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Plant function and evolutionary biology
RESEARCH ARTICLE

Systemic effects on leaf glutathione metabolism and defence protein expression caused by esca infection in grapevines

Christophe Valtaud A , Christine H. Foyer B , Pierrette Fleurat-Lessard A and Andrée Bourbouloux A C
+ Author Affiliations
- Author Affiliations

A Université de Poitiers, Laboratoire de Physiologie et Biochimie Végétales, UMR-CNRS 6161, Bâtiment Botanique, 40 Avenue du Recteur Pineau, F-86022 Poitiers, France.

B School of Agriculture, Food and Rural Development, Agriculture Building, The University of Newcastle upon Tyne, Newcastle upon Tyne, NE1 7RU, United Kingdom.

C Corresponding author. Email: andree.bourbouloux@univ-poitiers.fr

Functional Plant Biology 36(3) 260-279 https://doi.org/10.1071/FP08293
Submitted: 14 November 2008  Accepted: 12 January 2009   Published: 2 March 2009

Abstract

Esca is a devastating disease of Vitis vinifera L., caused by fungal pathogen(s) inhabiting the wood. The pathogens induce symptoms in the foliage, which are associated with structural and biochemical changes in leaves. The present study was undertaken to examine the effects of the disease on leaf glutathione metabolism in field-grown plants. The glutathione pool decreased and defence proteins such as PR-proteins and chitinases were expressed in the leaves before the appearance of visible symptoms in esca-infected canes. Glutathione depletion was increased as the disease developed in the leaves. The ratio of glutathione disulfide (GSSG) to the total glutathione pool was slightly decreased in leaves without visible symptoms, but it was significantly increased as the disease progressed. The abundance of γ-glutamylcysteine synthetase (γ-ECS) transcripts and of γ-ECS protein was greatly decreased in leaves exhibiting esca symptoms. Although glutathione reductase and glutathione peroxidase transcripts were largely unchanged by the spread of the esca disease, leaf glutathione S-transferase (GST) activities, the amounts of mRNAs encoding GSTU1 and GSTF2 and the abundance of the GSTU1 and GSTF2 proteins were highest at the early stages of infection and then decreased as visible symptoms appeared in the leaves. The GSTF2 protein, which was more abundant than GSTU1, was found in the nucleus and in the cytoplasm, whereas the GSTU1 protein was found largely in the plastids. These data demonstrate that the fungi involved in the esca disease induce pronounced systemic effects in the leaves before the appearance of visible damage. We conclude that the expression of GSTs, the extent of glutathione accumulation and the ratio of GSSG to total glutathione are early indicators of the presence of the esca disease in grapevine canes and thus these parameters can be used as stress markers in field-grown vines.

Additional keywords: esca disease, glutathione S-transferases, PR-proteins, redox status, Vitis vinifera.


Acknowledgements

The authors are grateful to Dr DP Dixon (School of Biological and Biomedical Sciences, University of Durham, UK) for the gift of antibodies directed against GSTs. They also wish to thank E Béré and G Théry in ‘Service Interdisciplinaire de Microscopie et d’Imagerie Scientifiques’ (UFR SFA, University of Poitiers) and F Thibault, M Vachaud and JM Pérault for technical assistance. This work was supported by the firm CLS Rémy-Cointreau, 20 rue Société Vinicole, BP 37, 16102 Cognac cedex, and CNRS (UMR 6161) (contract n°781263).


References


Afifi M, El-Kereamy A, Legrand V, Chervin C, Monje MC, Nepveu F, Roustan JP (2003) Control of anthocyanin biosynthesis pathway gene expression by eutypine, a toxin from Eutypa lata, in grape cell tissue cultures. Journal of Plant Physiology 160, 971–975.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Alvarez ME, Pennell RI, Meijer P, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediate mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ardi R, Kobiler I, Jacoby B, Keen NT, Prusky D (1998) Involvement of epicatechin biosynthesis in the activation of the mechanism of resistance of avocado fruits to Colletotrichum gloeosporioides. Physiological and Molecular Plant Pathology 53, 269–285.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Aziz A, Poinssot B, Daire X, Adrian M, Bézier A, Lambert B, Joubert JM, Pugin A (2003) Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Molecular Plant-Microbe Interactions 16, 1118–1128.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bergmann L , Rennenberg H (1993) Glutathione metabolism in plants. In ‘Sulfur nutrition and assimilation in higher plants’. (Ed. LJ de Kok) pp. 109–123. (SPB Academic Publishing, The Hague, the Nederlands)

Bézier A , Lambert B , Baillieul F (2002 a) Molecular cloning of grapevine glutathione S-transferase mRNA induced by grapevine in response to Botrytis cinerea infection. Submitted to EMBL/GenBank/DDBJ databases.

Bézier A, Lambert B, Baillieul F (2002b) Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. European Journal of Plant Pathology 108, 111–120.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bialczyk J, Lechowski Z, Libik A (1999) The protective action of tannins against glasshouse whitefly in tomato seedlings. Journal of Agricultural Science 133, 197–201.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Busam C, Kassemeyer H, Matern U (1997) Differential expression of chitinases in Vitis vinifera L. responding to systemic acquired resistance activators or fungal challenge. Plant Physiology 115, 1029–1038.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113–116.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chen S, Dickman MB (2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. Journal of Experimental Botany 55, 2617–2623.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Christen D, Tharin M, Perrin-Cherrioux S, Abou-Mansour E, Tabacchi R, Defago G (2005) Transformation of Eutypa dieback and esca disease pathogen toxins by antagonistic fungal strains reveals a second detoxification pathway not present in Vitis vinifera. Journal of Agricultural and Food Chemistry 53, 7043–7051.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cos P, DeBruyne T, Hermans N, Apers S, Berghe DV, Vlietinck AJ (2004) Proanthocyanidins in health care: current and new trends. Current Medicinal Chemistry 11, 1345–1359.
CAS | PubMed |
open url image1

Creissen G, Firmin J, Fryer M, Kular B, Leyland N , et al . (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. The Plant Cell 11, 1277–1291.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dangl J, Jones J (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basis domain/leucine zipper transcription factor TGA1. The Plant Cell 15, 2181–2191.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dixon DP, Cole DJ, Edwards R (1998) Purification, regulation and cloning of a glutathione transferase (GST) from maize resembling the auxin-inducible type-III GSTs. Plant Molecular Biology 36, 75–87.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biology 3, reviews3004.1–reviews3004.10.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins-a final frontier in flavonoid research? New Phytologist 165, 9–28.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Farmer EE (1985) Effects of fungal elicitor on lignin biosynthesis in cell suspension cultures of soybean. Plant Physiology 78, 338–342.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Fleurat-Lessard P, Bouché-Pillon S, Leloup C, Bonnemain JL (1997) Distribution and activity of the plasma membrane H+-ATPase in Mimosa pudica L. in relation to ionic fluxes and leaf movements. Plant Physiology 113, 747–754.
CAS | PubMed |
open url image1

Foyer CH, Noctor G (2005a) Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17, 1866–1875.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Foyer CH, Noctor G (2005b) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Foyer CH, Noctor G (2008) Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxidants & Redox Signalling in press. , open url image1

Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiologia Plantarum 100, 241–254.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, Phinney BS (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. Journal of Proteome Research 2, 413–425.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Garmier M, Priault P, Vidal G, Driscoll S, Djebbar R, Boccara M, Mathieu C, Foyer CH, De Paepe R (2007) Light and oxygen are not required for harpin-induced cell death. Journal of Biological Chemistry 282, 37556–37566.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gomez LD, Noctor G, Knight MR, Foyer CH (2004a) Regulation of calcium signalling and gene expression by glutathione. Journal of Experimental Botany 55, 1851–1859.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gomez LD, Vanacker H, Buchner P, Noctor G, Foyer CH (2004b) Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiology 134, 1662–1671.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Grant J, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiology 124, 21–30.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Guillen P, Guis M, Martinez-Reina G, Colrat S, Dalmayrac S , et al . (1998) A novel NADPH-dependent aldehyde reductase gene from Vigna radiata confers resistance to the grapevine fungal toxin eutypine. The Plant Journal 16, 335–343.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hernández I, Alegre L, Munné-Bosch S (2006) Enhanced oxidation of flavan-3-ols and proanthocyanidin accumulation in water-stressed tea plants. Phytochemistry 67, 1120–1126.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hwang EI, Ahn BT, Lee HB, Kim YK, Lee KS, Bok SH, Kim YT, Kim SU (2001) Inhibitory activity for chitin synthase II from Saccharomyces cerevisiae by tannins and related compounds. Planta Medica 67, 501–504.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jacobs A, Drya I, Robinsona S (1999) Induction of different pathogenesis-related cDNAs in grapevine infected with powdery mildew and treated with ethephon. Plant Pathology 48, 325–336.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proceedings of the National Academy of Sciences of the United States of America 103, 11086–11091.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kampranis S, Damaniova R, Atallah M, Toby G, Kondi G, Tsichlis P, Makris AM (2000) A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast. Journal of Biological Chemistry 275, 29207–29216.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Katsuhara M, Otsuka T, Ezaki B (2005) Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Science 169, 369–373.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kitamura S, Shikazono N, Tanaka A (2004) TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. The Plant Journal 37, 104–114.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kleffmann T, Hirsch-Hoffmann M, Gruissem W, Baginsky S (2006) plprot: A comprehensive proteome database for different plastid types. Plant & Cell Physiology 47, 432–436.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kmives T, Gullner G, Kiraly Z (1998) Role of glutathione and glutathione-related enzymes in response of plants to environmental stress. Annals of the New York Academy of Sciences 851, 251–258.
Crossref | GoogleScholarGoogle Scholar | open url image1

Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiology 147, 1358–1368.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kuzniak E, Sklodowska M (2005a) Compartment-specific role of the ascorbate-glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection. Journal of Experimental Botany 56, 921–933.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kuzniak E, Sklodowska M (2005b) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222, 192–200.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld JP (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiology 134, 1006–1016.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Larignon P, Dubos B (2001) Le Black Dead Arm: maladie nouvelle à ne pas confondre avec l’esca. Phytoma 538, 26–29. open url image1

Liu T, Van Staden J (2001) Partitioning of carbohydrates in salt-sensitive and salt-tolerant soybean callus cultures under salinity stress and its subsequent relief. Plant Growth Regulation 33, 13–17.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Markovic J, Borrás C, Ortega A, Sastre J, Viña J, Pallardó FV (2007) Glutathione is recruited into the nucleus in early phases of cell proliferation. Journal of Biological Chemistry 282, 20416–20424.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 127–158.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Maughan S, Foyer CH (2006) Engineering and genetic approaches to modulating the glutathione network in plants. Physiologia Plantarum 126, 382–397.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany 49, 649–667.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Mehdy MC (1994) Active oxygen species in plant defence against pathogens. Plant Physiology 105, 467–472.
CAS | PubMed |
open url image1

Miras S, Salvi D, Ferro M, Grunwald D, Garin J, Joyard J, Rolland N (2002) Non-canonical transit peptide for import into the chloroplast. Journal of Biological Chemistry 277, 47770–47778.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitamins and Hormones 72, 155–202.
CAS | Crossref | PubMed |
open url image1

Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Mugnai L, Graniti A, Surico G (1999) Esca (black measles) and brown wood-streaking: two old and elusive diseases of grapevines. Plant Disease 83, 404–418.
Crossref | GoogleScholarGoogle Scholar | open url image1

Neuefeind T, Reinemer P, Bieseler B (1997) Plant glutathione S-transferases and herbicide detoxification. Biological Chemistry 378, 199–205.
CAS | PubMed |
open url image1

Noctor G, Foyer CH (1998a) Simultaneous measurement of foliar glutathione, γ-glutamylcysteine, and amino acids by high-performance liquid chromatography: comparison with two other assay methods for glutathione. Analytical Biochemistry 264, 98–110.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Noctor G, Foyer CH (1998b) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Noctor G, Jouanin L, Arisi A-CM, Valadier M-H, Roux Y, Foyer CH (1997) Light-dependent modulation of foliar glutathione synthesis and associated amino acid metabolism in transformed poplar. Planta 202, 357–369.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Octave S, Roblin G, Vachaud M, Fleurat-Lessard P (2006) Polypeptide metabolites secreted by the fungal pathogen Eutypa lata participate in Vitis vinifera cell structure damage observed in Eutypa dieback. Functional Plant Biology 33, 297–307.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. The Plant Journal 49, 159–172.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides) . The Plant Journal 32, 701–712.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiology 132, 1631–1641.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pratelli R, Lacombe B, Torregrosa L, Gaymard F, Romieu C, Thibaud JB, Sentenac H (2002) A grapevine gene encoding a guard cell K+ channel displays developmental regulation in the grapevine berry. Plant Physiology 128, 564–577.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakière B, Vanacker H, Miginiac-Maslow M, Van Breusegem F, Noctor G (2007) Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. The Plant Journal 52, 640–657.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rausch T, Gromes R, Liedschulte V, Muller I, Bogs J, Galovic V, Wachter A (2007) Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biology 9, 565–572.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rea PA (1999) MRP subfamily ABC transporters from plants and yeast. Journal of Experimental Botany 50, 895–913.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Rellan-Alvarez R, Hernandez LE, Abadia J, Alvarez-Fernandez A (2006) Direct and simultaneous determination of reduced and oxidized glutathione and homoglutathione by liquid chromatography-electrospray/mass spectrometry in plant tissue extracts. Analytical Biochemistry 356, 254–264.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Reuber TL, Plotnikova JM, Dewdney J, Rogers EE, Wood W, Ausubel FM (1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. The Plant Journal 16, 473–485.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Richly E, Leister D (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329, 11–16.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675–709.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rossard S, Luini E, Pérault JM, Bonmort J, Roblin G (2006) Early changes in membrane permeability, production of oxidative burst and modification of PAL activity induced by ergosterol in cotyledons of Mimosa pudica. Journal of Experimental Botany 57, 1245–1252.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Roth U, Roepenack-Lahaye E, Clemensz S (2006) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. Journal of Experimental Botany 57, 4003–4013.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sappl PG, Oñate-Sánchez L, Singh KB, Millar AH (2004) Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Molecular Biology 54, 205–219.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2–1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. The Plant Journal 55, 774–786.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Senda K, Ogawa K (2004) Induction of PR-1 accumulation accompanied by runaway cell death in the lsd1 mutant of Arabidopsis is dependent on glutathione levels but independent of the redox state of glutathione. Plant & Cell Physiology 45, 1578–1585.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Shibuya N, Minami E (2001) Oligosaccharide signaling for defense responses in plant. Physiological and Molecular Plant Pathology 59, 223–233.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tabacchi R, Fkyerat A, Poliart C, Dubin GM (2000) Phytotoxins from fungi of esca of grapevine. Phytopathologia Mediterranea 39, 156–161.
CAS |
open url image1

Tietze F (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Analytical Biochemistry 27, 502–522.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397–403.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Torres MA, Jones JDG, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics 37, 1130–1134.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Vanacker H, Carver TL, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiology 117, 1103–1114.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Villadsen D, Rung JH, Nielsen TH (2005) Osmotic stress changes carbohydrate partitioning and fructose-2,6-bisphosphate metabolism in barley leaves. Functional Plant Biology 32, 1033–1043.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Villarejo A, Burén S, Larsson S, Déjardin A, Monné M , et al . (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nature Cell Biology 7, 1124–1131.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wachter A, Wolf S, Steiniger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. The Plant Journal 41, 15–30.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Molecular Biology 49, 515–532.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wagner D, Przybyla D, den Camp R, Kim C, Landgraf F , et al . (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183–1185.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wingler A, Quick WP, Bungard RA, Bailey KJ, Lea PJ, Leegood RC (1999) The role of photorespiration during drought stress: analysis utilizing barley mutants with reduced activities of photorespiratory enzymes. Plant, Cell & Environment 22, 361–373.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiology 126, 564–574.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yamane Y, Furuichi M, Song R, Van NT, Mulcahy RT, Ishikawa T, Kuo MT (1998) Expression of multidrug resistance protein/GS-X pump and γ-glutamylcysteine synthetase genes is regulated by oxidative stress. Journal of Biological Chemistry 273, 31075–31085.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yuan JS, Tranel PJ, Stewart CN (2007) Non-target-site herbicide resistance: a family business. Trends in Plant Science 12, 6–13.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1