Acta Physiologiae Plantarum

, Volume 30, Issue 5, pp 657–662 | Cite as

Mitochondrial RNA editing of F0-ATPase subunit 9 gene (atp9) transcripts of Yunnan purple rice cytoplasmic male sterile line and its maintainer line

  • Lei Wei
  • Zhi-Xiang Yan
  • Yi DingEmail author
Original Paper


On the base of construction of a new type of cytoplasmic male sterile (CMS) line ZidaoA, we analyzed the editing of transcripts of mitochondrial ATP synthase subunit 9 gene (atp9) from CMS line and its maintainer line. With PCR, RT-PCR, and direct sequencing, complete nucleotide sequences were determined for the mitochondrial atp9 gene and its cDNA from two lines of purple rice type rice: CMS line Ying xiang A and its maintainer line Ying xiang B. The atp9 transcript of Ying xiang A was shown to have no editing sites and the transcript of Ying xiang B was shown to have two editing sites with changes affecting the amino acid sequence of the protein product. The editing of the atp9 transcript from Ying xiang B was found to change an arginine codon into a termination codon, shortening the protein of Ying xiang B to the “standard” size. And the Ying xiang A transcript, which has no termination codon, cannot be translated to a normal protein. The results demonstrate the important role of RNA editing in the production of the functional ATP9 subunit and suggest that RNA editing could be likely associated with cytoplasmic male sterility.


atp9 Cytoplasmic male sterile (CMS) RNA editing Ying xiang A Ying xiang B 



Basic local alignment search tool


Cytoplasmic male sterile



We thank Dr. Josephine Richardson for her critical reading of the manuscript. We gratefully acknowledge Dr. Sun Qingping (Wuhan University) for his kind help with reverse transcription. This study was supported in part by the National Science Foundation of China (No. 30571143).


  1. Araya A, Domec C, Bégu D, Litvak S (1992) An in vitro system for the editing of ATP synthase subunit 9 mRNA using wheat mitochondrial extracts. Proc Natl Acad Sci USA 89:1040–1044PubMedCrossRefGoogle Scholar
  2. Bégu D, Graves PV, Domec C, Arselin G, Litvak S, Araya A (1990) RNA editing of wheat mitochondrial ATP synthase subunit 9: direct protein and cDNA sequencing. Plant Cell 2:1283–1290PubMedCrossRefGoogle Scholar
  3. Chapdelaine Y, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a f/ww-splicing model for this gene-in-pieces. Cell 65:465–472PubMedCrossRefGoogle Scholar
  4. Dewey RE, Levings CS III, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male sterile cytoplasm. Cell 44:439–449PubMedCrossRefGoogle Scholar
  5. Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25:461–486PubMedCrossRefGoogle Scholar
  6. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169PubMedCrossRefGoogle Scholar
  7. Hernould M, Suharsono S, Litvak S, Araya A, Mouras A (1993) Male sterility induction in transgenic tobacco plants with an unedited ATP9 mitochondrial gene from wheat. Proc Natl Acad Sci USA 90:2370–2374PubMedCrossRefGoogle Scholar
  8. Hernould M, Suharsono S, Zabaleta E, Carde JP, Litvak S, Araya A, Mouras A (1998) Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Mol Biol 36:499–508PubMedCrossRefGoogle Scholar
  9. Hu Y, Wei L, Liu S, Yu J, Ding Y (2005a) Analysis of male sterility-related protein of young panicle in rice (Oryza sativa L.) by two-dimensional electrophoresis. Wuhan Univ J Nat Sci 10(3):597–601CrossRefGoogle Scholar
  10. Hu Y, Wu Q, Liu S, Wei L, Chen X, Yan Z, Yu J, Zeng L, Ding Y (2005b) Study of rice pollen grains by multispectral imaging microscopy. Microsc Res Techn 68(6):335–346CrossRefGoogle Scholar
  11. Ishikawa M, Kadowaki KI (1993) Excess RNA editing in Rice mitochondrial atp9 transcripts. Plant Cell Physiol 34(6):959–963Google Scholar
  12. Kaleikau EK, Andre CP, Walbot V (1990) Sequence of the F0-ATPase proteolipid (atp9) gene from rice mitochondria. Nucleic Acids Res 18:370PubMedCrossRefGoogle Scholar
  13. Kaleikau EK, Andre CP, Walbot V (1993) Transcription of the gene coding for subunit 9 of ATP synthase in rice mitochondria. Plant Mol Biol 22:899–905PubMedCrossRefGoogle Scholar
  14. Kim DS, Cho DS, Park WM, Na HJ, Nam HG (2006) Proteomic pattern-based analyses of light responses in Arabidopsis thaliana wild-type and photoreceptor mutants. Proteomics 6:3040–3049PubMedCrossRefGoogle Scholar
  15. Larbi JG, Stephanie KB, Christine DC (2002) Mitochondrial RNA editing truncates a chimeric open reading frame associated with S male-sterility in maize. Curr Genet 42:179–184CrossRefGoogle Scholar
  16. Levings CS III (1990) The Texas cytoplasm of maize: cytoplasmic male sterility and disease susceptibility. Science 250:942–947PubMedCrossRefGoogle Scholar
  17. Mignouna H, Vermin SS, Briquet M (1987) Mitochondrial DNA modification associated with cytoplasmic male sterility in rice. Theor Appl Genet 74:666–669CrossRefGoogle Scholar
  18. Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268(4):434–445PubMedCrossRefGoogle Scholar
  19. Plomion C, Lalanne C, Claverol S, Meddour H, Kohler A, Bogeat-Triboulot MB, Barre A, Provost G, Dumazet H, Jacob D, Bastien C, Dreyer E, Daruvar A, Guehl JM, Schmitter JM, Martin F, Bonneu M (2006) Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. Proteomics 6:6509–6527PubMedCrossRefGoogle Scholar
  20. Rakwal R, Agrawal GK (2003) Rice proteomics: current status and future perspectives. Electrophoresis 24:3378–3389PubMedCrossRefGoogle Scholar
  21. Salazar RA, Pring DR, Kempken F (1991) Editing of mitochondrial atp9 transcripts from two sorghum lines. Curr Genet 20:483–486PubMedCrossRefGoogle Scholar
  22. Schuster W, Brennicke A (1991) RNA editing in ATPase subunit 6 mRNAs in Oenothera mitochondria. FEBS Lett 295:97–101PubMedCrossRefGoogle Scholar
  23. Tanaka N, Mitsui S, Nobori H, Yanagi K, Komatsu S (2005) Expression and function of proteins during development of the basal region in rice seedlings. Mol Cell Proteomics 4:796–808PubMedCrossRefGoogle Scholar
  24. Tian X, Zheng J, Hu S, Yu J (2006) The rice mitochondrial genomes and their variations. Plant Physiol 142(2):401–410CrossRefGoogle Scholar
  25. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu Y (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687PubMedCrossRefGoogle Scholar
  26. Wei L, Ding Y, Liu Y, Yu J (2002a) Microcalorimetric analysis of anthers of male sterile rice sterile line. J Wuhan Bot Res 20(4):308–310Google Scholar
  27. Wei L, Ding Y, Hu Y, Yu J (2002b) Analysis of leaf proteins of Zidao male sterile line by 2D-PAGE. Acta Genet Sin 29(8):696–699PubMedGoogle Scholar
  28. Willson TA, Nagley P (1987) Amino acids substitution in subunit 9 of the mitochondrial ATPase complex of Saccharomyces cerevisiae. Sequence analysis of a series of revertants of an olil mit-mutant carrying an amino acid substitution in the hydrophilic loop of subunit 9. Eur J Biochem 167(2):291–297PubMedCrossRefGoogle Scholar
  29. Wintz H, Hanson MR (1991) A termination codon is created by RNA editing in the petunia mitochondrial atp9 gene transcript. Curr Genet 19:61–64PubMedCrossRefGoogle Scholar
  30. Zabaleta E, Mouras A, Hernould M, Suharsono S, Araya A (1996) Transgenic male-sterile plant induced by an unedited atp9 gene is restored to fertility by inhibiting its expression with antisense RNA. Proc Natl Acad Sci USA 93:11259–11263PubMedCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2008

Authors and Affiliations

  1. 1.Key Laboratory of MOE for Plant Developmental Biology, College of Life SciencesWuhan UniversityWuhanPeople’s Republic of China

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