Abstract
Tomato cultivars with different tolerance to NaCl were analysed for basal endogenous jasmonate (JAs) content, and its changes in response to salt-stress. Steady-state levels of JA and related compounds were higher in the salt-tolerant cv. Pera than in cv. Hellfrucht Frühstamm (HF) and JA levels in both cultivars changed in response to salt-stress. A steady JA increase was observed in cv. HF from the beginning of salinisation, while in cv. Pera, JA level decreased after 24 h of salt treatment. These results support the hypothesis that changes in endogenous JA in response to stress are different in genotypes of contrasting salt tolerance. The effects of salinity were then studied on lipoxygenase (LOX) protein accumulation, transcripts of allene oxide synthase (AOS) and proteinase inhibitor II (Pin2), and activities of diacylglycerol kinase (DAG-k) and phosphatidate kinase (PA-k) (enzymes involved in the phosphatidic acid (PA) and diacylglycerol pyrophosphate (DGPP) metabolism). The accumulation of a high molecular weight LOX-like protein was more pronounced in salt treated-plants of cv. HF, although both cultivars responded to exogenous JA treatment by increasing LOX accumulation. AOS-mRNA and Pin2-mRNA had also accumulated after 6 h of NaCl and JA treatments. An increase in the phosphorylation of phospholipids PA and DGPP was evident in cv. Pera, indicating that DAG-k and PA-k were highly activated by salt treatment only in this cultivar. Thus, the difference in the lipid kinase activities between both cultivars may be related to the process of salt stress tolerance rather than to JA synthesis.
Similar content being viewed by others
References
Abdala G., Miersch O., Kramell R., Vigliocco A., Agostini E., Forchetti G. and Alemano S.2003. Jasmonate and octadecanoid occurrence in tomato hairy roots. Endogenous level changes in response to NaCl. Plant Growth Regul.40 (1):21-27.
Balboa M.A., Balsinde J., Dillon D.A., Carman G.M. and Dennis E.A.1999. Proinflammatory macrophage-activating properties of the novel phospholipid diacylglycerol pyrophosphate. J. Biol. Chem.274:522-526.
Bohlmann H.1994. The role of thionins in plant protection. Crit. Rev. Plant Sci.13:1-16.
Bradford M.M.1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.72:248-254.
Chapman K.D.1998. Phospholipase activity during plant growth and development and in response to environmental stress. Trends Plant Sci.3:419-426.
Creelman R.A. and Mullet J.E.1997. Oligosaccharins, brassinolides and jasmonates:nontraditional regulators of plant growth, development, and gene expression. Plant Cell9:1211-1223.
Epple P., Apel K. and Bohlmann H.1997. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell9:509-520.
Farmer E.E. and Ryan C.A.1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell4:129-134.
Feussner I. and Wasternack C.1998. Lipoxygenase catalyzed oxygenation of lipids. Fett/Lipid100:146-152.
Feussner I., Hause B., Vörös K., Parthier B. and Wasternack C.1995. Jasmonate-induced lipoxygenase forms are localized in chloroplasts of barley (Hordeum vulgare cv. Salome) leaves. Plant J.7:949-957.
Flowers T.J. and Yeo A.R.1986. Ion relations of plants under drought and salinity. Aust. J. Plant Physiol.13:75-91.
Hause B., Stenzel I., Miersch O., Maucher H., Kramell R., Ziegler J. and Wasternack C.2000. Tissue-specific oxylipin signature of tomato flowers:allene oxide cyclase is highly expressed in distintic flower organs and vascular bundles. Plant J.24:113-126.
Ishiguro S., Kawai-Oda A., Ueda J., Nishida I. and Okada K.2001. The defective in anther dehiscence1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell13:2191-2209.
Kindl H.1997. The oxygen-dependent modification of triacylglycerols and phospholipids, the different way of initiating lipid body mobilization. Z. Naturforsch.52c:1-8.
Kramell R., Atzorn R., Schneider G., Miersch O., Brückner C., Schmidt J., Sembdner G. and Parthier B.1995. Occurrence and identification of jasmonic acid and its amino acid conjugates induced by osmotic stress in barley leaf tissue. J. Plant Growth Regul.14:29-36.
Kramell R., Miersch O., Atzorn R., Parthier B. and Wasternack C.2000. Octadecanoid-derived alteration of gene expression and the 'oxylipin signature 'in stressed barley leaves. Implications for different signaling pathways. Plant Physiol.123:177-187.
Laudert D. and Weiler E.W.1998. Allene oxide synthase:a major control point in Arabidopsis thaliana octadecanoid signallig. Plant J.15:675-684.
Lee S., Suh S., Kim S., Crain R.C., Kwak J.M., Nam H. and Lee Y.1997. Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J.12:547-556.
Lehmann J., Atzorn R., Brückner C., Reinbothe S., Leopold J., Wasternack C. and Parthier B.1995. Accumulation of jasmonate, abscisic acid, specific transcripts and proteins in osmotically stressed barley leaf segments. Planta197:156-162.
McConn M., Creelman R.A., Bell F., Mullet J.E. and Browse J.1997. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A.94:5473-5477.
McPhail L.C., Waite K.A., Regier D.S., Nixon J.B., Qualliotine-Mann D., Zhang W.X., Wallin R. and Sergeant S.1999. A novel protein kinase target for the lipid second messenger phosphatidic acid. Biochim. Biophys. Acta1439:277-290.
Miersch O. and Wasternack C.2000. Octadecanoid and jasmonate signaling in tomato (Lycopersicon esculentum Mill.) leaves:endogenous jasmonates do not induce jasmonate biosynthesis. Biol. Chem.381:715-722.
Moons A., Prinsen E., Bauw G. and Van Montagu M.1997. Antagonistic effects on abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell9:2243-2259.
Munnik T., Meijer H.J.G., Riet B., Hirt H., Frank W., Bartels D. and Musgrave A.2000. Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J.22:1-8.
Munnik T.2001. Phosphatidic acid:an emerging plant lipid second messenger. Trends Plant Sci.6:227-233.
Narváez-Vásquez J., Florin-Christensen J. and Ryan C.A.1999. Positional specificity of a phospholipase A activity induced by wounding, systemin and oligosaccharide elicitors in tomato leaves. Plant Cell11:2249-2260.
Peña-Cortés H. and Willmitzer L.1995. The role of hormones in gene activation in response to wounding. In:Davies P.J. (ed.), Plant Hormones:Physiology, Biochemistry and Molecular Biology. Kluwer Academic Publishers, Dordrecht, pp. 395-414.
Pérez Alfocea F., Estañ M.T., Caro M. and Bolarín M.C.1993. Response of tomato cultivars to salinity. Plant and Soil150:203-211.
Racagni G., García de Lema M., Domenech C. and Machado-Domenech E.E.1992. Phospholipids in Trypanosoma cruzi:Phosphoinositide composition and turnover. Lipids27:275-278.
Racagni G., Pedranzani H., Alemano S., Taleisnik E., Abdala G. and Machado-Domenech E.2003. Effect of short-term salinity on lipid metabolism and ion accumulation in tomato roots. Biologia Plant(in press).
Ryu S.B. and Wang X.1996. Activation of phospholipase D and the possible mechanism of activation in wound-induced lipid hydrolysis in castor leaves. Biochim. Biophys. Acta1303:243-250.
Ryu S.B. and Wang X.1998. Increases in free linolenic and linoleic acids associated with phospholipase D-mediated hydrolysis of phospholipids in wounded castor bean leaves. Biochim. Biophys. Acta1393:193-202.
Sembdner G. and Parthier B.1993. The biochemistry and the physiological and molecular actions of Jasmonates. Ann. Rev. Plant Physiol. Plant Mol. Biol.44:569-589.
Sivasankar S., Sheldrick B. and Rothstein S.2000. Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol.122:1335-1342.
Topham M.K. and Prescott S.M.1999. Mammalian diacylglycerol kinases, a family of lipid kinases with signaling functions. J. Biol. Chem.274:11447-11450.
Wang X.1997. Molecular analysis of phospholipase D. Trends. Plant Sci.261-266.
Wang X.1999. The role of phospholipase D in signaling cascade. Plant Physiol.120:645-651.
Wasternack C. and Parthier B.1997. Jasmonate signalled plant gene expression. Trends Plant Sci.2:302-307.
Wasternack C. and Hause B.2002. Jasmonates and octadecanoids–signals in plant stress response and development. In:Moldave K. (ed.), Progress in Nucleic Acid Research and Molecular Biology, Academic Press, New York Vol. 72, pp. 165-221.
Wissing J.B. and Berhbohm H.1993. Diacylglycerol pyrophosphate, a novel phospholipid compound. FEBS Lett.315:95-99.
Xu Y., Chang P.L., Liu D., Narasimhan M.L., Raghothama K.G., Hasegawa P.M. and Bressan R.A.1994. Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell6:1077-1085.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pedranzani, H., Racagni, G., Alemano, S. et al. Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regulation 41, 149–158 (2003). https://doi.org/10.1023/A:1027311319940
Issue Date:
DOI: https://doi.org/10.1023/A:1027311319940