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. 1992 Sep;4(9):1123–1130. doi: 10.1105/tpc.4.9.1123

Calcium Requirement for Ethylene-Dependent Responses.

V Raz 1, R Fluhr 1
PMCID: PMC160202  PMID: 12297671

Abstract

Ethylene, a gaseous plant hormone, plays a role in plant development, defense, and climacteric fruit ripening. Both genetic and biochemical evidence suggest that the response of plants to ethylene is mediated by a specific ethylene receptor. The signal emanating from the receptor-effector complex is then presumably transduced via an unknown cascade pathway. We have used the plant pathogenesis response, exemplified by the induction of the pathogenesis-related gene chitinase, as a paradigm to investigate ethylene-dependent signal transduction in the plant cell. We showed that calcium is necessarily involved in the ethylene-mediated pathogenesis response. Blocking calcium fluxes with chelators inhibited ethylene-dependent induction of chitinase accumulation, but not ethylene independent induction. Artificially increasing cytosolic calcium levels by treatments with the calcium ionophore ionomycin or the calcium pump blocker thapsigargin stimulated chitinase accumulation. Plants grown in calcium-poor soil showed a 10-fold reduction in leaf extractable calcium. Their leaves exhibited a reduced pathogenesis reaction to ethylene and were impaired in another hormone response mediated by calcium, i.e., abscisic acid-controlled closure of guard cells. The addition of calcium to leaves excised from calcium-deficient plants restored their sensitivity to ethylene. Ethylene participates in the control of seedling growth, promoting the so-called "triple response" that results in distinct morphological development, such as hypocotyl hook formation. This effect, similar to the ethylene-promoted pathogenesis response, was found to be calcium dependent. The results indicate that calcium is required for a variety of ethylene-dependent processes.

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Selected References

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  1. 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]
  2. Ecker J. R., Davis R. W. Plant defense genes are regulated by ethylene. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5202–5206. doi: 10.1073/pnas.84.15.5202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Enyedi A. J., Yalpani N., Silverman P., Raskin I. Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2480–2484. doi: 10.1073/pnas.89.6.2480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eyal Y., Sagee O., Fluhr R. Dark-induced accumulation of a basic pathogenesis-related (PR-1) transcript and a light requirement for its induction by ethylene. Plant Mol Biol. 1992 Jul;19(4):589–599. doi: 10.1007/BF00026785. [DOI] [PubMed] [Google Scholar]
  5. Fuchs Y., Saxena A., Gamble H. R., Anderson J. D. Ethylene biosynthesis-inducing protein from cellulysin is an endoxylanase. Plant Physiol. 1989 Jan;89(1):138–143. doi: 10.1104/pp.89.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gilroy S., Hughes W. A., Trewavas A. J. A Comparison between Quin-2 and Aequorin as Indicators of Cytoplasmic Calcium Levels in Higher Plant Cell Protoplasts. Plant Physiol. 1989 Jun;90(2):482–491. doi: 10.1104/pp.90.2.482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goeschl J. D., Rappaport L., Pratt H. K. Ethylene as a factor regulating the growth of pea epicotyls subjected to physical stress. Plant Physiol. 1966 May;41(5):877–884. doi: 10.1104/pp.41.5.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Guzmán P., Ecker J. R. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell. 1990 Jun;2(6):513–523. doi: 10.1105/tpc.2.6.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Knight M. R., Campbell A. K., Smith S. M., Trewavas A. J. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature. 1991 Aug 8;352(6335):524–526. doi: 10.1038/352524a0. [DOI] [PubMed] [Google Scholar]
  10. Lee J. S., Mulkey T. J., Evans M. L. Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science. 1983 Jun 24;220(4604):1375–1376. doi: 10.1126/science.220.4604.1375. [DOI] [PubMed] [Google Scholar]
  11. Legrand M., Kauffmann S., Geoffroy P., Fritig B. Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6750–6754. doi: 10.1073/pnas.84.19.6750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Liu C., Hermann T. E. Characterization of ionomycin as a calcium ionophore. J Biol Chem. 1978 Sep 10;253(17):5892–5894. [PubMed] [Google Scholar]
  13. Lotan T., Fluhr R. Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway for induction. Plant Physiol. 1990 Jun;93(2):811–817. doi: 10.1104/pp.93.2.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Mason M. J., Garcia-Rodriguez C., Grinstein S. Coupling between intracellular Ca2+ stores and the Ca2+ permeability of the plasma membrane. Comparison of the effects of thapsigargin, 2,5-di-(tert-butyl)-1,4-hydroquinone, and cyclopiazonic acid in rat thymic lymphocytes. J Biol Chem. 1991 Nov 5;266(31):20856–20862. [PubMed] [Google Scholar]
  16. Mauch F., Hadwiger L. A., Boller T. Ethylene: Symptom, Not Signal for the Induction of Chitinase and beta-1,3-Glucanase in Pea Pods by Pathogens and Elicitors. Plant Physiol. 1984 Nov;76(3):607–611. doi: 10.1104/pp.76.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ozaki Y., Kume S. Functional responses of aequorin-loaded human neutrophils. Comparison with fura-2-loaded cells. Biochim Biophys Acta. 1988 Nov 18;972(2):113–119. doi: 10.1016/0167-4889(88)90109-7. [DOI] [PubMed] [Google Scholar]
  18. Poovaiah B. W., Reddy A. S. Calcium messenger system in plants. CRC Crit Rev Plant Sci. 1987;6(1):47–103. doi: 10.1080/07352688709382247. [DOI] [PubMed] [Google Scholar]
  19. Schönthal A., Sugarman J., Brown J. H., Hanley M. R., Feramisco J. R. Regulation of c-fos and c-jun protooncogene expression by the Ca(2+)-ATPase inhibitor thapsigargin. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7096–7100. doi: 10.1073/pnas.88.16.7096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Takahashi H., Scott T. K., Suge H. Stimulation of root elongation and curvature by calcium. Plant Physiol. 1992;98:246–252. doi: 10.1104/pp.98.1.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Takemura H., Hughes A. R., Thastrup O., Putney J. W., Jr Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane. J Biol Chem. 1989 Jul 25;264(21):12266–12271. [PubMed] [Google Scholar]
  22. Thastrup O., Cullen P. J., Drøbak B. K., Hanley M. R., Dawson A. P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466–2470. doi: 10.1073/pnas.87.7.2466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Trewavas A., Gilroy S. Signal transduction in plant cells. Trends Genet. 1991 Nov-Dec;7(11-12):356–361. doi: 10.1016/0168-9525(91)90255-o. [DOI] [PubMed] [Google Scholar]
  24. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Watowich S. S., Morimoto R. I. Complex regulation of heat shock- and glucose-responsive genes in human cells. Mol Cell Biol. 1988 Jan;8(1):393–405. doi: 10.1128/mcb.8.1.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zook M. N., Rush J. S., Kuć J. A. A role for ca in the elicitation of rishitin and lubimin accumulation in potato tuber tissue. Plant Physiol. 1987 Jun;84(2):520–525. doi: 10.1104/pp.84.2.520. [DOI] [PMC free article] [PubMed] [Google Scholar]

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