Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 May 9;92(10):4138–4144. doi: 10.1073/pnas.92.10.4138

Involvement of small GTP-binding proteins in defense signal-transduction pathways of higher plants.

H Sano 1, Y Ohashi 1
PMCID: PMC41900  PMID: 11607540

Abstract

Small GTP-binding proteins play a critical role in the regulation of a range of cellular processes--including growth, differentiation, and intracellular transportation. Previously, we isolated a gene, rgp1, encoding a small GTP-binding protein, by differential screening of a rice cDNA library with probe DNAs from rice tissues treated with or without 5-azacytidine, a powerful inhibitor of DNA methylation. To determine the physiological role of rgp1, the coding region was introduced into tobacco plants. Transformants, with rgp1 in either sense or antisense orientations, showed distinct phenotypic changes with reduced apical dominance, dwarfism, and abnormal flower development. These abnormal phenotypes appeared to be associated with the higher levels of endogenous cytokinins that were 6-fold those of wild-type plants. In addition, the transgenic plants produced salicylic acid and salicylic acid-beta-glucoside in an unusual response to wounding, thus conferring increased resistance to tobacco mosaic virus infection. In normal plants, the wound- and pathogen-induced signal-transduction pathways are considered to function independently. However, the wound induction of salicylic acid in the transgenic plants suggests that expression of rgp1 somehow interfered with the normal signaling pathways and resulted in cross-signaling between these distinct transduction systems. The results imply that the defense signal-transduction system consists of a complicated and finely tuned network of several regulatory factors, including cytokinins, salicylic acid, and small GTP-binding proteins.

Full text

PDF
4138

Images in this article

4139Fig. 1
on p.4139
4140Fig. 2
on p.4140
4142Fig. 3
on p.4142
4143Fig. 4
on p.4143

Selected References

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

  1. Alexander D., Goodman R. M., Gut-Rella M., Glascock C., Weymann K., Friedrich L., Maddox D., Ahl-Goy P., Luntz T., Ward E. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7327–7331. doi: 10.1073/pnas.90.15.7327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balch W. E. Biochemistry of interorganelle transport. A new frontier in enzymology emerges from versatile in vitro model systems. J Biol Chem. 1989 Oct 15;264(29):16965–16968. [PubMed] [Google Scholar]
  3. Barbacid M. ras genes. Annu Rev Biochem. 1987;56:779–827. doi: 10.1146/annurev.bi.56.070187.004023. [DOI] [PubMed] [Google Scholar]
  4. Bishop P. D., Pearce G., Bryant J. E., Ryan C. A. Isolation and characterization of the proteinase inhibitor-inducing factor from tomato leaves. Identity and activity of poly- and oligogalacturonide fragments. J Biol Chem. 1984 Nov 10;259(21):13172–13177. [PubMed] [Google Scholar]
  5. Blumenkrantz N., Asboe-Hansen G. New method for quantitative determination of uronic acids. Anal Biochem. 1973 Aug;54(2):484–489. doi: 10.1016/0003-2697(73)90377-1. [DOI] [PubMed] [Google Scholar]
  6. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991 Jan 10;349(6305):117–127. doi: 10.1038/349117a0. [DOI] [PubMed] [Google Scholar]
  7. Brederode F. T., Linthorst H. J., Bol J. F. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol. 1991 Dec;17(6):1117–1125. doi: 10.1007/BF00028729. [DOI] [PubMed] [Google Scholar]
  8. Brogue K., Chet I., Holliday M., Cressman R., Biddle P., Knowlton S., Mauvais C. J., Broglie R. Transgenic Plants with Enhanced Resistance to the Fungal Pathogen Rhizoctonia solani. Science. 1991 Nov 22;254(5035):1194–1197. doi: 10.1126/science.254.5035.1194. [DOI] [PubMed] [Google Scholar]
  9. Cordero M. J., Raventós D., San Segundo B. Expression of a maize proteinase inhibitor gene is induced in response to wounding and fungal infection: systemic wound-response of a monocot gene. Plant J. 1994 Aug;6(2):141–150. doi: 10.1046/j.1365-313x.1994.6020141.x. [DOI] [PubMed] [Google Scholar]
  10. Damsky C. H., Werb Z. Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr Opin Cell Biol. 1992 Oct;4(5):772–781. doi: 10.1016/0955-0674(92)90100-q. [DOI] [PubMed] [Google Scholar]
  11. Darvill A., Augur C., Bergmann C., Carlson R. W., Cheong J. J., Eberhard S., Hahn M. G., Ló V. M., Marfà V., Meyer B. Oligosaccharins--oligosaccharides that regulate growth, development and defence responses in plants. Glycobiology. 1992 Jun;2(3):181–198. doi: 10.1093/glycob/2.3.181. [DOI] [PubMed] [Google Scholar]
  12. Davis K. R., Darvill A. G., Albersheim P., Dell A. Host-Pathogen Interactions : XXIX. Oligogalacturonides Released from Sodium Polypectate by Endopolygalacturonic Acid Lyase Are Elicitors of Phytoalexins in Soybean. Plant Physiol. 1986 Feb;80(2):568–577. doi: 10.1104/pp.80.2.568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dietrich A., Mayer J. E., Hahlbrock K. Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. J Biol Chem. 1990 Apr 15;265(11):6360–6368. [PubMed] [Google Scholar]
  14. Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
  15. Farmer E. E., Moloshok T. D., Saxton M. J., Ryan C. A. Oligosaccharide signaling in plants. Specificity of oligouronide-enhanced plasma membrane protein phosphorylation. J Biol Chem. 1991 Feb 15;266(5):3140–3145. [PubMed] [Google Scholar]
  16. Farmer E. E., Pearce G., Ryan C. A. In vitro phosphorylation of plant plasma membrane proteins in response to the proteinase inhibitor inducing factor. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1539–1542. doi: 10.1073/pnas.86.5.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Farmer E. E., Ryan C. A. Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. Plant Cell. 1992 Feb;4(2):129–134. doi: 10.1105/tpc.4.2.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Feig L. A. The many roads that lead to Ras. Science. 1993 May 7;260(5109):767–768. doi: 10.1126/science.8484117. [DOI] [PubMed] [Google Scholar]
  19. Felix G., Grosskopf D. G., Regenass M., Boller T. Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8831–8834. doi: 10.1073/pnas.88.19.8831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Felix G., Regenass M., Spanu P., Boller T. The protein phosphatase inhibitor calyculin A mimics elicitor action in plant cells and induces rapid hyperphosphorylation of specific proteins as revealed by pulse labeling with [33P]phosphate. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):952–956. doi: 10.1073/pnas.91.3.952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gruenbaum Y., Naveh-Many T., Cedar H., Razin A. Sequence specificity of methylation in higher plant DNA. Nature. 1981 Aug 27;292(5826):860–862. doi: 10.1038/292860a0. [DOI] [PubMed] [Google Scholar]
  22. Hall A. The cellular functions of small GTP-binding proteins. Science. 1990 Aug 10;249(4969):635–640. doi: 10.1126/science.2116664. [DOI] [PubMed] [Google Scholar]
  23. Hayashi T., Yoshida K. Cell expansion and single-cell separation induced by colchicine in suspension-cultured soybean cells. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2618–2622. doi: 10.1073/pnas.85.8.2618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jacinto T., Farmer E. E., Ryan C. A. Purification of Potato Leaf Plasma Membrane Protein pp34, a Protein Phosphorylated in Response to Oligogalacturonide Signals for Defense and Development. Plant Physiol. 1993 Dec;103(4):1393–1397. doi: 10.1104/pp.103.4.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Juliano R. L., Haskill S. Signal transduction from the extracellular matrix. J Cell Biol. 1993 Feb;120(3):577–585. doi: 10.1083/jcb.120.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kahn R. A., Der C. J., Bokoch G. M. The ras superfamily of GTP-binding proteins: guidelines on nomenclature. FASEB J. 1992 May;6(8):2512–2513. doi: 10.1096/fasebj.6.8.1592203. [DOI] [PubMed] [Google Scholar]
  27. Kaziro Y., Itoh H., Kozasa T., Nakafuku M., Satoh T. Structure and function of signal-transducing GTP-binding proteins. Annu Rev Biochem. 1991;60:349–400. doi: 10.1146/annurev.bi.60.070191.002025. [DOI] [PubMed] [Google Scholar]
  28. Legendre L., Rueter S., Heinstein P. F., Low P. S. Characterization of the Oligogalacturonide-Induced Oxidative Burst in Cultured Soybean (Glycine max) Cells. Plant Physiol. 1993 May;102(1):233–240. doi: 10.1104/pp.102.1.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lever M. A new reaction for colorimetric determination of carbohydrates. Anal Biochem. 1972 May;47(1):273–279. doi: 10.1016/0003-2697(72)90301-6. [DOI] [PubMed] [Google Scholar]
  30. Malamy J., Carr J. P., Klessig D. F., Raskin I. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990 Nov 16;250(4983):1002–1004. doi: 10.1126/science.250.4983.1002. [DOI] [PubMed] [Google Scholar]
  31. Marshall M. S. The effector interactions of p21ras. Trends Biochem Sci. 1993 Jul;18(7):250–254. doi: 10.1016/0968-0004(93)90175-m. [DOI] [PubMed] [Google Scholar]
  32. Melançon P., Glick B. S., Malhotra V., Weidman P. J., Serafini T., Gleason M. L., Orci L., Rothman J. E. Involvement of GTP-binding "G" proteins in transport through the Golgi stack. Cell. 1987 Dec 24;51(6):1053–1062. doi: 10.1016/0092-8674(87)90591-5. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Mohnen D., Eberhard S., Marfà V., Doubrava N., Toubart P., Gollin D. J., Gruber T. A., Nuri W., Albersheim P., Darvill A. The control of root, vegetative shoot and flower morphogenesis in tobacco thin cell-layer explants (TCLs). Development. 1990 Jan;108(1):191–201. doi: 10.1242/dev.108.1.191. [DOI] [PubMed] [Google Scholar]
  35. Métraux J. P., Signer H., Ryals J., Ward E., Wyss-Benz M., Gaudin J., Raschdorf K., Schmid E., Blum W., Inverardi B. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science. 1990 Nov 16;250(4983):1004–1006. doi: 10.1126/science.250.4983.1004. [DOI] [PubMed] [Google Scholar]
  37. Pena-Cortes H., Willmitzer L., Sanchez-Serrano J. J. Abscisic Acid Mediates Wound Induction but Not Developmental-Specific Expression of the Proteinase Inhibitor II Gene Family. Plant Cell. 1991 Sep;3(9):963–972. doi: 10.1105/tpc.3.9.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Raskin I. Salicylate, a new plant hormone. Plant Physiol. 1992 Jul;99(3):799–803. doi: 10.1104/pp.99.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ridley A. J., Hall A. Signal transduction pathways regulating Rho-mediated stress fibre formation: requirement for a tyrosine kinase. EMBO J. 1994 Jun 1;13(11):2600–2610. doi: 10.1002/j.1460-2075.1994.tb06550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sano H., Seo S., Orudgev E., Youssefian S., Ishizuka K. Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10556–10560. doi: 10.1073/pnas.91.22.10556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sano H., Youssefian S. A novel ras-related rgp1 gene encoding a GTP-binding protein has reduced expression in 5-azacytidine-induced dwarf rice. Mol Gen Genet. 1991 Aug;228(1-2):227–232. doi: 10.1007/BF00282470. [DOI] [PubMed] [Google Scholar]
  42. Shinshi H., Mohnen D., Meins F. Regulation of a plant pathogenesis-related enzyme: Inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc Natl Acad Sci U S A. 1987 Jan;84(1):89–93. doi: 10.1073/pnas.84.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Smart C. M., Scofield S. R., Bevan M. W., Dyer T. A. Delayed Leaf Senescence in Tobacco Plants Transformed with tmr, a Gene for Cytokinin Production in Agrobacterium. Plant Cell. 1991 Jul;3(7):647–656. doi: 10.1105/tpc.3.7.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Terryn N., Arias M. B., Engler G., Tiré C., Villarroel R., Van Montagu M., Inzé D. rha1, a gene encoding a small GTP binding protein from Arabidopsis, is expressed primarily in developing guard cells. Plant Cell. 1993 Dec;5(12):1761–1769. doi: 10.1105/tpc.5.12.1761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Terryn N., Van Montagu M., Inzé D. GTP-binding proteins in plants. Plant Mol Biol. 1993 Apr;22(1):143–152. doi: 10.1007/BF00039002. [DOI] [PubMed] [Google Scholar]
  46. Yalpani N., Leon J., Lawton M. A., Raskin I. Pathway of Salicylic Acid Biosynthesis in Healthy and Virus-Inoculated Tobacco. Plant Physiol. 1993 Oct;103(2):315–321. doi: 10.1104/pp.103.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Yoshida K., Nagano Y., Murai N., Sasaki Y. Phytochrome-regulated expression of the genes encoding the small GTP-binding proteins in peas. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6636–6640. doi: 10.1073/pnas.90.14.6636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. van Loon L. C., van Kammen A. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. "Samsun" and "Samsun NN". II. Changes in protein constitution after infection with tobacco mosaic virus. Virology. 1970 Feb;40(2):190–211. doi: 10.1016/0042-6822(70)90395-8. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES