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Mitochondrial Diseases pp 327–341Cite as

Plant Cytoplasmic Male Sterility: A Mitochondrial Pathology and Its Biotechnological Application

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Abstract

While the molecular origin of mitochondrial human pathologies started to be known in some detail at the end of the 1980s, plant mitochondrial mutations were known several decades before (Rogers and Edwardson 1952). In this review we describe the molecular origin of a mitochondrial mutation observed in plants leading to the emergence of cytoplasmic male sterility (CMS). We will focus the general description on maize and petunia. CMS can be defined as a phenotype produced by the incompatibility between nuclear and mitochondrial genomes of a given plant. The CMS phenotype may be relied to have high gene recombination, which plays an important role in modeling the plant mitochondrial genome. Mitochondrial gene recombination may lead to the formation of chimeric genes. Chimeric proteins having an altered mitochondrial function, may lead to the emergence of the CMS phenotype. The male sterility trait is used to obtain hybrids seeds carrying favourable agronomic traits.

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References

  • 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 extract. Proc Natl Acad Sci USA 89:1040–1044

    Article  PubMed  CAS  Google Scholar 

  • Araya A, Bégu D, Graves PV, Hernould M, Litvak S, Mouras A, Suharsono S (1993) Of RNA editing and cytoplasmic male sterility in plants. In: Brennicke A, Kück U (eds) Plant mitochondria. VCH Chemie, Weinheim, pp 83–91

    Google Scholar 

  • Araya A, Bégu D, Litvak S (1994) RNA editing in plants. Physiol Plant 91:543–550

    Article  CAS  Google Scholar 

  • Bégu D, Graves PV, Domec C, Arselin G, Litvak S, Araya A (1990) RNA editing of wheat mitochondrial ATPase subunit 9: direct protein and cDNA sequencing. Plant Cell 2:1238–1290

    Article  Google Scholar 

  • Belliard G, Pelletier G, Vedel F, Quetier F (1978) Morphological characteristics and chloroplast DNA distribution in different cytoplasmic parasexual hybrids of Nicotiana tabacum. Mol Gen Genet 165:231–237

    Article  CAS  Google Scholar 

  • Belliard G, Vedel F, Pelletier G (1979) Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature 28:401–403

    Article  Google Scholar 

  • Blanc V, Litvak S, Araya A (1995) RNA editing in wheat mitochondria proceeds by a deamination mechanism. FEBS Lett 373:56–60

    Article  PubMed  CAS  Google Scholar 

  • Carignani G, Groudinsky O, Frezza D, Schiavon E, Bergantino E, Slonimski P (1983) An mRNA maturase is encoded by the first intron of the mitochondrial gene for the subunit I of cytochrome oxidase in S. cerevisiae. Cell 35:733–742

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Covello PS, Gray MW (1990) RNA sequence and the nature of the CuA-binding site in cytochrome c oxidase. FEBS Lett 268:5–7

    Article  PubMed  CAS  Google Scholar 

  • Dewey RE, Levings CS III, Timothy DH (1986) Novel recombination in the maize mitochondrial genome produces a unique transcriptional unit in the Texas male sterile cytoplasm. Cell 44:439–444

    Article  PubMed  CAS  Google Scholar 

  • Dewey RE, Timothy DH, Levings CS III (1987) A mitochondrial protein associated with male sterility in the T cytoplasm of maize. Proc Natl Acad Sci USA 84:5374–5378

    Article  PubMed  CAS  Google Scholar 

  • Dewey RE, Siedow JN, Timothy DH, Levings CS III (1988) A 13 kDa maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science 239:293–295

    Article  PubMed  CAS  Google Scholar 

  • Feiler HS, Newton KJ (1987) Altered mitochondrial gene expression in the nonchromosomal stripe 2 mutant of maize. EMBO J6:1535–1539

    Google Scholar 

  • Glab N, Wise RP, Pring DR, Jacq C, Slominski P (1990) Expression in S. cerevisiae of a gene associated with cytoplasmic male sterility from maize: respiratory dysfunction and uncoupling. Mol Gen Genet 223:24–32

    Article  PubMed  CAS  Google Scholar 

  • Gray MW (1990) Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol 5:25–50

    Article  Google Scholar 

  • Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25:461–486

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR, Rothenberg M, Boeshore ML, Nivison HT (1985) Organelle segregation and recombination following protoplast fusion: analysis of sterile cytoplasms. In: Zaitlin M, Day P, Hollaender A (eds) Biotechnology in plant science. Academic Press, New York, pp 129–144

    Google Scholar 

  • Hanson MR, Pruitt KD, Nivison HT (1989) Male sterility loci in plant mitochondrial genomes. Oxf Surv Plant Mol Cell Biol 6:61–85

    CAS  Google Scholar 

  • Hanson MR, Sutton CA, Lu B (1996) Plant organelle gene expression: altered by RNA editing. Trends Plant Sci 1:57–64

    Article  Google Scholar 

  • Heisert V, Rasmusson AG, Thick O, Brennicke A, Grohman L (1997) Antisense repression of the mitochondrial NADH-binding subunit of complex I in transgenic potato plants affects male fertility. Plant Sci 127:61–69

    Article  Google Scholar 

  • 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 90:2370–2374

    Article  PubMed  CAS  Google Scholar 

  • Hernould M, Suharsono, 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 36:499–508

    Article  PubMed  CAS  Google Scholar 

  • Kable ML, Seuwert SD, Heidmann S, Stuart K (1996) RNA editing: a mechanism of gRNA-specified uridylate insertion into precursor mRNA. Science 273:1189–1195

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kurek I, Ezra D, Bégu D, Erel N, Litvak S, Breiman A (1997) Studies on the effect of nuclear background and tissue specificity on RNA editing of the mitochondrial ATP synthase subunits a, 6 and 9 in fertile and cytoplasmic male sterile (CMS) wheat. Theor Appl Genet 95:1305–1311

    Article  CAS  Google Scholar 

  • Laughnan JR, Gabay-Laughnan G (1983) Cytoplasmic male sterility in maize. Annu Rev Genet 17:27–48

    Article  PubMed  CAS  Google Scholar 

  • Lonsdale DM, Hodge JP, Fauron CMR (1984) The physical map and organization of the mitochondrial genome from fertile cytoplasm of maize. Nucleic Acids Res 12:9249–9261

    Article  PubMed  CAS  Google Scholar 

  • Malek O, Lättig K, Hiesel R, Brennicke A, Knoop V (1996) RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J 15:1403–1411

    PubMed  CAS  Google Scholar 

  • Maréchal-Drouard L, Weil JH, Dietrich A (1993) tRNA and rRNAs genes in plants. Annu Rev Plant Physiol Plant Mol Biol 44:13–32

    Article  Google Scholar 

  • Mariani C, de Beuckeleer M, Truettner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by chimaeric ribonuclease gene. Nature 347:737–741

    Article  CAS  Google Scholar 

  • Mariani C, Gossele V, de Beuckeleer M, de Block M, Goldberg RB, de Greef W, Leemans J (1992) A chimaeric ribonuclease inhibitor gene restores fertility to male sterile plants. Nature 257:384–387

    Article  Google Scholar 

  • Melcher T, Maas S, Higuchi M, Keller W, Seeburg PH (1995) Editing of a-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR-B pre-mRNA in vitro reveals site-selective adenosine to inosine conversion. J Biol Chem 270:8566–8570

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mulligan RM, Leon P, Walbot V (1991) Transcriptional and post-transcriptional regulation of maize mitochondrial gene expression. Mol Cell Biol 11:533–543

    PubMed  CAS  Google Scholar 

  • Newton KJ, Winberg B, Yamato K, Lupoid S, Stern DB (1995) Evidence for a novel mitochondrial promoter preceding the cox2 gene of perennial teosintes. EMBO J 14:585–593

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemuru M, Nozato N, Akashi K, Kanegue T, Ogura Y, Kohshi T, Okyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia potymorpha mitochondrial DNA: a primitive form of plant mitochondria genome. J Mol Biol 223:1–7

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD (1990) Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet 6:115–120

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD, Herbon LA (1987) Unicircular structure of the Brassica hirta mitochondrial genome. Curr Genet 11:565–570

    Article  PubMed  CAS  Google Scholar 

  • Palmer JP, Shields CR, Cohen DB, Orton TJ (1983) An unusual mitochondrial DNA plasmid in the genus Brassica. Nature 301:725–728

    Article  CAS  Google Scholar 

  • Pring DR, Levings CS III, Huww L, Timothy DM (1977) Unique DNA associated with mitochondria in the S type-cytoplasm of male sterile maize. Proc Natl Acad Sci USA 74:2904–2908

    Article  PubMed  CAS  Google Scholar 

  • Rajesakhar VK, Mullligan RM (1993) RNA editing in plant mitochondria: a-phosphate is retained during C-to-U conversion in mRNAs. Plant Cell 5:1843–1852

    Article  Google Scholar 

  • Rogers SJ, Edwardson JR (1952) The utilization of cytoplasmic male sterile inbreds in the production of corn hybrids. Agron J 44:8–13

    Article  Google Scholar 

  • Smith HC, Gott JM, Hanson MR (1997) A guide to RNA editing. RNA 3:1105–1123

    PubMed  CAS  Google Scholar 

  • Stuart K, Allen TE, Heideman S, Seiwert SD (1997) RNA editing of kinetoplast protozoa. Microbiol Mol Biol Rev 61:105–120

    PubMed  CAS  Google Scholar 

  • Teng B, Burant CF, Davidson NO (1993) Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260:1816–1819

    Article  PubMed  CAS  Google Scholar 

  • Unseld M, Marienfeld JF, Brandt P, Brennicke A (1997) The mitochondria genome of Arabidopsis thaliana contains 57 genes in 366 924 nucleotides. Nat Genet 15:57–61

    Article  PubMed  CAS  Google Scholar 

  • Van der Meer I, Stam ME, van Tunen AJ, Mol JNM, Stuitje AR (1992) Antisense inhibition of flavonoid synthesis in Petunia anthers results in male sterility. Plant Cell 4:253–262

    Article  PubMed  Google Scholar 

  • Vedel F, Pia M, Vitart V, Gutierrez S, Chétrit P, De Paepe R (1994) Molecular basis of nuclear and cytoplasmic male sterility in higher plants. Plant Physiol Biochem 32:601–618

    CAS  Google Scholar 

  • Worrald D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tabacco. Plant Cell 4:759–771

    Article  Google Scholar 

  • Young EG, Hanson MR (1987) A fused mitochondrial gene associated with CMS is developmentally regulated. Cell 50:41–49

    Article  PubMed  CAS  Google Scholar 

  • Yu W, Schuter W (1995) Evidence for a site-specific cytidine deamination reaction involved in C to U RNA editing in plant mitochondria. J Biol Chem 270:18227–18233

    Article  PubMed  CAS  Google Scholar 

  • 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 93:11259–11263

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Zanlungo S, Quiñones V, Holuigue L, Moenne A, Jordana X (1995) Splicing and editing of rps 10 transcripts in potato mitochondria. Curr Genet 27:565–571

    Article  PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. EP 630, CNRS-Université Victor Segalen-Bordeaux 2, 1 rue Camille Saint Saëns, 33077, Bordeaux Cedex, France

    S. Litvak, E. Zabaleta, V. Blanc, A. Mouras & A. Araya

  2. Laboratoire de Biologie Cellulaire et Biotechnologie Végétale, Université Victor Segalen-Bordeaux 2, Avenue des Facultés, 33405, Talence, France

    M. Hernould, D. Begu & A. Mouras

  3. Department of Botany, University of Tel-Aviv, Tel-Aviv, Israel

    I. Kurek & A. Breiman

  4. Departamento de Genética Molecular y Microbiologia, Facultad de Ciencias Biológicas, P. Universidad Católica de Chile, P.O.Box 114-D, Santiago, Chile

    X. Jordana

Authors
  1. S. Litvak
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  2. M. Hernould
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  3. E. Zabaleta
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  4. V. Blanc
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  5. D. Begu
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  6. I. Kurek
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  7. A. Breiman
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  8. X. Jordana
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  9. A. Mouras
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  10. A. Araya
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Editor information

Editors and Affiliations

  1. E 99-29 INSERM, Physiologie Mitochondriale, Université Victor Segalen Bordeaux 2, 146, rue Léo Saignat, 33076, Bordeaux Cedex, France

    Patrick Lestienne (Directeur de Recherche INSERM) (Directeur de Recherche INSERM)

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© 1999 Springer-Verlag Berlin Heidelberg

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Litvak, S. et al. (1999). Plant Cytoplasmic Male Sterility: A Mitochondrial Pathology and Its Biotechnological Application. In: Lestienne, P. (eds) Mitochondrial Diseases. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59884-5_25

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  • DOI: https://doi.org/10.1007/978-3-642-59884-5_25

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64166-4

  • Online ISBN: 978-3-642-59884-5

  • eBook Packages: Springer Book Archive

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