Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1994 Jul 15;13(14):3378–3388. doi: 10.1002/j.1460-2075.1994.tb06640.x

An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems.

M Van Lijsebettens 1, R Vanderhaeghen 1, M De Block 1, G Bauw 1, R Villarroel 1, M Van Montagu 1
PMCID: PMC395235  PMID: 7913892

Abstract

In Arabidopsis, mutation at PFL causes pointed first leaves, reduced fresh weight and growth retardation. We have cloned the wild-type PFL gene by T-DNA tagging, and demonstrate that it complements the mutant phenotype. PFL codes for ribosomal protein S18, based on the high homology with rat S18 and on purification of S18-equivalent peptides from plant ribosomes. pfl represents the first mutation in eukaryotic S18 proteins or their S13 prokaryotic counterparts, involved in translation initiation. Arabidopsis contains three S18 gene copies dispersed in the genetic map; they are all transcribed and code for completely identical proteins. No transcript is detected from the mutated gene, S18A. The activity of the S18A promoter is restricted to meristems, with a markedly high expression at the embryonic heart stage, and to wounding sites. This means that plants activate an extra copy of this ribosomal protein gene in tissues with cell division activity. We postulate that in meristematic tissues plants use transcriptional control to synthesize extra ribosomes to increase translational efficiency. In analogy with this, an additional, developmentally regulated gene copy might be expected for all ribosomal proteins.

Full text

PDF
3378

Images in this article

3379Image
on p.3379
3380Image
on p.3380
3383Image
on p.3383
3384Image
on p.3384

Selected References

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

  1. Alliotte T., Tiré C., Engler G., Peleman J., Caplan A., Van Montagu M., Inzé D. An Auxin-Regulated Gene of Arabidopsis thaliana Encodes a DNA-Binding Protein. Plant Physiol. 1989 Mar;89(3):743–752. doi: 10.1104/pp.89.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arnon D. I. COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. Plant Physiol. 1949 Jan;24(1):1–15. doi: 10.1104/pp.24.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bauw G., Rasmussen H. H., van den Bulcke M., van Damme J., Puype M., Gesser B., Celis J. E., Vandekerckhove J. Two-dimensional gel electrophoresis, protein electroblotting and microsequencing: a direct link between proteins and genes. Electrophoresis. 1990 Jul;11(7):528–536. doi: 10.1002/elps.1150110703. [DOI] [PubMed] [Google Scholar]
  4. Bonham-Smith P. C., Oancia T. L., Moloney M. M. Cytoplasmic ribosomal protein S15a from Brassica napus: molecular cloning and developmental expression in mitotically active tissues. Plant Mol Biol. 1992 Mar;18(5):909–919. doi: 10.1007/BF00019205. [DOI] [PubMed] [Google Scholar]
  5. Capel M. S., Bourque D. P. Characterization of Nicotiana tabacum chloroplast and cytoplasmic ribosomal proteins. J Biol Chem. 1982 Jul 10;257(13):7746–7755. [PubMed] [Google Scholar]
  6. Chan Y. L., Paz V., Wool I. G. The primary structure of rat ribosomal protein S18. Biochem Biophys Res Commun. 1991 Aug 15;178(3):1212–1218. doi: 10.1016/0006-291x(91)91022-5. [DOI] [PubMed] [Google Scholar]
  7. Chang C., Bowman J. L., DeJohn A. W., Lander E. S., Meyerowitz E. M. Restriction fragment length polymorphism linkage map for Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6856–6860. doi: 10.1073/pnas.85.18.6856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chassin D., Bellet D., Koman A. The human homolog of ribosomal protein S18. Nucleic Acids Res. 1993 Feb 11;21(3):745–745. doi: 10.1093/nar/21.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen I. T., Roufa D. J. The transcriptionally active human ribosomal protein S17 gene. Gene. 1988 Oct 15;70(1):107–116. doi: 10.1016/0378-1119(88)90109-6. [DOI] [PubMed] [Google Scholar]
  10. Davies B., Feo S., Heard E., Fried M. A strategy to detect and isolate an intron-containing gene in the presence of multiple processed pseudogenes. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6691–6695. doi: 10.1073/pnas.86.17.6691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Etter A., Aboutanos M., Tobler H., Müller F. Eliminated chromatin of Ascaris contains a gene that encodes a putative ribosomal protein. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1593–1596. doi: 10.1073/pnas.88.5.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fang R. X., Nagy F., Sivasubramaniam S., Chua N. H. Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell. 1989 Jan;1(1):141–150. doi: 10.1105/tpc.1.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fisher E. M., Beer-Romero P., Brown L. G., Ridley A., McNeil J. A., Lawrence J. B., Willard H. F., Bieber F. R., Page D. C. Homologous ribosomal protein genes on the human X and Y chromosomes: escape from X inactivation and possible implications for Turner syndrome. Cell. 1990 Dec 21;63(6):1205–1218. doi: 10.1016/0092-8674(90)90416-c. [DOI] [PubMed] [Google Scholar]
  14. Goldberg R. B., Barker S. J., Perez-Grau L. Regulation of gene expression during plant embryogenesis. Cell. 1989 Jan 27;56(2):149–160. doi: 10.1016/0092-8674(89)90888-x. [DOI] [PubMed] [Google Scholar]
  15. Grill E., Somerville C. Construction and characterization of a yeast artificial chromosome library of Arabidopsis which is suitable for chromosome walking. Mol Gen Genet. 1991 May;226(3):484–490. doi: 10.1007/BF00260662. [DOI] [PubMed] [Google Scholar]
  16. Hamilton B. A., Palazzolo M. J., Meyerowitz E. M. Rapid isolation of long cDNA clones from existing libraries. Nucleic Acids Res. 1991 Apr 25;19(8):1951–1952. doi: 10.1093/nar/19.8.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jones J. D., Dunsmuir P., Bedbrook J. High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J. 1985 Oct;4(10):2411–2418. doi: 10.1002/j.1460-2075.1985.tb03949.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kamalay J. C., Goldberg R. B. Regulation of structural gene expression in tobacco. Cell. 1980 Apr;19(4):935–946. doi: 10.1016/0092-8674(80)90085-9. [DOI] [PubMed] [Google Scholar]
  20. Kim Y., Zhang H., Scholl R. L. Two evolutionarily divergent genes encode a cytoplasmic ribosomal protein of Arabidopsis thaliana. Gene. 1990 Sep 14;93(2):177–182. doi: 10.1016/0378-1119(90)90222-d. [DOI] [PubMed] [Google Scholar]
  21. Koncz C., Németh K., Rédei G. P., Schell J. T-DNA insertional mutagenesis in Arabidopsis. Plant Mol Biol. 1992 Dec;20(5):963–976. doi: 10.1007/BF00027166. [DOI] [PubMed] [Google Scholar]
  22. Kongsuwan K., Yu Q., Vincent A., Frisardi M. C., Rosbash M., Lengyel J. A., Merriam J. A Drosophila Minute gene encodes a ribosomal protein. Nature. 1985 Oct 10;317(6037):555–558. doi: 10.1038/317555a0. [DOI] [PubMed] [Google Scholar]
  23. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  24. Lake J. A. Evolving ribosome structure: domains in archaebacteria, eubacteria, eocytes and eukaryotes. Annu Rev Biochem. 1985;54:507–530. doi: 10.1146/annurev.bi.54.070185.002451. [DOI] [PubMed] [Google Scholar]
  25. Larkin J. C., Hunsperger J. P., Culley D., Rubenstein I., Silflow C. D. The organization and expression of a maize ribosomal protein gene family. Genes Dev. 1989 Apr;3(4):500–509. doi: 10.1101/gad.3.4.500. [DOI] [PubMed] [Google Scholar]
  26. MacMurray A. J., Shin H. S. The murine MHC encodes a mammalian homolog of bacterial ribosomal protein S13. Mamm Genome. 1992;2(2):87–95. doi: 10.1007/BF00353855. [DOI] [PubMed] [Google Scholar]
  27. Mason H. S., Mullet J. E., Boyer J. S. Polysomes, Messenger RNA, and Growth in Soybean Stems during Development and Water Deficit. Plant Physiol. 1988 Mar;86(3):725–733. doi: 10.1104/pp.86.3.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Moore P. B. Structure-function correlations in the small ribosomal subunit from Escherichia coli. Annu Rev Biophys Biophys Chem. 1988;17:349–367. doi: 10.1146/annurev.bb.17.060188.002025. [DOI] [PubMed] [Google Scholar]
  29. Patel R., Jacobs-Lorena M. Generation of Minute phenotypes by a transformed antisense ribosomal protein gene. Dev Genet. 1992;13(4):256–263. doi: 10.1002/dvg.1020130403. [DOI] [PubMed] [Google Scholar]
  30. Poethig R. S. Phase change and the regulation of shoot morphogenesis in plants. Science. 1990 Nov 16;250(4983):923–930. doi: 10.1126/science.250.4983.923. [DOI] [PubMed] [Google Scholar]
  31. Porter A. C., Chernajovsky Y., Dale T. C., Gilbert C. S., Stark G. R., Kerr I. M. Interferon response element of the human gene 6-16. EMBO J. 1988 Jan;7(1):85–92. doi: 10.1002/j.1460-2075.1988.tb02786.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pruitt R. E., Meyerowitz E. M. Characterization of the genome of Arabidopsis thaliana. J Mol Biol. 1986 Jan 20;187(2):169–183. doi: 10.1016/0022-2836(86)90226-3. [DOI] [PubMed] [Google Scholar]
  33. Radin J. W. Responses of transpiration and hydraulic conductance to root temperature in nitrogen- and phosphorus-deficient cotton seedlings. Plant Physiol. 1990 Mar;92(3):855–857. doi: 10.1104/pp.92.3.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rychlik W., Spencer W. J., Rhoads R. E. Optimization of the annealing temperature for DNA amplification in vitro. Nucleic Acids Res. 1990 Nov 11;18(21):6409–6412. doi: 10.1093/nar/18.21.6409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schuster A. M., Davies E. Ribonucleic Acid and Protein Metabolism in Pea Epicotyls : II. Response to Wounding in Aged Tissue. Plant Physiol. 1983 Nov;73(3):817–821. doi: 10.1104/pp.73.3.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smith L. G., Hake S. The Initiation and Determination of Leaves. Plant Cell. 1992 Sep;4(9):1017–1027. doi: 10.1105/tpc.4.9.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sonenberg N. Translation factors as effectors of cell growth and tumorigenesis. Curr Opin Cell Biol. 1993 Dec;5(6):955–960. doi: 10.1016/0955-0674(93)90076-3. [DOI] [PubMed] [Google Scholar]
  39. Stafstrom J. P., Sussex I. M. Expression of a ribosomal protein gene in axillary buds of pea seedlings. Plant Physiol. 1992 Nov;100(3):1494–1502. doi: 10.1104/pp.100.3.1494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Warner J. R. Synthesis of ribosomes in Saccharomyces cerevisiae. Microbiol Rev. 1989 Jun;53(2):256–271. doi: 10.1128/mr.53.2.256-271.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES