140–145 (1993).
Conklin PL, Hanson MR: Ribosomal protein S19 is encoded by the mitochondrial genome in Petunia hybrida. Nucl Acids Res 19: 2701–2705 (1991).
Covello PS, Gray MW: Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 11: 3815–3820 (1992).
Gonzalez DH, Bonnard G, Grienenberger J-M: A gene involved in the biogenesis of cytochromes is co-transcribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 24: 248–255 (1993).
Gray MW: The endosymbiont hypothesis revisited: Int Rev Cytol 141: 233–357 (1992).
Gruska I, Jekabsons W, Schuster W: Oenothera mitochondrial orf454, a gene involved in cytochrome c biogenesis corres-ponds to orf169 and orf322 of Marchantia. Mol Gen Genet 247: 529–536 (1995).
Gualberto JM, Wintz H, Weil J-H, Grienenberger J-M: The genes coding for subunit 3 of NADH dehydrogenase and for ribosomal protein S12 are present in the wheat and maize mitochondrial genomes and are co-transcribed. Mol Gen Genet 215: 118–127 (1988).
Gualberto JM, Bonnard G, Lamattina L, Grienenberger JM: Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3: 1109–1120 (1991).
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun C-R, Meng B-Y, Li Y-Q, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M: The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194 (1989).
Hunt MD, Newton KJ: The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. EMBO J 10: 1045–1052 (1991).
Itadani H, Wakasugi T, Sugita M, Sugiura M, Nakazono M, Hirai A: Nucleotide sequence of a 28-kbp portion of rice mitochondrial DNA: the existence of many sequences that correspond to parts of mitochondrial genes in intergenic regions. Plant Cell Physiol 35: 1239–1244 (1994).
Iwahashi M, Nakazono M, Kanno A, Sugino K, Ishibashi T, Hirai A: Genetic and physical maps and a clone bank of mitochondrial DNA from rice. Theor Appl Genet 84: 275–279 (1992).
Kadowaki K, Suzuki T, Kazama S, Oh-fuchi T, Sakamoto W: Nucleotide sequence of the cytochrome oxidase subunit I gene from rice mitochondria. Nucl Acids Res 17: 7519 (1989).
Knoop V, Ehrhardt T, Lättig K, Brennicke A: The gene for ribosomal protein S10 is present in motochondria of pea and potato but absent from those of Arabidopsis and Oenothera. Curr Genet 27: 559–564 (1995).
Knoop V, Schuster W, Wissinger B, Brennicke A: Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J 10: 3483–3493 (1995).
Kumar R: Mitochondrial Ribosomes and their Proteins: The Molecular Biology of Plant Mitochondria. Advances in Cellular and Molecular Biology of Plants, vol. 3, pp. 131–183. Kluwer Academic Publishers, Dordrecht, Netherlands (1995).
Michel F, Umesono K, Ozeki H: Comparative and functional anatomy of group II catalytic introns: a review. Gene 82: 5–30 (1989).
Nakazono M, Hirai A: Identification of the entire set of transferred chloroplast DNA sequences in the mitochondrial genome of rice. Mol Gen Genet 236: 341–346 (1993).
Nugent JM, Palmer JD: Evolution of gene content and gene organization in flowering plant mitochondrial DNA: a general survey and further studies on coxII gene transfer to the nucleus. In: Brennicke A, Kück U (eds) Plant Mitochondria, pp. 163–170. VCH Publishers, Weinheim, Germany (1993).
Ohyama K, Oda K, Ohta E, Takemura M: Gene organization and evolution of introns of a liverwort, Marchantia polymorpha, mitochondrial genome. In: Brennicke A and Kück U (eds) Plant Mitochondria, pp. 15–129. VCH Press, Weinheim, Germany (1993).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Schuster W: Ribosomal protein gene rpl5 is cotranscribed with the nad3 gene in Oenothera mitochondria. Mol Gen Genet 240: 445–449 (1993).
Schuster W, Brennicke A: RNA editing makes mistakes in plant mitochondria: editing loses sense in transcripts of a rps19 pseudogene and in creating stop codons in coxl and rps3 mRNAs of Oenothera. Nucl Acids Res 19: 6923–6928 (1991).
Stern DB, Newton KJ: Isolation of plant mitochondrial RNA. Meth Enzymol 118: 488–496 (1986).
Sünkel S, Brennicke A, Knoop V: RNA editing of a conserved reading frame in plant mitochondria increases its similarity to two overlapping reading frames in Escherichia coli. Mol Gen Genet 242: 65–72 (1994).
Sutton CA, Conklin PL, Pruitt KD, Hanson MR: Editing of pre-mRNAs can occur before cis-and trans-splicing in Petunia mitochondria. Mol Cell Biol 11: 4274–4277 (1991).
Takemura M, Oda K, Yamato K, Ohta E, Nakamura Y, Nozato N, Akashi K, Ohyama K: Gene clusters for ribosomal proteins in the mitochondrial genome of a liverwort, Marchantia polymorpha. Nucl Acids Res 20: 3199–3205 (1992).
Umbeck PF, Gengenbach BG: Reversion of male-sterile T-cytoplasm maize to male fertility in tissue culture. Crop Sci 23: 584–588 (1983).
Vitart V, DePaepe R, Mathieu C, Chétrit P, Vedel F: Amplification of substoichiometric recombinant mitochondrial DNA sequences in a nuclear, male sterile mutant regenerated from protoplast culture in Nicotiana sylvestris. Mol Gen Genet 233: 193–200 (1992).
Wahleithner JA, Wolstenholme DR: Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucl Acids Res 16: 6897–6913 (1988).
Wolff G, Plante I, Lang BF, Kück U, Burger G: Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii gene content and genome organization. J Mol Biol 237: 75–86 (1994).
Yang AJ, Mulligan RM: RNA editing intermediates of cox2 transcripts in maize mitochondria. Mol Cell Biol 11: 4278–4281 (1991).
Zanlungo S, Quiñones V, Moenne A, Holuigue L, Jordana X: A ribosomal protein S10 gene is found in the mitochondrial genome in Solanum tuberosum. Plant Mol Biol 25: 743–749 (1994).
Zanlungo S, Quiñones V, Moenne A, Holuigue L, Jordana X: Splicing and editing of rps10 transcripts in potato mitochondria. Curr Genet 27: 565–571 (1995).
Zhuo D, Bonen L: Characterization of the S7 ribosomal protein gene in wheat mitochondria. Mol Gen Genet 236: 395–401 (1993).
Zurawski G, Zurawski SM: Structure of the Escherichia coli S10 ribosomal protein operon. Nucl Acids Res 13: 4521–4526 (1985).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kubo, N., Ozawa, K., Hino, T. et al. A ribosomal protein L2 gene is transcribed, spliced, and edited at one site in rice mitochondria. Plant Mol Biol 31, 853–862 (1996). https://doi.org/10.1007/BF00019472
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00019472