Skip to main content
Log in

Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

An Arabidopsis mutant rnr1, which has a defect in the basic genetic system in chloroplasts, was isolated using the screening of the high chlorophyll fluorescence phenotype. Whereas chlorophyll fluorescence and immunoblot studies showed the mutant had reduced activities of photosystems I and II, molecular characterization of the mutant suggested that a T-DNA insertion impaired the expression of a gene encoding a RNase R family member with a targeting signal to chloroplasts. Since RNase R family members have a 3′–5′ exoribonuclease activity, we examined the RNA profile in chloroplasts. In rnr1 the intercistronic cleavage between 23S and 4.5S rRNA was impaired, and a significant reduction in rRNA in chloroplasts was found, suggesting that RNR1 functions in the maturation of chloroplast rRNA. The present results suggest that defects in the genetic system in chloroplasts cause high chlorophyll fluorescence, pale green leaf, and marked reduction in the growth rate, whereas the levels of some chloroplast RNA were higher in rnr1 than in the wild-type.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allison, L.A., Simon, L.D. and Maliga, P. 1996. Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 15: 2802–2809.

    PubMed  Google Scholar 

  • Arnon, D.I. 1949. Copper enzymes in isolated chloroplast. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24: 1–15.

    Google Scholar 

  • Aro, E.M., Virgin, I. and Andersson, B. 1993. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143: 113–134.

    PubMed  Google Scholar 

  • Barkan, A. 1993. Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5: 389–402.

    PubMed  Google Scholar 

  • Barkan, A. and Goldshmidt-Clemont, M. 2000. Participation of nuclear genes in chloroplast gene expression. Biochimie 82: 559–572.

    PubMed  Google Scholar 

  • Bellaoui, M., Keddie, J.M. and Gruissem, W. 2003. DCL is a plant-specific protein required for plastid ribosomal RNA processing and embryo development. Plant Mol. Biol. 53: 531–543.

    PubMed  Google Scholar 

  • Bisanz, C., Begot, L., Carol, P., Perez, P., Bligny, M., Pesey, H., Gallois, J.L., Lerbs-Mache, S. and Mache, R. 2003. The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of the plastid ribosomal RNAs and is essential for chloroplast differentiation. Plant Mol. Biol. 51: 651–663.

    PubMed  Google Scholar 

  • Cheng, Z.-F. and Deutscher, M.P. 2002. Purification and characterization of the Escherichia coli exoribonuclease RNase R. J. Biol. Chem. 277: 21624–21629.

    Google Scholar 

  • Chiu, W.L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. and Sheen, J. 1996. Engineered GFP as a vital reporter in plants. Curr. Biol. 6: 325–330.

    PubMed  Google Scholar 

  • Deutscher, M.P. and Reuven, N.B. 1991. Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. USA. 88: 3277–3280.

    PubMed  Google Scholar 

  • Deutscher, M.P. and Li, Z. 2001. Exoribonucleases and their multiple roles in RNA metabolism. Prog. Nucleic Acid Res. Mol. Biol. 66: 67–105.

    PubMed  Google Scholar 

  • Donovan, W.P. and Kushner, S.R. 1986. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA. 83: 120–124.

    PubMed  Google Scholar 

  • Dziembowski, A., Malewicz, M., Minczuk, M., Golik, P., Dmochowska, A. and Stepien, P.P. 1998. The yeast nuclear gene DSS1, which codes for a putative RNase II, is necessary for the function of the mitochondrial degradosome in processing and turnover of RNA. Mol. Gen. Genet. 260: 108–114.

    PubMed  Google Scholar 

  • Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300: 1005–1016.

    PubMed  Google Scholar 

  • Feldmann, K.A. 1987. Agrobacterium-mediated transformation of germinating seeds of Arabidopsis thaliana: a non-tissue culture approach. Mol. Gen. Genet. 208: 1–9.

    Google Scholar 

  • Gegenheimer, P. and Apirion, D. 1981. Processing of procaryotic ribonucleic acid. Microbiol. Rev. 45: 502–541.

    PubMed  Google Scholar 

  • Harris, E.H., Boynton, J.E. and Gillham, N.W. 1994. Chloroplast ribosomes and protein synthesis. Microbiol. Rev. 58: 700–754.

    PubMed  Google Scholar 

  • Hess, W.R. and Bo¨ rner, T. 1999. Organellar RNA polymerases of higher plants. Int. Rev. Cytol. 190: 1–59.

    PubMed  Google Scholar 

  • Holloway, S.P. and Herrin D.L. 1998. Processing of a composite large subunit rRNA: studies with Chlamydomonas mutant deficient in maturation of the 23S-like rRNA. Plant Cell 10: 1193–1206.

    PubMed  Google Scholar 

  • Ko¨ ssel, H., Natt, E., Strittmatter, G., Fritzsche, E., Gozdicka-Jozefiak, A. and Przybyl, D. 1985. Structure and expression of rRNA operons from plastid of higher plants. In: L. van Vloten-Doting, G. Groot and T. Hall (Eds.) Molecular Form and Function of the Plant Genome, Plenum Press, New York, pp. 183–198.

    Google Scholar 

  • Krause, G.H. and Weis, E. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 313–349.

    Google Scholar 

  • Liu, Y.G., Mitsukawa, N., Oosumi, T. and Whittier, R.F. 1995.Efficient isolation and mapping of Arabidopsis thaliana TDNA insert junction by thermal asymmetric interlaced PCR. Plant J. 8: 457–463.

    PubMed  Google Scholar 

  • Meurer, J., Meierhoff, K and Westhoff, P. 1996. Isolation of high-chlorophyll-fluorescence mutants of Arabidopsis thaliana and characterization by spectroscopy, immunoblotting and northern hybridization. Planta 198: 385–396.

    PubMed  Google Scholar 

  • Miles, D. 1980. Mutants of higher plants: maize. Methods Enzymol. 69: 3–23.

    Google Scholar 

  • Mitchell, P., Petfalski, E. Shevchenko, A., Mann, M. and Tollervey, D. 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 30–50 exoribonucleases. Cell 91: 457–466.

    PubMed  Google Scholar 

  • Monde, R.A., Schuster, G. and Stern, D.B. 2000. Processing and degradation of chloroplast mRNA. Biochimie 82: 573–582.

    PubMed  Google Scholar 

  • Muramoto, T., Kohchi, T., Yokota, A., Hwang, I. and Goodman, H.M. 1999. The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11: 335–348.

    PubMed  Google Scholar 

  • Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol. Plant. 15: 473–497.

    Google Scholar 

  • Pesaresi, P., Varotto, C., Meurer, J., Jahns, P., Salamini, F. and Leister, D. 2001. Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. Plant J. 27: 179–189.

    PubMed  Google Scholar 

  • Schreiber, U., Klughammer, C. and Neubauer, C. 1988.Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system. Z. Naturforsch. [C] 43: 686–698.

    Google Scholar 

  • Schultes, N.P., Sawers, R.J., Brutnull, T.P. and Krueger, R.W. 2000. Maize high chlorophyll fluorescent 60 mutation is caused by Ac disruption of the gene encoding the chloroplast ribosomal small subunit protein 17. Plant J. 21: 317–327.

    PubMed  Google Scholar 

  • Shikanai, T., Shimizu, K., Endo, T. and Hashimoto, T. 1998.Screening of Arabidopsis mutants lacking down regulation of photosystem II using an imaging system of chlorophyll fluorescence. In: G. Garab (Ed.), Photosynthesis: Mechanism and Effects, Vol. V, Kluwer Academic Publishers, Dordrecht, pp. 4293–4296.

    Google Scholar 

  • Shikanai, T., Munekage, Y., Shimizu, K., Endo, T. and Hashimoto, T. 1999. Identification and characterization of Arabidopsis mutants with reduced quenching of chlorophyll fluorescence. Plant Cell Physiol. 40: 1134–1142.

    PubMed  Google Scholar 

  • Srivastava, A.K. and Schlessinger, D. 1990. Mechanism and regulation of bacterial ribosomal RNA processing. Annu. Rev. Microbiol. 44: 105–129.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Walter, M., Kilian, J. and Kudla, J. 2002. PNPase activity determines the efficiency of mRNA 30-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. EMBO J. 21: 6905–6914.

    PubMed  Google Scholar 

  • Yamamoto, Y.Y., Puente. P. and Deng, X.-W. 2000. An Arabidopsis cotyledon-specific albino locus: possible role in 16S rRNA maturation. Plant Cell Physiol. 41: 68–76.

    PubMed  Google Scholar 

  • Zuo, Y. and Deutscher, M.P. 2001. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29: 1017–1026.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kishine, M., Takabayashi, A., Munekage, Y. et al. Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Mol Biol 55, 595–606 (2004). https://doi.org/10.1007/s11103-004-1507-1

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-1507-1

Navigation