Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1991 Jun;10(6):1317–1324. doi: 10.1002/j.1460-2075.1991.tb07650.x

Differential targeting of the tobacco PR-1 pathogenesis-related proteins to the extracellular space and vacuoles of crystal idioblasts.

D C Dixon 1, J R Cutt 1, D F Klessig 1
PMCID: PMC452789  PMID: 2026137

Abstract

Several biochemical and localization studies have shown that the acidic isoforms of the tobacco pathogenesis-related (PR) proteins, PR-1a, -1b and -1c are secreted to the extracellular spaces of leaves in response to pathogen infection or chemical treatment. Here we report the differential accumulation of these proteins within the vacuoles of specialized cells known as crystal idioblasts. In situ hybridization analysis indicated that crystal idioblasts expressed the PR-1 genes at the mRNA level and suggested that PR-1 proteins were synthesized by these cells. Transgenic plants which constitutively express a chimeric gene encoding an acidic PR-1b isoform also accumulated PR-1 protein in the extracellular spaces and within crystal idioblast vacuoles. Analysis of mRNA derived from these transgenic plants indicated that expression of the introduced PR-1b gene was responsible for the accumulation of PR-1 protein in these two distinct locations. The synthesis and accumulation within crystal idioblasts of PR-1 proteins, which are secreted by other cell types, indicates that idioblasts sort these proteins in a unique manner. Moreover, this suggests that protein sorting in higher plants may be modulated in a cell specific manner.

Full text

PDF
1317

Images in this article

Selected References

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

  1. Baker D., Wuestehube L., Schekman R., Botstein D., Segev N. GTP-binding Ypt1 protein and Ca2+ function independently in a cell-free protein transport reaction. Proc Natl Acad Sci U S A. 1990 Jan;87(1):355–359. doi: 10.1073/pnas.87.1.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bednarek S. Y., Wilkins T. A., Dombrowski J. E., Raikhel N. V. A carboxyl-terminal propeptide is necessary for proper sorting of barley lectin to vacuoles of tobacco. Plant Cell. 1990 Dec;2(12):1145–1155. doi: 10.1105/tpc.2.12.1145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bol J. F., van Kan J. A. The synthesis and possible functions of virus-induced proteins in plants. Microbiol Sci. 1988 Feb;5(2):47–52. [PubMed] [Google Scholar]
  4. Bowles D. J. Defense-related proteins in higher plants. Annu Rev Biochem. 1990;59:873–907. doi: 10.1146/annurev.bi.59.070190.004301. [DOI] [PubMed] [Google Scholar]
  5. Bulcke M. V., Bauw G., Castresana C., Van Montagu M., Vandekerckhove J. Characterization of vacuolar and extracellular beta(1,3)-glucanases of tobacco: Evidence for a strictly compartmentalized plant defense system. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2673–2677. doi: 10.1073/pnas.86.8.2673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burgess T. L., Kelly R. B. Constitutive and regulated secretion of proteins. Annu Rev Cell Biol. 1987;3:243–293. doi: 10.1146/annurev.cb.03.110187.001331. [DOI] [PubMed] [Google Scholar]
  7. Carr J. P., Dixon D. C., Klessig D. F. Synthesis of pathogenesis-related proteins in tobacco is regulated at the level of mRNA accumulation and occurs on membrane-bound polysomes. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7999–8003. doi: 10.1073/pnas.82.23.7999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carr J. P., Dixon D. C., Nikolau B. J., Voelkerding K. V., Klessig D. F. Synthesis and localization of pathogenesis-related proteins in tobacco. Mol Cell Biol. 1987 Apr;7(4):1580–1583. doi: 10.1128/mcb.7.4.1580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cornelissen B. J., Hooft van Huijsduijnen R. A., Van Loon L. C., Bol J. F. Molecular characterization of messenger RNAs for 'pathogenesis related' proteins la, lb and lc, induced by TMV infection of tobacco. EMBO J. 1986 Jan;5(1):37–40. doi: 10.1002/j.1460-2075.1986.tb04174.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cornelissen B. J., Horowitz J., van Kan J. A., Goldberg R. B., Bol J. F. Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucleic Acids Res. 1987 Sep 11;15(17):6799–6811. doi: 10.1093/nar/15.17.6799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cutt J. R., Dixon D. C., Carr J. P., Klessig D. F. Isolation and nucleotide sequence of cDNA clones for the pathogenesis-related proteins PR1a, PR1b and PR1c of Nicotiana tabacum cv. Xanthi nc induced by TMV infection. Nucleic Acids Res. 1988 Oct 25;16(20):9861–9861. doi: 10.1093/nar/16.20.9861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cutt J. R., Harpster M. H., Dixon D. C., Carr J. P., Dunsmuir P., Klessig D. F. Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. Virology. 1989 Nov;173(1):89–97. doi: 10.1016/0042-6822(89)90224-9. [DOI] [PubMed] [Google Scholar]
  13. Johnson L. M., Bankaitis V. A., Emr S. D. Distinct sequence determinants direct intracellular sorting and modification of a yeast vacuolar protease. Cell. 1987 Mar 13;48(5):875–885. doi: 10.1016/0092-8674(87)90084-5. [DOI] [PubMed] [Google Scholar]
  14. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol. 1989;5:483–525. doi: 10.1146/annurev.cb.05.110189.002411. [DOI] [PubMed] [Google Scholar]
  15. Linthorst H. J., van Loon L. C., van Rossum C. M., Mayer A., Bol J. F., van Roekel J. S., Meulenhoff E. J., Cornelissen B. J. Analysis of acidic and basic chitinases from tobacco and petunia and their constitutive expression in transgenic tobacco. Mol Plant Microbe Interact. 1990 Jul-Aug;3(4):252–258. doi: 10.1094/mpmi-3-252. [DOI] [PubMed] [Google Scholar]
  16. Mauch F., Staehelin L. A. Functional Implications of the Subcellular Localization of Ethylene-Induced Chitinase and [beta]-1,3-Glucanase in Bean Leaves. Plant Cell. 1989 Apr;1(4):447–457. doi: 10.1105/tpc.1.4.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Memelink J., Linthorst H. J., Schilperoort R. A., Hoge J. H. Tobacco genes encoding acidic and basic isoforms of pathogenesis-related proteins display different expression patterns. Plant Mol Biol. 1990 Feb;14(2):119–126. doi: 10.1007/BF00018553. [DOI] [PubMed] [Google Scholar]
  18. Pelham H. R., Hardwick K. G., Lewis M. J. Sorting of soluble ER proteins in yeast. EMBO J. 1988 Jun;7(6):1757–1762. doi: 10.1002/j.1460-2075.1988.tb03005.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rudolph H. K., Antebi A., Fink G. R., Buckley C. M., Dorman T. E., LeVitre J., Davidow L. S., Mao J. I., Moir D. T. The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Cell. 1989 Jul 14;58(1):133–145. doi: 10.1016/0092-8674(89)90410-8. [DOI] [PubMed] [Google Scholar]
  20. Sambrook J. F. The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell. 1990 Apr 20;61(2):197–199. doi: 10.1016/0092-8674(90)90798-j. [DOI] [PubMed] [Google Scholar]
  21. Schmitt H. D., Puzicha M., Gallwitz D. Study of a temperature-sensitive mutant of the ras-related YPT1 gene product in yeast suggests a role in the regulation of intracellular calcium. Cell. 1988 May 20;53(4):635–647. doi: 10.1016/0092-8674(88)90579-x. [DOI] [PubMed] [Google Scholar]
  22. Tague B. W., Dickinson C. D., Chrispeels M. J. A short domain of the plant vacuolar protein phytohemagglutinin targets invertase to the yeast vacuole. Plant Cell. 1990 Jun;2(6):533–546. doi: 10.1105/tpc.2.6.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Valls L. A., Hunter C. P., Rothman J. H., Stevens T. H. Protein sorting in yeast: the localization determinant of yeast vacuolar carboxypeptidase Y resides in the propeptide. Cell. 1987 Mar 13;48(5):887–897. doi: 10.1016/0092-8674(87)90085-7. [DOI] [PubMed] [Google Scholar]

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

RESOURCES