View More View Less
  • 1 Hungarian Academy of Sciences Plant Protection Institute, Centre for Agricultural Research Herman Ottó út 15 H-1022 Budapest Hungary
Restricted access

Purchase article

USD  $20.00

1 year subscription (Individual Only)

USD  $542.00

The monoterpenoid (S)-carvone was shown earlier to induce glutathione S-transferase (GST) activity and to attenuate necrotic lesion formation in Tobacco mosaic virus (TMV) inoculated, hypersensitively reacting tobacco Xanthi-nc plants. To explore structure-activity relationships, three monoterpenes and five monoterpenoids were tested for their ability to induce increased GST activity in tobacco leaf discs. (S)-Carvone proved to be the most potent inducer. (S)-Carvone treatments markedly up-regulated the expression of several tobacco GST genes belonging to the phi, tau and theta classes, particularly in the case of tau class GSTs. Furthermore, TMV inoculation slightly induced the transcript abundance of the GSTT2 gene. The expression of three catalase (CAT) genes was also examined in (S)-carvone-treated tobacco leaf discs. The expression of CAT1 was not influenced by (S)-carvone treatments, whereas that of CAT2 was significantly repressed. (S)-Carvone very weakly induced the transcription of the CAT3 gene. The effect of the opposite enantiomer, (R)-carvone on the expression of GST and CAT genes was similar to that of (S)-carvone. Our results suggest that the antioxidative reactions catalyzed by tau and theta class GSTs contribute to the attenuation of necrotic disease symptoms in TMV-inoculated tobacco plants.

  • Aebi, H. (1984): Catalase in vitro. Methods Enzymol. 105, 121–126.

    Aebi H. , 'Catalase in vitro ' (1984 ) 105 Methods Enzymol. : 121 -126.

  • Allan, A. C., Lapidot, M., Culver, J. N. and Fluhr, R. (2001): An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiol. 126, 97–108.

    Fluhr R. , 'An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein ' (2001 ) 126 Plant Physiol. : 97 -108.

    • Search Google Scholar
  • Ashida, Y., Matsushima, A., Hirota, T., Watanabe, J. and Hirata, T. (2002): Geraniol-inducible glutathione S-transferase in cultured soybean cells. Biosci. Biotechnol. Biochem. 66, 168–170.

    Hirata T. , 'Geraniol-inducible glutathione S-transferase in cultured soybean cells ' (2002 ) 66 Biosci. Biotechnol. Biochem. : 168 -170.

    • Search Google Scholar
  • Bartling, D., Radzio, R., Steiner, U. and Weiler, E. W. (1993): A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. Eur. J. Biochem. 216, 579–586.

    Weiler E. W. , 'A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization ' (1993 ) 216 Eur. J. Biochem. : 579 -586.

    • Search Google Scholar
  • Bendahmane, A., Kanyuka, K. and Baulcombe, D. C. (1999): The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11, 781–791.

    Baulcombe D. C. , 'The Rx gene from potato controls separate virus resistance and cell death responses ' (1999 ) 11 Plant Cell : 781 -791.

    • Search Google Scholar
  • Bouwmeester, H. J., Gershenzon, J., Konings, M. C. J. M. and Croteau, R. (1998): Biosynthesis of the monoterpenes limonene and carvone in the fruit of caraway. I. Demonstration of enzyme activities and their changes with development. Plant Physiol. 117, 901–912.

    Croteau R. , 'Biosynthesis of the monoterpenes limonene and carvone in the fruit of caraway. I. Demonstration of enzyme activities and their changes with development ' (1998 ) 117 Plant Physiol. : 901 -912.

    • Search Google Scholar
  • Chen, I. H., Chiu, M. H., Cheng, S. F., Hsu, Y. H. and Tsai, C. H. (2013): The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic virus. New Phytol. 199, 749–757.

    Tsai C. H. , 'The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic virus ' (2013 ) 199 New Phytol. : 749 -757.

    • Search Google Scholar
  • Chen, Z., Silva, H. and Klessig, D. F. (1993): Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262, 1883–1886.

    Klessig D. F. , 'Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid ' (1993 ) 262 Science : 1883 -1886.

    • Search Google Scholar
  • Dean, J. D., Goodwin, P. H. and Hsiang, T. (2005): Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J. Exp. Bot. 56, 1525–1533.

    Hsiang T. , 'Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance ' (2005 ) 56 J. Exp. Bot. : 1525 -1533.

    • Search Google Scholar
  • Dixon, D. P., Davis, B. G. and Edwards, R. (2002): Functional divergence in the glutathione transferase superfamily in plants: identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 277, 30859–30869.

    Edwards R. , 'Functional divergence in the glutathione transferase superfamily in plants: identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana ' (2002 ) 277 J. Biol. Chem. : 30859 -30869.

    • Search Google Scholar
  • Dixon, D. P. and Edwards, R. (2009): Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J. Biol. Chem. 284, 21249–21256.

    Edwards R. , 'Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases ' (2009 ) 284 J. Biol. Chem. : 21249 -21256.

    • Search Google Scholar
  • Dixon, D. P., Hawkins, T., Hussey, P. J. and Edwards, R. (2009): Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J. Exp. Bot. 60, 1207–1218.

    Edwards R. , 'Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily ' (2009 ) 60 J. Exp. Bot. : 1207 -1218.

    • Search Google Scholar
  • Dixon, D. P., Sellars, J. D. and Edwards, R. (2011): The Arabidopsis phi class glutathione transferase AtGSTF2: binding and regulation by biologically active heterocyclic ligands. Biochem. J. 438, 63–70.

    Edwards R. , 'The Arabidopsis phi class glutathione transferase AtGSTF2: binding and regulation by biologically active heterocyclic ligands ' (2011 ) 438 Biochem. J. : 63 -70.

    • Search Google Scholar
  • Doke, N. and Ohashi, Y. (1988): Involvement of an O2 generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol. Mol. Plant Pathol. 32, 163–175.

    Ohashi Y. , 'Involvement of an O2− generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus ' (1988 ) 32 Physiol. Mol. Plant Pathol. : 163 -175.

    • Search Google Scholar
  • Dorey, S., Baillieul, F., Saindrenan, P., Fritig, B. and Kauffmann, S. (1998): Tobacco class I and II catalases are differentially expressed during elicitor induced hypersensitive cell death and localized acquired resistance. Mol. Plant-Microbe Interact. 11, 1102–1109.

    Kauffmann S. , 'Tobacco class I and II catalases are differentially expressed during elicitor induced hypersensitive cell death and localized acquired resistance ' (1998 ) 11 Mol. Plant-Microbe Interact. : 1102 -1109.

    • Search Google Scholar
  • Durner, J. and Klessig, D. F. (1996): Salicylic acid is a modulator of tobacco and mammalian catalases. J. Biol. Chem. 271, 28492–28501.

    Klessig D. F. , 'Salicylic acid is a modulator of tobacco and mammalian catalases ' (1996 ) 271 J. Biol. Chem. : 28492 -28501.

    • Search Google Scholar
  • Edwards, R., Dixon, D. P. and Walbot, V. (2000): Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5, 193–198.

    Walbot V. , 'Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health ' (2000 ) 5 Trends Plant Sci. : 193 -198.

    • Search Google Scholar
  • Farkas, G. L., Király, Z. and Solymosy, F. (1960): Role of oxidative metabolism in the localization of plant viruses. Virology 12, 408–421.

    Solymosy F. , 'Role of oxidative metabolism in the localization of plant viruses ' (1960 ) 12 Virology : 408 -421.

    • Search Google Scholar
  • Fodor, J., Gullner, G., Ádám, A. L., Barna, B., Kőmíves, T. and Király, Z. (1997): Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Role in systemic acquired resistance. Plant Physiol. 114, 1443–1451.

    Király Z. , 'Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Role in systemic acquired resistance ' (1997 ) 114 Plant Physiol. : 1443 -1451.

    • Search Google Scholar
  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993): Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756.

    Ryals J. , 'Requirement of salicylic acid for the induction of systemic acquired resistance ' (1993 ) 261 Science : 754 -756.

    • Search Google Scholar
  • Gechev, T., Gadjev, I., Van Breusegem, F., Inzé, D., Dukiandjiev, S., Toneva, V. and Minkov, I. (2002): Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell. Mol. Life Sci. 59, 708–714.

    Minkov I. , 'Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes ' (2002 ) 59 Cell. Mol. Life Sci. : 708 -714.

    • Search Google Scholar
  • Gullner, G., Tóbiás, I., Fodor, J. and Kőmíves, T. (1999): Elevation of glutathione level and activation of glutathione-related enzymes affect virus infection in tobacco. Free Rad. Res. 31S, 155–161.

    Kőmíves T. , 'Elevation of glutathione level and activation of glutathione-related enzymes affect virus infection in tobacco ' (1999 ) 31S Free Rad. Res. : 155 -161.

    • Search Google Scholar
  • Gullner, G. and Kőmíves, T. (2001): The role of glutathione and glutathione-related enzymes in plant-pathogen interactions. In: D. Grill, M. Tausz and L. J. De Kok (eds): Significance of Glutathione in Plant Adaptation to the Environment. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 207–239.

    Kőmíves T. , '', in Significance of Glutathione in Plant Adaptation to the Environment , (2001 ) -.

    • Search Google Scholar
  • Hafez, Y. M., Bacsó, R., Király, Z., Künstler, A. and Király, L. (2012): Upregulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms. Phytopathology 102, 848–856.

    Király L. , 'Upregulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms ' (2012 ) 102 Phytopathology : 848 -856.

    • Search Google Scholar
  • Huchelmann, A., Gastaldo, C., Veinante, M., Zeng, Y., Heintz, D., Tritsch, D., Schaller, H., Rohmer, M., Bach, T. J. and Hemmerlin, A. (2014): S-Carvone suppresses cellulase-induced capsidiol production in Nicotiana tabacum by interfering with protein isoprenylation. Plant Physiol. 164, 935–950.

    Hemmerlin A. , 'S-Carvone suppresses cellulase-induced capsidiol production in Nicotiana tabacum by interfering with protein isoprenylation ' (2014 ) 164 Plant Physiol. : 935 -950.

    • Search Google Scholar
  • Kilili, K. G., Atanassova, N., Vardanyan, A., Clatot, N., Al-Sabarna, K., Kanellopoulos, P. N., Makris, A. M. and Kampranis, S. C. (2004): Differential roles of tau class glutathione S-transferases in oxidative stress. J. Biol. Chem. 279, 24540–24551.

    Kampranis S. C. , 'Differential roles of tau class glutathione S-transferases in oxidative stress ' (2004 ) 279 J. Biol. Chem. : 24540 -24551.

    • Search Google Scholar
  • Király, L. and Király, Z. (2006): To die or not to die — is cell death dispensable for resistance during the plant hypersensitive response? Acta Phytopathol. et Entomol. Hung. 41, 11–21.

    Király Z. , 'To die or not to die — is cell death dispensable for resistance during the plant hypersensitive response? ' (2006 ) 41 Acta Phytopathol. et Entomol. Hung. : 11 -21.

    • Search Google Scholar
  • Király, L., Künstler, A., Fattinger, M., Höller, K., Juhász, C., Müller, M., Gullner, G. and Zechmann, B. (2012): Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response. Plant Physiol. Biochem. 59, 44–54.

    Zechmann B. , 'Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response ' (2012 ) 59 Plant Physiol. Biochem. : 44 -54.

    • Search Google Scholar
  • Künstler, A., Hafez, Y. M. and Király, L. (2007a): Transient suppression of a catalase and an alternative oxidase gene during virus-induced local lesion formation (hypersensitive response) is independent of the extent of leaf necrotization. Acta Phytopathol. et Entomol. Hung. 42, 185–196.

    Király L. , 'Transient suppression of a catalase and an alternative oxidase gene during virus-induced local lesion formation (hypersensitive response) is independent of the extent of leaf necrotization ' (2007 ) 42 Acta Phytopathol. et Entomol. Hung. : 185 -196.

    • Search Google Scholar
  • Künstler, A., Király, L., Pogány, M., Tóbiás, I. and Gullner, G. (2007b): Lipoxygenase and glutathione peroxidase activity in tobacco leaves inoculated with Tobacco mosaic virus. Acta Phytopathol. et Entomol. Hung. 42, 197–207.

    Gullner G. , 'Lipoxygenase and glutathione peroxidase activity in tobacco leaves inoculated with Tobacco mosaic virus ' (2007 ) 42 Acta Phytopathol. et Entomol. Hung. : 197 -207.

    • Search Google Scholar
  • Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. (1994): H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583–593.

    Lamb C. , 'H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response ' (1994 ) 79 Cell : 583 -593.

    • Search Google Scholar
  • Mauch, F. and Dudler, R. (1993): Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol. 102, 1193–1201.

    Dudler R. , 'Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack ' (1993 ) 102 Plant Physiol. : 1193 -1201.

    • Search Google Scholar
  • Mittler, R., Feng, X. and Cohen, M. (1998): Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell. 10, 461–473.

    Cohen M. , 'Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco ' (1998 ) 10 Plant Cell. : 461 -473.

    • Search Google Scholar
  • Mittler, R., Lam, E., Shulaev, V. and Cohen, M. (1999): Signals controlling the expression of cytosolic ascorbate peroxidase during pathogen-induced programmed cell death in tobacco. Plant Mol. Biol. 39, 1025–1035.

    Cohen M. , 'Signals controlling the expression of cytosolic ascorbate peroxidase during pathogen-induced programmed cell death in tobacco ' (1999 ) 39 Plant Mol. Biol. : 1025 -1035.

    • Search Google Scholar
  • Oosterhaven, K., Hartmans, K. J. and Huizing, H. J. (1993): Inhibition of potato (Solanum tuberosum) sprout growth by the monoterpene S-carvone: reduction of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity without effect on its mRNA level. J. Plant Physiol. 141, 463–469.

    Huizing H. J. , 'Inhibition of potato (Solanum tuberosum) sprout growth by the monoterpene S-carvone: reduction of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity without effect on its mRNA level ' (1993 ) 141 J. Plant Physiol. : 463 -469.

    • Search Google Scholar
  • Oosterhaven, K., Hartmans, K. J., Scheffer, J. J. C. and van der Plas, L. H. W. (1995a): Inhibitory effect of S-carvone on wound healing of potato tuber tissue. Physiol. Plant 93, 225–232.

    van der Plas L. H. W. , 'Inhibitory effect of S-carvone on wound healing of potato tuber tissue ' (1995 ) 93 Physiol. Plant : 225 -232.

    • Search Google Scholar
  • Oosterhaven, K., Hartmans, K. J., Scheffer, J. J. C. and van der Plas, L. H. W. (1995b): S-Carvone inhibits phenylalanine ammonia lyase (PAL) activity and suberization during wound healing of potato tubers. J. Plant Physiol. 146, 288–294.

    van der Plas L. H. W. , 'S-Carvone inhibits phenylalanine ammonia lyase (PAL) activity and suberization during wound healing of potato tubers ' (1995 ) 146 J. Plant Physiol. : 288 -294.

    • Search Google Scholar
  • Portoghese, P. S., Kedziora, G. S., Larson, D. L., Bernard, B. K. and Hall, R. L. (1989): Reactivity of glutathione with α,β-unsaturated ketone flavouring substances. Food Chem. Toxicol. 27, 773–776.

    Hall R. L. , 'Reactivity of glutathione with α,β-unsaturated ketone flavouring substances ' (1989 ) 27 Food Chem. Toxicol. : 773 -776.

    • Search Google Scholar
  • Taylor, J. L., Fritzemeier, K. H., Häuser, I., Kombrink, E., Rohwer, F., Schröder, M., Strittmatter, G. and Hahlbrock, K. (1990): Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato. Mol. Plant-Microbe Interact. 3, 72–77.

    Hahlbrock K. , 'Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato ' (1990 ) 3 Mol. Plant-Microbe Interact. : 72 -77.

    • Search Google Scholar
  • Thangavelu, M., Belostotsky, D., Bevan, M. W., Flavell, R. B., Rogers, H. J. and Lonsdale, D. M. (1993): Partial characterization of the Nicotiana tabacum actin gene family: evidence for pollen-specific expression of one of the gene family members. Mol. Gen. Genet. 240, 290–295.

    Lonsdale D. M. , 'Partial characterization of the Nicotiana tabacum actin gene family: evidence for pollen-specific expression of one of the gene family members ' (1993 ) 240 Mol. Gen. Genet. : 290 -295.

    • Search Google Scholar
  • van der Zaal, E. J., Droog, F. N., Boot, C. J., Hensgens, L. A., Hoge, J. H., Schilperoort, R. A. and Libbenga, K. R. (1991): Promoters of auxin-induced genes from tobacco can lead to auxin-inducible and root tip-specific expression. Plant Mol. Biol. 16, 983–998.

    Libbenga K. R. , 'Promoters of auxin-induced genes from tobacco can lead to auxin-inducible and root tip-specific expression ' (1991 ) 16 Plant Mol. Biol. : 983 -998.

    • Search Google Scholar
  • Wagner, U., Edwards, R., Dixon, D. P. and Mauch, F. (2002): Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515–532.

    Mauch F. , 'Probing the diversity of the Arabidopsis glutathione S-transferase gene family ' (2002 ) 49 Plant Mol. Biol. : 515 -532.

    • Search Google Scholar
  • Whitham, S., McCormick, S. and Baker, B. (1996): The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc. Natl. Acad. Sci. USA 93, 8776–8781.

    Baker B. , 'The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato ' (1996 ) 93 Proc. Natl. Acad. Sci. USA : 8776 -8781.

    • Search Google Scholar
  • Willekens, H., Langebartels, C., Tiré, C., Van Montagu, M., Inzé, D. and Van Camp, W. (1994): Differential expression of catalase genes in Nicotiana plumbaginifolia (L.). Proc. Natl. Acad. Sci. USA 91, 10450–10454.

    Van Camp W. , 'Differential expression of catalase genes in Nicotiana plumbaginifolia (L.) ' (1994 ) 91 Proc. Natl. Acad. Sci. USA : 10450 -10454.

    • Search Google Scholar
  • Yi, S.-Y., Yu, S.-H. and Choi, D. (1999): Molecular cloning of a catalase cDNA from Nicotiana glutinosa L. and its repression by tobacco mosaic virus infection. Mol. Cells 9, 320–325.

    Choi D. , 'Molecular cloning of a catalase cDNA from Nicotiana glutinosa L. and its repression by tobacco mosaic virus infection ' (1999 ) 9 Mol. Cells : 320 -325.

    • Search Google Scholar
  • Yu, D., Xie, Z., Chen, C., Fan, B. and Chen, Z. (1999): Expression of tobacco class II catalase gene activates the endogenous homologous gene and is associated with disease resistance in transgenic potato plants. Plant Mol. Biol. 39, 477–488.

    Chen Z. , 'Expression of tobacco class II catalase gene activates the endogenous homologous gene and is associated with disease resistance in transgenic potato plants ' (1999 ) 39 Plant Mol. Biol. : 477 -488.

    • Search Google Scholar
  • Zheng, G.-Q., Kenney, P. M. and Lam, L. K. T. (1992): Effects of carvone compounds on glutathione S-transferase activity in A/J mice. J. Agric. Food Chem. 40, 751–755.

    Lam L. K. T. , 'Effects of carvone compounds on glutathione S-transferase activity in A/J mice ' (1992 ) 40 J. Agric. Food Chem. : 751 -755.

    • Search Google Scholar