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Overexpression of mitochondrial genes is caused by interactions between the nucleus of Brassica rapa and the cytoplasm of Diplotaxis muralis in the leaves of alloplasmic lines of B. rapa

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Abstract

In Brassica species, alloplasmic lines displaying cytoplasmic male sterility (CMS) are established by combining the nucleus from B. rapa with the cytoplasm from Diplotaxis muralis. The failure to observe restriction fragment length polymorphism (RFLP) patterns of mitochondrial genes (coxII, coxIII, atpA, atp6, atp9, cob, nad3, nad6, and nad9) between alloplasmic lines of B. rapa and D. muralis indicates that introgression of the B. rapa nucleus into the cytoplasm of D. muralis does not cause any alterations in the structure of the mitochondrial genome. To investigate how the nucleus influences the cytoplasm, we examined the expression of mitochondrial genes in the leaves of euplasmic and alloplasmic lines of B. rapa and D. muralis. We detected higher levels of mitochondrial gene mRNAs in alloplasmic lines of B. rapa than in D. muralis. Patterns of mitochondrial gene transcription also differed among the alloplasmic lines of B. rapa. Thus, expression of mitochondrial genes in alloplasmic lines of B. rapa differed in the leaves compared to D. muralis. Overexpression of mitochondrial genes may be the result of novel interactions between the nucleus and the mitochondria in alloplasmic lines of B. rapa. Further study is necessary to clarify how these phenomena are involved in CMS.

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References

  • Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male sterile plants. Proc Natl Acad Sci USA 99:10887–10892

    Article  CAS  PubMed  Google Scholar 

  • Bergman P, Edqvist J, Farbos I, Glimelius K (2000) Male sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol Biol 42:531–544

    Article  CAS  PubMed  Google Scholar 

  • Binder S, Marchfelder A, Brennicke A (1996) Regulation of gene expression in plant mitochondria. Plant Mol Biol 32:303–314

    CAS  PubMed  Google Scholar 

  • Cermakian N, Ikeda TM, Cedergren R, Gray MW (1996) Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res 24:648–654

    Article  CAS  PubMed  Google Scholar 

  • Dennis DT (1987) The biochemistry of energy utilization in plants. Chapman and Hall, New York

  • Gray MW, Lang BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn TG, Plante I, Rioux P, Saint-Louis D, Zhu Y, Burger G (1998) Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res 26:865–878

    Article  CAS  PubMed  Google Scholar 

  • Gray MW, Lang BF (1998) Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol 6:1–3

    Article  CAS  PubMed  Google Scholar 

  • Hanson MR, Folkerts O (1992) Structure and function of the higher plant mitochondrial genome. Int Rev Cytol 141:129–172

    CAS  Google Scholar 

  • Hedtke B, Borner T, Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerase in Arabidopsis. Science 277:809–811

    Article  CAS  PubMed  Google Scholar 

  • Hess WR, Borner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59

    CAS  PubMed  Google Scholar 

  • Hinata K, Konno N (1979) Studies on a male sterile strain having the Brassica campestris nucleus and the Diplotaxis muralis cytoplasm. 1 On the breeding procedure and some characteristics of the male sterile strain. Jpn J Breed 29:305–311

    Google Scholar 

  • Kazama T, Toriyama K (2003) A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544:99–102

    Article  CAS  PubMed  Google Scholar 

  • Kempken F, Pring DR (1999) Male sterility in higher plants-fundamentals and applications. Progress in botany, vol 60. Springer, Berlin Heidelberg New York, pp140–166

  • Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 34:407–415

    Article  CAS  PubMed  Google Scholar 

  • Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 37:315–325

    Article  CAS  PubMed  Google Scholar 

  • Landgren M, Zetterstrand M, Sundberg E, Glimelius K (1996) Alloplasmic male-sterile Brassica lines containing B. tournefortii mitochondria express an ORF 3′ of the atp6 gene and a 32 kDa protein. Plant Mol Biol 32:879–890

    CAS  PubMed  Google Scholar 

  • Laver HK, Reynolds SJ, Moneger F, Leaver CJ (1991) Mitochondrial genome organization and expression associated with cytoplasmic male sterility in sunflower (Helianthus annuus). Plant J 1:185–193

    CAS  PubMed  Google Scholar 

  • Li X-Q, Zhang M, Brown GG (1996) Cell-specific expression of mitochondrial transcripts in maize seedlings. Plant Cell 8:1961–1975

    Article  CAS  PubMed  Google Scholar 

  • Liu Ji-H, Landgren M, Glimelius K (1996) Transfer of the Brassica tournefortii cytoplasm to B. napus for the production of cytoplasmic male sterile B. napus. Physiol Plant 96:123–129

    Article  CAS  Google Scholar 

  • Mackenzie S, He S, Lyznik A (1994) The elusive plant mitochondrion as a genetic system. Plant Physiol 105:775–780

    CAS  PubMed  Google Scholar 

  • Masters BS, Stohl LL, Clayton DA (1987) Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7. Cell 51:89–99

    Article  CAS  PubMed  Google Scholar 

  • Moneger F, Smart CJ, Leaver CJ (1994) Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J 13:8–17

    CAS  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    CAS  PubMed  Google Scholar 

  • Nakamura C, Yamakawa S, Suzuki T (1991a) Recovery of normal photosynthesis and respiration in common wheat with Agropyron cytoplasms by telocentric Agropyron chromosomes. Theor Appl Genet 81:514–518

    Google Scholar 

  • Nakamura C, Suzuki T, Kasai K, Kubota Y, Yamagami C, Mori N (1991b) Cytoplasmic variability in wheat and its related species revealed by photosynthetic and respiratory characteristics. In: Sasakuma T, Kinoshita T (eds) Nuclear and organellar genomes of wheat species. Kihara Memorial Foundation, Yokohama, pp 195–204

  • Ogihara Y, Futami K, Tsuji K, Murai K (1997) Alloplasmic wheats with Aegilops crassa cytoplasm which express photoperiod-sensitive homeotic transformations of anthers, show alterations in mitochondrial DNA structure and transcription. Mol Gen Genet 255:45–53

    Article  CAS  PubMed  Google Scholar 

  • Pathania A, Bhat SR, Dinesh Kumar V, Ashutosh Kirti PB, Prakash S, Chopra VL (2003) Cytoplasmic male sterility in alloplasmic Brassica juncea carrying Diplotaxis catholica cytoplasm: molecular characterization and genetics of fertility restoration. Theor Appl Genet 107:455–461

    Article  CAS  PubMed  Google Scholar 

  • Pradhan AK, Mukhopadhyay A, Pental D (1991) Identification of the putative cytoplasmic donor of a CMS system in Brassica juncea. Plant Breed 106:204–208

    Google Scholar 

  • Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Singh M, Brown GG (1993) Characterization of expression of a mitochondrial gene region associated with the Brassica “Polima” CMS: developmental influences. Curr Genet 24:316–322

    CAS  PubMed  Google Scholar 

  • Smart CJ, Moneger F, Leaver CJ (1994) Cell-specific regulation of gene expression in mitochondria during anther development in sunflower. Plant Cell 6:811–825

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Nakamura C, Mori N, Kaneda C (1995) Overexpression of mitochondrial genes in alloplasmic common wheat with a cytoplasm of wheatgrass (Agropyron trichophorum) showing depressed vigor and male sterility. Plant Mol Biol 27:553–565

    CAS  PubMed  Google Scholar 

  • Topping JF, Leaver CJ (1990) Mitochondrial gene expression during wheat leaf development. Planta 182:399–407

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Weihe A, Hedtke B, Borner T (1997) Cloning and characterization of a cDNA encoding a bacteriophage-type RNA polymerase from the higher plant Chenopodium album. Nucleic Acids Res 25:2319–2325

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki S, Konno N, Kishitani S (1998) An alteration in transcription patterns of mitochondrial genes in alloplasmic lines of Brassica rapa. Genes Genet Syst 73:167–172

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported partly by a Grant-in-aid for Co-operative Research (No. 06304011) from the Ministry of Education, Science, Sports and Culture of Japan. We wish to thank T. Mikami, T. Kubo, and A. Kanno for gifts of probes and for their valuable comments.

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Correspondence to Seiji Yamasaki.

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Yamasaki, S., Konno, N. & Kishitani, S. Overexpression of mitochondrial genes is caused by interactions between the nucleus of Brassica rapa and the cytoplasm of Diplotaxis muralis in the leaves of alloplasmic lines of B. rapa. J Plant Res 117, 339–344 (2004). https://doi.org/10.1007/s10265-004-0162-6

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  • DOI: https://doi.org/10.1007/s10265-004-0162-6

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