Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1999 Jan 15;18(2):490–499. doi: 10.1093/emboj/18.2.490

Involvement of Arabidopsis thaliana ribosomal protein S27 in mRNA degradation triggered by genotoxic stress.

E Revenkova 1, J Masson 1, C Koncz 1, K Afsar 1, L Jakovleva 1, J Paszkowski 1
PMCID: PMC1171142  PMID: 9889204

Abstract

A recessive Arabidopsis mutant with elevated sensitivity to DNA damaging treatments was identified in one out of 800 families generated by T-DNA insertion mutagenesis. The T-DNA generated a chromosomal deletion of 1287 bp in the promoter of one of three S27 ribosomal protein genes (ARS27A) preventing its expression. Seedlings of ars27A developed normally under standard growth conditions, suggesting wild-type proficiency of translation. However, growth was strongly inhibited in media supplemented with methyl methane sulfate (MMS) at a concentration not affecting the wild type. This inhibition was accompanied by the formation of tumor-like structures instead of auxiliary roots. Wild-type seedlings treated with increasing concentrations of MMS up to a lethal dose never displayed such a trait, neither was this phenotype observed in ars27A plants in the absence of MMS or under other stress conditions. Thus, the hypersensitivity and tumorous growth are mutant-specific responses to the genotoxic MMS treatment. Another important feature of the mutant is its inability to perform rapid degradation of transcripts after UV treatment, as seen in wild-type plants. Therefore, we propose that the ARS27A protein is dispensable for protein synthesis under standard conditions but is required for the elimination of possibly damaged mRNA after UV irradiation.

Full Text

The Full Text of this article is available as a PDF (515.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bailey T. L., Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol. 1994;2:28–36. [PubMed] [Google Scholar]
  2. Bailey T. L., Gribskov M. Combining evidence using p-values: application to sequence homology searches. Bioinformatics. 1998;14(1):48–54. doi: 10.1093/bioinformatics/14.1.48. [DOI] [PubMed] [Google Scholar]
  3. Baudin-Baillieu A., Tollervey D., Cullin C., Lacroute F. Functional analysis of Rrp7p, an essential yeast protein involved in pre-rRNA processing and ribosome assembly. Mol Cell Biol. 1997 Sep;17(9):5023–5032. doi: 10.1128/mcb.17.9.5023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chan Y. L., Suzuki K., Olvera J., Wool I. G. Zinc finger-like motifs in rat ribosomal proteins S27 and S29. Nucleic Acids Res. 1993 Feb 11;21(3):649–655. doi: 10.1093/nar/21.3.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Connelly S., Filipowicz W. Activity of chimeric U small nuclear RNA (snRNA)/mRNA genes in transfected protoplasts of Nicotiana plumbaginifolia: U snRNA 3'-end formation and transcription initiation can occur independently in plants. Mol Cell Biol. 1993 Oct;13(10):6403–6415. doi: 10.1128/mcb.13.10.6403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dietrich R. A., Richberg M. H., Schmidt R., Dean C., Dangl J. L. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell. 1997 Mar 7;88(5):685–694. doi: 10.1016/s0092-8674(00)81911-x. [DOI] [PubMed] [Google Scholar]
  8. Feaver W. J., Gileadi O., Kornberg R. D. Purification and characterization of yeast RNA polymerase II transcription factor b. J Biol Chem. 1991 Oct 5;266(28):19000–19005. [PubMed] [Google Scholar]
  9. Feaver W. J., Henry N. L., Wang Z., Wu X., Svejstrup J. Q., Bushnell D. A., Friedberg E. C., Kornberg R. D. Genes for Tfb2, Tfb3, and Tfb4 subunits of yeast transcription/repair factor IIH. Homology to human cyclin-dependent kinase activating kinase and IIH subunits. J Biol Chem. 1997 Aug 1;272(31):19319–19327. doi: 10.1074/jbc.272.31.19319. [DOI] [PubMed] [Google Scholar]
  10. Feaver W. J., Svejstrup J. Q., Bardwell L., Bardwell A. J., Buratowski S., Gulyas K. D., Donahue T. F., Friedberg E. C., Kornberg R. D. Dual roles of a multiprotein complex from S. cerevisiae in transcription and DNA repair. Cell. 1993 Dec 31;75(7):1379–1387. doi: 10.1016/0092-8674(93)90624-y. [DOI] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  12. Fernandez-Pol J. A., Klos D. J., Hamilton P. D. A growth factor-inducible gene encodes a novel nuclear protein with zinc finger structure. J Biol Chem. 1993 Oct 5;268(28):21198–21204. [PubMed] [Google Scholar]
  13. Fernandez-Pol J. A. Metallopanstimulin as a novel tumor marker in sera of patients with various types of common cancers: implications for prevention and therapy. Anticancer Res. 1996 Jul-Aug;16(4B):2177–2185. [PubMed] [Google Scholar]
  14. Grabowski D. T., Deutsch W. A., Derda D., Kelley M. R. Drosophila AP3, a presumptive DNA repair protein, is homologous to human ribosomal associated protein P0. Nucleic Acids Res. 1991 Aug 11;19(15):4297–4297. doi: 10.1093/nar/19.15.4297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gulyas K. D., Donahue T. F. SSL2, a suppressor of a stem-loop mutation in the HIS4 leader encodes the yeast homolog of human ERCC-3. Cell. 1992 Jun 12;69(6):1031–1042. doi: 10.1016/0092-8674(92)90621-i. [DOI] [PubMed] [Google Scholar]
  16. Heyer W. D. The search for the right partner: homologous pairing and DNA strand exchange proteins in eukaryotes. Experientia. 1994 Mar 15;50(3):223–233. doi: 10.1007/BF01924005. [DOI] [PubMed] [Google Scholar]
  17. Humbert S., van Vuuren H., Lutz Y., Hoeijmakers J. H., Egly J. M., Moncollin V. p44 and p34 subunits of the BTF2/TFIIH transcription factor have homologies with SSL1, a yeast protein involved in DNA repair. EMBO J. 1994 May 15;13(10):2393–2398. doi: 10.1002/j.1460-2075.1994.tb06523.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iordanov M. S., Pribnow D., Magun J. L., Dinh T. H., Pearson J. A., Magun B. E. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J Biol Chem. 1998 Jun 19;273(25):15794–15803. doi: 10.1074/jbc.273.25.15794. [DOI] [PubMed] [Google Scholar]
  19. Jacobson A., Peltz S. W. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu Rev Biochem. 1996;65:693–739. doi: 10.1146/annurev.bi.65.070196.003401. [DOI] [PubMed] [Google Scholar]
  20. Kearsey S., Kipling D. Recombination and RNA processing: a common strand? Trends Cell Biol. 1991 Nov;1(5):110–112. doi: 10.1016/0962-8924(91)90101-e. [DOI] [PubMed] [Google Scholar]
  21. Kim J., Chubatsu L. S., Admon A., Stahl J., Fellous R., Linn S. Implication of mammalian ribosomal protein S3 in the processing of DNA damage. J Biol Chem. 1995 Jun 9;270(23):13620–13629. doi: 10.1074/jbc.270.23.13620. [DOI] [PubMed] [Google Scholar]
  22. Kiss T., Kis M., Solymosy F. Nucleotide sequence of a 25S rRNA gene from tomato. Nucleic Acids Res. 1989 Jan 25;17(2):796–796. doi: 10.1093/nar/17.2.796. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kiss T., Marshallsay C., Filipowicz W. 7-2/MRP RNAs in plant and mammalian cells: association with higher order structures in the nucleolus. EMBO J. 1992 Oct;11(10):3737–3746. doi: 10.1002/j.1460-2075.1992.tb05459.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Koncz C., Martini N., Mayerhofer R., Koncz-Kalman Z., Körber H., Redei G. P., Schell J. High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8467–8471. doi: 10.1073/pnas.86.21.8467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Louie D. F., Resing K. A., Lewis T. S., Ahn N. G. Mass spectrometric analysis of 40 S ribosomal proteins from Rat-1 fibroblasts. J Biol Chem. 1996 Nov 8;271(45):28189–28198. doi: 10.1074/jbc.271.45.28189. [DOI] [PubMed] [Google Scholar]
  26. Maquat L. E. When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells. RNA. 1995 Jul;1(5):453–465. [PMC free article] [PubMed] [Google Scholar]
  27. Masson J. E., King P. J., Paszkowski J. Mutants of Arabidopsis thaliana hypersensitive to DNA-damaging treatments. Genetics. 1997 May;146(1):401–407. doi: 10.1093/genetics/146.1.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mengiste T., Amedeo P., Paszkowski J. High-efficiency transformation of Arabidopsis thaliana with a selectable marker gene regulated by the T-DNA 1' promoter. Plant J. 1997 Oct;12(4):945–948. doi: 10.1046/j.1365-313x.1997.12040945.x. [DOI] [PubMed] [Google Scholar]
  29. Minet M., Dufour M. E., Lacroute F. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 1992 May;2(3):417–422. doi: 10.1111/j.1365-313x.1992.00417.x. [DOI] [PubMed] [Google Scholar]
  30. Mitchell P., Petfalski E., Shevchenko A., Mann M., Tollervey D. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'-->5' exoribonucleases. Cell. 1997 Nov 14;91(4):457–466. doi: 10.1016/s0092-8674(00)80432-8. [DOI] [PubMed] [Google Scholar]
  31. Nairn C. J., Winesett L., Ferl R. J. Nucleotide sequence of an actin gene from Arabidopsis thaliana. Gene. 1988 May 30;65(2):247–257. doi: 10.1016/0378-1119(88)90461-1. [DOI] [PubMed] [Google Scholar]
  32. Oberto J., Bonnefoy E., Mouray E., Pellegrini O., Wikström P. M., Rouvière-Yaniv J. The Escherichia coli ribosomal protein S16 is an endonuclease. Mol Microbiol. 1996 Mar;19(6):1319–1330. doi: 10.1111/j.1365-2958.1996.tb02476.x. [DOI] [PubMed] [Google Scholar]
  33. Peters J. L., Silverthorne J. Organ-Specific Stability of Two Lemna rbcS mRNAs Is Determined Primarily in the Nuclear Compartment. Plant Cell. 1995 Jan;7(1):131–140. doi: 10.1105/tpc.7.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Phillips J. R., Dunn M. A., Hughes M. A. mRNA stability and localisation of the low-temperature-responsive barley gene family blt14. Plant Mol Biol. 1997 Apr;33(6):1013–1023. doi: 10.1023/a:1005717613224. [DOI] [PubMed] [Google Scholar]
  35. Pulak R., Anderson P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 1993 Oct;7(10):1885–1897. doi: 10.1101/gad.7.10.1885. [DOI] [PubMed] [Google Scholar]
  36. Ruiz-Echevarria M. J., Czaplinski K., Peltz S. W. Making sense of nonsense in yeast. Trends Biochem Sci. 1996 Nov;21(11):433–438. doi: 10.1016/s0968-0004(96)10055-4. [DOI] [PubMed] [Google Scholar]
  37. Saebøe-Larssen S., Urbanczyk Mohebi B., Lambertsson A. The Drosophila ribosomal protein L14-encoding gene, identified by a novel Minute mutation in a dense cluster of previously undescribed genes in cytogenetic region 66D. Mol Gen Genet. 1997 Jun;255(2):141–151. doi: 10.1007/s004380050482. [DOI] [PubMed] [Google Scholar]
  38. Seeley K. A., Byrne D. H., Colbert J. T. Red Light-Independent Instability of Oat Phytochrome mRNA in Vivo. Plant Cell. 1992 Jan;4(1):29–38. doi: 10.1105/tpc.4.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tishkoff D. X., Johnson A. W., Kolodner R. D. Molecular and genetic analysis of the gene encoding the Saccharomyces cerevisiae strand exchange protein Sep1. Mol Cell Biol. 1991 May;11(5):2593–2608. doi: 10.1128/mcb.11.5.2593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tsugeki R., Kochieva E. Z., Fedoroff N. V. A transposon insertion in the Arabidopsis SSR16 gene causes an embryo-defective lethal mutation. Plant J. 1996 Sep;10(3):479–489. doi: 10.1046/j.1365-313x.1996.10030479.x. [DOI] [PubMed] [Google Scholar]
  41. Turck F., Kozma S. C., Thomas G., Nagy F. A heat-sensitive Arabidopsis thaliana kinase substitutes for human p70s6k function in vivo. Mol Cell Biol. 1998 Apr;18(4):2038–2044. doi: 10.1128/mcb.18.4.2038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Van Larebeke N., Engler G., Holsters M., Van den Elsacker S., Zaenen I., Schilperoort R. A., Schell J. Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature. 1974 Nov 8;252(5479):169–170. doi: 10.1038/252169a0. [DOI] [PubMed] [Google Scholar]
  43. Van Lijsebettens M., Vanderhaeghen R., De Block M., Bauw G., Villarroel R., Van Montagu M. An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J. 1994 Jul 15;13(14):3378–3388. doi: 10.1002/j.1460-2075.1994.tb06640.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wang Z., Buratowski S., Svejstrup J. Q., Feaver W. J., Wu X., Kornberg R. D., Donahue T. F., Friedberg E. C. The yeast TFB1 and SSL1 genes, which encode subunits of transcription factor IIH, are required for nucleotide excision repair and RNA polymerase II transcription. Mol Cell Biol. 1995 Apr;15(4):2288–2293. doi: 10.1128/mcb.15.4.2288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wang Z., Svejstrup J. Q., Feaver W. J., Wu X., Kornberg R. D., Friedberg E. C. Transcription factor b (TFIIH) is required during nucleotide-excision repair in yeast. Nature. 1994 Mar 3;368(6466):74–76. doi: 10.1038/368074a0. [DOI] [PubMed] [Google Scholar]
  46. Woodgate R., Rajagopalan M., Lu C., Echols H. UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD'. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7301–7305. doi: 10.1073/pnas.86.19.7301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wool I. G. Extraribosomal functions of ribosomal proteins. Trends Biochem Sci. 1996 May;21(5):164–165. [PubMed] [Google Scholar]
  48. Yoon H., Miller S. P., Pabich E. K., Donahue T. F. SSL1, a suppressor of a HIS4 5'-UTR stem-loop mutation, is essential for translation initiation and affects UV resistance in yeast. Genes Dev. 1992 Dec;6(12B):2463–2477. doi: 10.1101/gad.6.12b.2463. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES