Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-24T05:20:18.655Z Has data issue: false hasContentIssue false
  • English
  • Français

Endogenous jasmonates and octadecanoids in hypersensitive tomato mutants during germination and seedling development in response to abiotic stress

Published online by Cambridge University Press:  22 February 2007

Andrea Andrade ,
Ana Vigliocco ,
Sergio Alemano ,
Otto Miersch ,
Miguel A. Botella  and
Guillermina Abdala
Andrea Andrade
Affiliation:
Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, 5800-Río Cuarto, Argentina
Ana Vigliocco
Affiliation:
Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, 5800-Río Cuarto, Argentina
Sergio Alemano
Affiliation:
Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, 5800-Río Cuarto, Argentina
Otto Miersch
Affiliation:
Institut für Pflanzenbiochemie, Weinberg, 3, 06120-Halle, Germany
Miguel A. Botella
Affiliation:
Departamento de Biología Molecular y Bioquímica, Universidad de Málaga, 29071, Málaga, España
Guillermina Abdala*
Affiliation:
Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, 5800-Río Cuarto, Argentina
*
*Correspondence: Fax: +54 358 4676230 Email: gabdala@exa.unrc.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

Although jasmonates (JAs) are involved in germination and seedling development, the regulatory mechanism of JAs, and their relation with endogenous level modifications in these processes, is not well understood. We report here the detection of 12-oxo-phytodienoic acid (OPDA), jasmonic acid (JA), 11-hydroxyjasmonate (11-OH-JA), 12-hydroxyjasmonate (12-OH-JA) and methyljasmonate (JAME) in unimbibed seeds and seedlings of tomato Lycopersicon esculentum Mill cv. Moneymaker (wild type) and tss1, tss2, tos1 mutants. The main compounds in wild-type and tss1, tss2, tos1 seeds were the hydroxylate-JAs; 12-OH-JA was the major component in dry seeds of the wild type and in tss2 and tos1. The amounts of these derivatives were higher in seeds than in seedlings. Changes in JAs during wild-type and tss1 imbibition were analysed in seeds and the imbibition water. In wild-type imbibed seeds, 11-OH-JA content was higher than in tss1. 12-OH-JA showed a different tendency with respect to 11-OH-JA, with high levels in the wild type at early imbibition. In tss1, levels of 12-OH-JA rose from 24 to 48 h of imbibition. At 72 h of imbibition, when radicles had emerged, the amounts of both hydroxylates in wild-type and tss1 seeds were minimal. An important release of the hydroxylate forms was observed in the imbibition water. 11-OH-JA decreased in the imbibition water of wild-type seeds at 48 h. On the contrary, a high and sustained liberation of this compound was observed in tss1 after 24 h. 12-OH-JA increased in wild-type as well in tss1 until 24 h. Thereafter, a substantial reduction in the content of this compound was registered. NaCl-treated wild-type seedlings increased their 12-OH-JA, but tss1 seedlings increased their JA in response to salt treatment. In tss2 seedlings, NaCl caused a slight decrease in 11-OH-JA and JAME, whereas tos1 seedlings showed a dramatic OPDA and 12-OH-JA decrease in response to salt treatment. Under salt stress the mutant seedlings showed different patterns of JAs according to their differential hypersensitivity to abiotic stress. The JA-hydroxylate forms found, and the differential accumulation of JAs during germination, imbibition and seedling development, as well as their response to NaCl stress, provide new evidence about the control of many developmental processes by JA.

Keywords

germinationjasmonatesLycopersicon esculentumNaCl stressseedling developmenttomato mutants
Type
Research Article
Information
Seed Science Research , Volume 15 , Issue 4 , December 2005 , pp. 309 - 318
Copyright
Copyright © Cambridge University Press 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdala, G., Castro, G., Guiñazú, M., Tizio, R. and Miersch, O. (1996) Occurrence of jasmonic acid in organs of Solanum tuberosum L. and its effect on tuberization. Plant Growth Regulation 19, 139–143.CrossRefGoogle Scholar
Abdala, G., Castro, G., Miersch, O. and Pearce, D. (2002) Changes in jasmonate and gibberellin levels during development of potato plants (Solanum tuberosum L.). Plant Growth Regulation 36, 121–126.CrossRefGoogle Scholar
Berger, S., Bell, E. and Mullet, J.E. (1996) Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiology 111, 525–531.Google Scholar
Borsani, O., Cuartero, J., Fernández, J.A., Valpuesta, V. and Botella, M.A. (2001) Identification of two loci in tomato reveals distinct mechanisms for salt tolerance. Plant Cell 13, 873–888.CrossRefGoogle ScholarPubMed
Borsani, O., Cuartero, J., Valpuesta, V. and Botella, M.A. (2002) Tomato tos1 mutation identifies a gene essential for osmotic tolerance and abscisic acid sensitivity. Plant Journal 32, 905–914.CrossRefGoogle ScholarPubMed
Cenzano, A.M., Vigliocco, A., Miersch, O. and Abdala, G. (2005) Octadecanoid levels during stolon to tuber transition in potato Potato ResearchGoogle Scholar
Corbineau, F., Rudnicki, R.M. and Come, D. (1988) The effects of methyl jasmonate on sunflower (Helianthus annuus L.) seed germination and seedling development. Plant Growth Regulation 7, 157–169.CrossRefGoogle Scholar
Creelman, R.A. and Mullet, J.E. (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proceedings of the National Academy of Sciences, USA 92, 4114–4119.CrossRefGoogle ScholarPubMed
Creelman, R.A. and Mullet, J.E. (1997) Oligosaccharins, brassinolides and jasmonates: nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9, 1211–1223.CrossRefGoogle ScholarPubMed
Ellis, C. and Turner, J.G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13, 1025–1033.Google Scholar
Feys, B.J.F., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751–759.CrossRefGoogle Scholar
Gidda, S.K., Miersch, O., Levitin, A., Schmidt, J., Wasternack, C. and Varin, L. (2003) Biochemical and molecular characterization of a hydroxyjasmonate sulfotransferase from Arabidopsis thaliana. Journal of Biological Chemistry 278, 17895–17900.CrossRefGoogle ScholarPubMed
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 distinct flower organs and vascular bundles. Plant Journal 24, 113–126.Google Scholar
Helder, H., Miersch, O., Vreugdenhil, D. and Sembdner, G. (1993) Occurrence of hydroxylated jasmonic acids in leaflets of Solanum demissum plants grown under long- and short-day conditions. Physiologia Plantarum 88, 647–653.CrossRefGoogle ScholarPubMed
Hilpert, B., Bohlmann, H. op, den, Camp, R., Przybyla, D., Miersch, O., Buchala, A. and Apel, K. (2001) Isolation and characterization of signal transduction mutants of Arabidopsis thaliana that constitutively activate the octadecanoid pathway and form necrotic microlesions. Plant Journal 26, 435–446.Google Scholar
Kepczynski, J. and Bialecka, B. (1994) Stimulatory effect of ethephon, ACC, gibberellin A 3 and A 4+7 on germination of methyl jasmonate inhibited Amaranthus caudatus L. seeds. Plant Growth Regulation 14, 211–216.Google Scholar
Koda, Y. (1992) The role of jasmonic acid and related compounds in the regulation of plant development. International Review of Cytology 135, 155–199.CrossRefGoogle ScholarPubMed
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 Physiology 123, 177–187.CrossRefGoogle ScholarPubMed
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. Planta 197, 156–162.CrossRefGoogle Scholar
Leung, J. and Giraudat, J. (1998) Abscisic acid signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 49, 199–222.CrossRefGoogle ScholarPubMed
Maucher, H., Hause, B., Feussner, I., Ziegler, J. and Wasternack, C. (2000) Allene oxide synthases of barley (Hordeum vulgare cv. Salome): tissue specific regulation in seedling development. Plant Journal 21, 199–213.CrossRefGoogle ScholarPubMed
McConn, M. and Browse, J. (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8, 403–416.CrossRefGoogle ScholarPubMed
Miersch, O., Schneider, G. and Sembdner, G. (1991) Hydroxylated jasmonic acid and related compounds from Botryodiplodia theobromae. Phytochemistry 30, 4049–4051.CrossRefGoogle Scholar
Miersch, O., Knöfel, H.D., Schmidt, J., Kramell, R. and Parthier, B. (1998) A jasmonic acid conjugate, N[(?)-jasmonoyl]-tyramine, from Petunia pollen. Phytochemistry 47, 327–329.CrossRefGoogle Scholar
Miersch, O., Weichert, H., Stenzel, I., Hause, B., Maucher, H., Feussner, I. and Wasternack, C. (2004) Constitutive overexpression of allene oxide cyclase in tomato (Lycopersicon esculentum cv. Lukullus) elevates levels of some jasmonates and octadecanoids in flower organs but not in leaves. Phytochemistry 65, 847–856.Google Scholar
Moller, S.G. and Chua, N.H. (1999) Interactions and intersections of plant signaling pathways. Journal of Molecular Biology 293, 219–234.Google Scholar
Nojavan-Asghari, M. and Ishizawa, K. (1998) Inhibitory effects of methyl jasmonate on the germination and ethylene production in cocklebur seeds. Journal of Plant Growth Regulation 17, 13–18.CrossRefGoogle Scholar
Parthier, B., Brückner, C., Dathe, W., Hause, B., Herrmann, G., Knöfel, H.D., Kramell, H.M., Kramell, R., Lehmann, J., Miersch, O., Reinbothe, S.T., Sembdner, G., Wasternack, C., Zur Nieden, U. (1992) Jasmonates: metabolism, biological activities, and modes of action in senescence and stress response. pp. 276–285. Karssen, C.M.;, van Loon, L.C.;, Vreugdenhil, D. (Eds) Progress in plant growth regulation. Dordrecht, Kluwer Academic.CrossRefGoogle Scholar
Pedranzani, H., Racagni, G., Alemano, S., Miersch, O., Ramírez, I., Peña-Cortés, H., Taleisnik, E., Machado-Domenech, E. and Abdala, G. (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regulation 41, 149–158.CrossRefGoogle Scholar
Richmond, T.A. and Bleeker, A.B. (1999) A defect in β-oxidation causes abnormal inflorescence development in Arabidopsis. Plant Cell 11, 1911–1923.Google ScholarPubMed
Sanders, P.M., Lee, P.Y., Biesgen, C., Boone, J.D., Beals, T.P., Weiler, E.W. and Goldberg, R.B. (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12, 1041–1062.Google Scholar
Schaller, F., Biesgen, C., Müssig, C., Altmann, T. and Weiler, E.W. (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210, 979–984.CrossRefGoogle ScholarPubMed
Sembdner, G. and Gross, D. (1986) Plant growth substances of plant and microbial origin. pp. 139–147. Bopp, M. (Ed.) Plant growth substances. Berlin, Springer-Verlag.Google Scholar
Sembdner, G. and Parthier, B. (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annual Review of Plant Physiology and Plant Molecular Biology 44, 569–589.CrossRefGoogle Scholar
Sembdner, G., Meyer, A., Miersch, O., Brückner, C. (1990) Metabolism of jasmonic acid. pp. 374–379. in Pharis, R.P.;, Rood, S.B. (Eds.) Plant growth subtances. New York, Springer-Verlag.Google Scholar
Stenzel, I., Hause, B., Maucher, H., Pitzschkle, A., Miersch, O., Ziegler, J., Ryan, C.A. and Wasternack, C. (2003a) Allene oxide cyclase dependence of the wound response and vascular bundle specific generation of jasmonates in tomato – amplification in wound-signaling. Plant Journal 33, 577–589.CrossRefGoogle Scholar
Stenzel, I., Hause, B., Miersch, O., Kurz, T., Maucher, H., Weichert, H., Ziegler, J., Feussner, I. and Wasternack, C. (2003b) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Molecular Biology 51, 895–911.CrossRefGoogle ScholarPubMed
Stenzel, I., Hause, B., Feussner, I. and Wasternack, C. (2003c) Transcriptional activation of jasmonate biosynthesis enzymes is not reflected at protein level. pp. in 267–270. Murata, N.;, Yamada, M.;, Nishida, I.;, Okuyama, H.;, Sekijar, J.;, Hajime, W. (Eds) Advanced research on plant lipids. Dordrecht, Kluwer Academic.CrossRefGoogle Scholar
Stintzi, A. and Browse, J. (2000c) The Arabidopsis male-sterile mutant opr3 lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proceedings of the National Academy of Sciences, USA 97, 10625–10630.Google Scholar
Wasternack, C. and Hause, B. (2002) Jasmonates and octadecanoids: Signals in plant stress responses and development. Progress in Nucleic Acid Research and Molecular Biology 72, 165–221.CrossRefGoogle ScholarPubMed
Wasternack, C. and Parthier, B. (1997) Jasmonate signalled plant gene expression. Trends in Plant Science 2, 302–307.CrossRefGoogle Scholar
Weber, H., Vick, B.A. and Farmer, E.E. (1997) Dinor-oxo-phytodienoic acid: a new hexadecanoid signal in the jasmonate familiy. Proceedings of the National Academy of Sciences, USA 94, 10473–10478.CrossRefGoogle Scholar
Weiler, E.W., Albrecht, T., Groth, B., Xia, Z.Q., Luxem, M., Liss, H., Andert, L. and Spengler, P. (1993) Evidence for the involvement of jasmonates and their octadecanoid precursors in the tendril coiling response of Bryonia dioica. Phytochemistry 32, 591–600.CrossRefGoogle Scholar
Xin, Z.Y., Zhou, X. and Pilet, P.E. (1997) Level changes of jasmonic, abscisic, and indole-3yl-acetic acids in maize under desiccation stress. Journal of Plant Physiology 151, 120–124.CrossRefGoogle Scholar
Xu, L., Liu, F., Wang, Z., Peng, W., Huang, R., Huang, D. and Xie, D. (2001) An Arabidopsis mutant cex1 exhibits constant accumulation of jasmonate-regulated AtVSP, Thi2.1 and PDF1.2. FEBS Letters 494, 161–164.CrossRefGoogle ScholarPubMed
Yamane, H., Takagi, H., Abe, H., Yokota, T. and Takahashi, N. (1981) Identification of jasmonic acid in three species of higher plants and its biological activities. Plant and Cell Physiology 22, 689–697.Google Scholar
Yoshihara, T., Omer, E.A., Koshino, H., Sakamura, S., Kikuta, Y. and Koda, Y. (1989) Structure of a tuber-inducing stimulus from potato leaves ( Solanum tuberosum L.). Agricultural and Biological Chemistry 53, 2835–2837.Google Scholar
Zhu, J.K. (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.Google Scholar
Zhu, J.K., Liu, J. and Xiong, L. (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10, 1181–1191.CrossRefGoogle ScholarPubMed
Ziegler, J., Stenzel, I., Hause, B., Maucher, H., Hamberg, M., Grimm, R., Ganal, M. and Wasternack, C. (2000) Molecular cloning of allene oxide cyclase – The enzyme establishing the stereochemistry of octadecanoids and jasmonates. Journal of Biological Chemistry 275, 19132–19138.Google Scholar