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Constancy of organellar genome copy numbers during leaf development and senescence in higher plants

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Abstract

In higher plants, plastid and mitochondrial genomes occur at high copy numbers per cell. Several recent publications have suggested that, in higher plants like Arabidopsis and maize, chloroplast DNA is virtually absent in mature and old leaves. This conclusion was mainly based on DAPI staining of isolated chloroplasts. If correct, the finding that chloroplasts in mature leaves lack DNA would change dramatically our understanding of gene expression, mRNA stability and protein stability in chloroplasts. In view of the wide implications that the disposal of chloroplast DNA during leaf development would have, we have reinvestigated the age dependency of genome copy numbers in chloroplasts and, in addition, tested for possible changes in mitochondrial genome copy number during plant development. Analyzing chloroplast and mitochondrial DNA amounts in Arabidopsis and tobacco plants, we find that organellar genome copy numbers remain remarkably constant during leaf development and are present in essentially unchanged numbers even in the senescing leaves. We conclude that, during leaf development, organellar gene expression in higher plants is not significantly regulated at the level of genome copy number and we discuss possible explanations for the failure to detect DNA in isolated chloroplasts stained with DAPI.

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References

  • Aguettaz P, Seyer P, Pesey H, Lescure A-M (1987) Relation between the plastid gene dosage and the levels of 16S rRNA and rbcL gene transcripts during amyloplast to chloroplast change in mixotrophic spinach cell suspensions. Plant Mol Biol 8:169–177

    Article  CAS  Google Scholar 

  • Allison LA, Maliga P (1995) Light-responsive and transcription-enhancing elements regulate the plastid psbD core promoter. EMBO J 14:3721–3730

    PubMed  CAS  Google Scholar 

  • Atchison BA, Whitfeld PR, Bottomley W (1976) Comparison of chloroplast DNAs by specific fragmentation with EcoRI endonuclease. Mol Gen Genet 148:263–269

    Article  CAS  Google Scholar 

  • Ayliffe MA, Timmis JN (1992) Tobacco nuclear DNA contains long tracts of homology to chloroplast DNA. Theor Appl Genet 85:229–238

    Article  CAS  Google Scholar 

  • Ayliffe MA, Scott NS, Timmis JN (1998) Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants. Mol Biol Evol 15:738–745

    PubMed  CAS  Google Scholar 

  • Backert S, Nielsen BL, Börner T (1997) The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci 2:477–483

    Article  Google Scholar 

  • Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277:2006–2011

    Article  PubMed  CAS  Google Scholar 

  • Baumgartner BJ, Rapp JC, Mullet JE (1988) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89:1011–1018

    Google Scholar 

  • Bendich AJ (1987) Why do chloroplasts and mitochondria contain so many copies of their genome? Bioessays 6:279–282

    Article  PubMed  CAS  Google Scholar 

  • Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16:1661–1666

    Article  PubMed  CAS  Google Scholar 

  • Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338

    Article  PubMed  CAS  Google Scholar 

  • Bock R (2001) Transgenic chloroplasts in basic research and plant biotechnology. J Mol Biol 312:425–438

    Article  PubMed  CAS  Google Scholar 

  • Bock R (2005) Extranuclear inheritance: gene transfer out of plastids. Prog Bot 67:75–98

    Article  Google Scholar 

  • Coleman AW, Nerozzi AM (1999) Temporal and spatial coordination of cells with their plastid component. Int Rev Cytol 193:125–164

    PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Eberhard S, Drapier D, Wollman F-A (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31:149–160

    Article  PubMed  CAS  Google Scholar 

  • Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop H-U (1999) In vivo analysis of plastid psbA, rbcL and rpl32 UTR elements by chloroplast transformation: tobacco plastid gene expression is controlled by modulation of transcript levels and translation efficiency. Plant J 19:333–345

    Article  PubMed  CAS  Google Scholar 

  • Giegé P, Hoffmann M, Binder S, Brennicke A (2000) RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep 1:164–170

    Article  PubMed  Google Scholar 

  • Gillham NW, Boynton JE, Hauser CR (1994) Translational regulation of gene expression in chloroplasts and mitochondria. Annu Rev Genet 28:71–93

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Lang BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Tumel 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  PubMed  CAS  Google Scholar 

  • Hagemann R (2002) Milestones in plastid genetics of higher plants. Prog Bot 63:1–51

    Google Scholar 

  • Hermann M, Bock R (1999) Transfer of plastid RNA-editing activity to novel sites suggests a critical role for spacing in editing-site recognition. Proc Natl Acad Sci USA 96:4856–4861

    Article  PubMed  CAS  Google Scholar 

  • Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76

    Article  PubMed  CAS  Google Scholar 

  • Huang CY, Grünheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138:1723–1733

    Article  PubMed  CAS  Google Scholar 

  • Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139

    Article  PubMed  CAS  Google Scholar 

  • Kroymann J, Schneider W, Zetsche K (1995) Opposite regulation of the copy number and the expression of plastid and mitochondrial genes by light and acetate in the green flagellate Chlorogonium. Plant Physiol 108:1641–1646

    PubMed  Google Scholar 

  • Kuroiwa T (1982) Mitochondrial nuclei. Int Rev Cytol 75:1–59

    Article  PubMed  CAS  Google Scholar 

  • Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62

    CAS  Google Scholar 

  • Major F, Gautheret D, Cedergren R (1993) Reproducing the three-dimensional structure of a tRNA molecule from structural constraints. Proc Natl Acad Sci USA 90:9408–9412

    Article  PubMed  CAS  Google Scholar 

  • Maliga P (2004) Plastid transformation in higher plants. Annu Rev Plant Biol 55:289–313

    Article  PubMed  CAS  Google Scholar 

  • Miyamura S, Kuroiwa T, Nagata T (1990) Multiplication and differentiation of plastid nucleoids during development of chloroplasts and etioplasts from proplastids in Triticum aestivum. Plant Cell Physiol 31:597–602

    CAS  Google Scholar 

  • Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357–363

    Article  PubMed  CAS  Google Scholar 

  • Noutsos C, Richly E, Leister D (2005) Generation and evolutionary fate of insertions of organelle DNA in the nuclear genomes of flowering plants. Genome Res 15:616–628

    Article  PubMed  CAS  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2004) Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize. J Mol Biol 344:1311–1330

    Article  PubMed  CAS  Google Scholar 

  • Rochaix J-D (1992) Post-transcriptional steps in the expression of chloroplast genes. Ann Rev Cell Biol 8:1–28

    PubMed  CAS  Google Scholar 

  • Rowan BA, Oldenburg DJ, Bendich AJ (2004) The demise of chloroplast DNA in Arabidopsis. Curr Genet 46:176–181

    Article  PubMed  CAS  Google Scholar 

  • Scott NS, Timmis JN (1984) Homologies between nuclear and plastid DNA in spinach. Theor Appl Genet 67:279–288

    Article  CAS  Google Scholar 

  • Staub JM, Maliga P (1994) Translation of the psbA mRNA is regulated by light via the 5′-untranslated region in tobacco plastids. Plant J 6:547–553

    Article  PubMed  CAS  Google Scholar 

  • Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci USA 100:8828–8833

    Article  PubMed  CAS  Google Scholar 

  • Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Gen Genomics 272:603–615

    Article  CAS  Google Scholar 

  • Sun C-W, Callis J (1993) Recent stable insertion of mitochondrial DNA into an Arabidopsis polyubiquitin gene by nonhomologous recombination. Plant Cell 5:97–107

    Article  PubMed  CAS  Google Scholar 

  • Suzuki JY, Sriraman P, Svab Z, Maliga P (2003) Unique architecture of the plastid ribosomal RNA operon promoter recognized by the multisubunit RNA polymerase in tobacco and other higher plants. Plant Cell 15:195–205

    Article  PubMed  CAS  Google Scholar 

  • Timmis JN, Scott NS (1983) Spinach nuclear and chloroplast DNAs have homologous sequences. Nature 305:65–67

    Article  CAS  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–136

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Wakasugi T, Tsudzuki T, Sugiura M (2001) The genomics of land plant chloroplasts: gene content and alteration of genomic information by RNA editing. Photosynthesis Res 70:107–118

    Article  CAS  Google Scholar 

  • Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121–128

    Article  PubMed  CAS  Google Scholar 

  • Zerges W (2000) Translation in chloroplasts. Biochimie 82:583–601

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Katrin Piepenburg for technical assistance and the MPI-MP Green Team for plant care and cultivation. We are indebted to Dr. Masahiro Sugiura for providing cloned tobacco mitochondrial DNA fragments. This research was supported by grants from the European Union (FP6 Plastomics project LSHG-CT-2003-503238) and by the Max Planck Society.

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Authors and Affiliations

  1. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Weimin Li, Stephanie Ruf & Ralph Bock

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  1. Weimin Li
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  2. Stephanie Ruf
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  3. Ralph Bock
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Correspondence to Ralph Bock.

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Communicated by R. Hagemann

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Li, W., Ruf, S. & Bock, R. Constancy of organellar genome copy numbers during leaf development and senescence in higher plants. Mol Genet Genomics 275, 185–192 (2006). https://doi.org/10.1007/s00438-005-0075-7

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  • DOI: https://doi.org/10.1007/s00438-005-0075-7

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