Abstract
The NADH dehydrogenase subunit A (ndhA) gene from maize chloroplasts encodes a highly conserved peptide, which at several positions could be restored to consensus sequences by potential C-to-U editing of the codons involved. This gene was, therefore, chosen for analysis of its mRNA sequence in the form of amplified cDNA. A comparison of this cDNA sequence with the plastome-encoded ndhA sequence reveals four C-to-U editing sites, thereby demonstrating as a novel finding that chloroplast editing can also affect internal mRNA positions. All the edited codons restore amino acids that are conserved in the ndhA-encoded peptides of other chloroplast species. Alignment with homologous mitochondrial NADH-ubiquinone reductase subunit 1 (nad1) sequences of plant and even nonplant species shows that two of the editing positions restore universally conserved amino acids and that one editing site is even shared with nad1 mRNA of plant mitochondria. No editing sites could be detected in the cDNA derived from transcripts of the maize chloroplast RNA polymerase alpha-subunit (rpoA) gene.
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- Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Benne R. RNA editing in trypanosomes: is there a message? Trends Genet. 1990 Jun;6(6):177–181. doi: 10.1016/0168-9525(90)90173-4. [DOI] [PubMed] [Google Scholar]
- Blum B., Sturm N. R., Simpson A. M., Simpson L. Chimeric gRNA-mRNA molecules with oligo(U) tails covalently linked at sites of RNA editing suggest that U addition occurs by transesterification. Cell. 1991 May 17;65(4):543–550. doi: 10.1016/0092-8674(91)90087-f. [DOI] [PubMed] [Google Scholar]
- Chapdelaine Y., Bonen L. The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell. 1991 May 3;65(3):465–472. doi: 10.1016/0092-8674(91)90464-a. [DOI] [PubMed] [Google Scholar]
- Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
- Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
- Conklin P. L., Wilson R. K., Hanson M. R. Multiple trans-splicing events are required to produce a mature nad1 transcript in a plant mitochondrion. Genes Dev. 1991 Aug;5(8):1407–1415. doi: 10.1101/gad.5.8.1407. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Hiratsuka J., Shimada H., Whittier R., Ishibashi T., Sakamoto M., Mori M., Kondo C., Honji Y., Sun C. R., Meng B. Y. 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. 1989 Jun;217(2-3):185–194. doi: 10.1007/BF02464880. [DOI] [PubMed] [Google Scholar]
- Hoch B., Maier R. M., Appel K., Igloi G. L., Kössel H. Editing of a chloroplast mRNA by creation of an initiation codon. Nature. 1991 Sep 12;353(6340):178–180. doi: 10.1038/353178a0. [DOI] [PubMed] [Google Scholar]
- Kudla J., Igloi G. L., Metzlaff M., Hagemann R., Kössel H. 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. 1992 Mar;11(3):1099–1103. doi: 10.1002/j.1460-2075.1992.tb05149.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin C. H., Wu M. A ferredoxin-type iron-sulfur protein gene, frx B, is expressed in the chloroplasts of tobacco and spinach. Plant Mol Biol. 1990 Sep;15(3):449–455. doi: 10.1007/BF00019161. [DOI] [PubMed] [Google Scholar]
- 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]
- Maier R. M., Döry I., Igloi G., Kössel H. The ndhH genes of gramminean plastomes are linked with the junctions between small single copy and inverted repeat regions. Curr Genet. 1990 Oct;18(3):245–250. doi: 10.1007/BF00318388. [DOI] [PubMed] [Google Scholar]
- Matsubayashi T., Wakasugi T., Shinozaki K., Yamaguchi-Shinozaki K., Zaita N., Hidaka T., Meng B. Y., Ohto C., Tanaka M., Kato A. Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol Gen Genet. 1987 Dec;210(3):385–393. doi: 10.1007/BF00327187. [DOI] [PubMed] [Google Scholar]
- Pruitt K. D., Hanson M. R. Splicing of the Petunia cytochrome oxidase subunit II intron. Curr Genet. 1991 Mar;19(3):191–197. doi: 10.1007/BF00336486. [DOI] [PubMed] [Google Scholar]
- Scherer S. Do photosynthetic and respiratory electron transport chains share redox proteins? Trends Biochem Sci. 1990 Dec;15(12):458–462. doi: 10.1016/0968-0004(90)90296-n. [DOI] [PubMed] [Google Scholar]
- Schuster W., Ternes R., Knoop V., Hiesel R., Wissinger B., Brennicke A. Distribution of RNA editing sites in Oenothera mitochondrial mRNAs and rRNAs. Curr Genet. 1991 Nov;20(5):397–404. doi: 10.1007/BF00317068. [DOI] [PubMed] [Google Scholar]
- Stern D. B., Palmer J. D. Tripartite mitochondrial genome of spinach: physical structure, mitochondrial gene mapping, and locations of transposed chloroplast DNA sequences. Nucleic Acids Res. 1986 Jul 25;14(14):5651–5666. doi: 10.1093/nar/14.14.5651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stuart K. RNA editing in trypanosomatid mitochondria. Annu Rev Microbiol. 1991;45:327–344. doi: 10.1146/annurev.mi.45.100191.001551. [DOI] [PubMed] [Google Scholar]
- Weissmann C., Cattaneo R., Billeter M. A. RNA editing. Sometimes an editor makes sense. Nature. 1990 Feb 22;343(6260):697–699. doi: 10.1038/343697a0. [DOI] [PubMed] [Google Scholar]
- Wissinger B., Schuster W., Brennicke A. Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group II intron sequences. Cell. 1991 May 3;65(3):473–482. doi: 10.1016/0092-8674(91)90465-b. [DOI] [PubMed] [Google Scholar]