Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection.

SUMMARY Physical injury inflicted on living tissue makes it vulnerable to invasion by pathogens. Wounding of Arabidopsis thaliana leaves, however, does not conform to this concept and leads to immunity to Botrytis cinerea, the causal agent of grey mould. In wounded leaves, hyphal growth was strongly inhibited compared to unwounded controls. Wound-induced resistance was not associated with salicylic acid-, jasmonic acid- or ethylene-dependent defence responses. The phytoalexin camalexin was found to be involved in this defence response as camalexin-deficient mutants were not protected after wounding and the B. cinerea strains used here were sensitive to this compound. Wounding alone did not lead to camalexin production but primed its accumulation after inoculation with B. cinerea, further supporting the role of camalexin in wound-induced resistance. In parallel with increased camalexin production, genes involved in the biosynthesis of camalexin were induced faster in wounded and infected plants in comparison with unwounded and infected plants. Glutathione was also found to be required for resistance, as mutants deficient in gamma-glutamylcysteine synthetase showed susceptibility to B. cinerea after wounding, indicating that wild-type basal levels of glutathione are required for the wound-induced resistance. Furthermore, expression of the gene encoding glutathione-S-transferase 1 was primed by wounding in leaves inoculated with B. cinerea. In addition, the priming of MAP kinase activity was observed after inoculation of wounded leaves with B. cinerea compared to unwounded inoculated controls. Our results demonstrate how abiotic stress can induce immunity to virulent strains of B. cinerea, a process that involves camalexin and glutathione.

[1]  Jean-Luc Cacas,et al.  Mechanisms of Defence to Pathogens: Biochemistry and Physiology , 2007 .

[2]  F. Cardinale,et al.  Wounding induces resistance to pathogens with different lifestyles in tomato: role of ethylene in cross-protection. , 2007, Plant, cell & environment.

[3]  D. Giustarini,et al.  S-glutathionylation in protein redox regulation. , 2007, Free radical biology & medicine.

[4]  J. Glazebrook,et al.  Arabidopsis Cytochrome P450 Monooxygenase 71A13 Catalyzes the Conversion of Indole-3-Acetaldoxime in Camalexin Synthesis[W] , 2007, The Plant Cell Online.

[5]  E. Glawischnig,et al.  Regulatory variability of camalexin biosynthesis. , 2007, Journal of plant physiology.

[6]  J. Metraux,et al.  Cuticular defects lead to full immunity to a major plant pathogen. , 2007, The Plant journal : for cell and molecular biology.

[7]  John C. Walker,et al.  Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis[W] , 2007, The Plant Cell Online.

[8]  B. Poinssot,et al.  Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[9]  B. Halkier,et al.  CYP71B15 (PAD3) Catalyzes the Final Step in Camalexin Biosynthesis1 , 2006, Plant Physiology.

[10]  S. Davis Faculty Opinions recommendation of Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. , 2006 .

[11]  Synan F. AbuQamar,et al.  The Membrane-Anchored BOTRYTIS-INDUCED KINASE1 Plays Distinct Roles in Arabidopsis Resistance to Necrotrophic and Biotrophic Pathogens[W] , 2005, The Plant Cell Online.

[12]  B. Ellis,et al.  RNA interference-based (RNAi) suppression of AtMPK6, an Arabidopsis mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3. , 2005, Environmental pollution.

[13]  D. Kliebenstein,et al.  Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. , 2005, The Plant journal : for cell and molecular biology.

[14]  J. Glazebrook Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. , 2005, Annual review of phytopathology.

[15]  K. Matsui,et al.  Volatile C6-aldehydes and Allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. , 2005, Plant & cell physiology.

[16]  C. Foyer,et al.  Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses , 2005, The Plant Cell Online.

[17]  J. Benen,et al.  Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. , 2005, The Plant journal : for cell and molecular biology.

[18]  P. Vera,et al.  An Arabidopsis Homeodomain Transcription Factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, Mediates Resistance to Infection by Necrotrophic Pathogens , 2005, The Plant Cell Online.

[19]  K. Denby,et al.  ups1, an Arabidopsis thaliana camalexin accumulation mutant defective in multiple defence signalling pathways. , 2005, The Plant journal : for cell and molecular biology.

[20]  G. Howe Jasmonates as Signals in the Wound Response , 2004, Journal of Plant Growth Regulation.

[21]  I. G. Collado,et al.  Virulence–Toxin Production Relationship in Isolates of the Plant Pathogenic Fungus Botrytis cinerea , 2004 .

[22]  P. Mullineaux,et al.  Evidence for a Direct Link between Glutathione Biosynthesis and Stress Defense Gene Expression in Arabidopsisw⃞ , 2004, The Plant Cell Online.

[23]  B. G. Hansen,et al.  Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Kliebenstein,et al.  Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[25]  D. Joyce,et al.  Elicitors of induced disease resistance in postharvest horticultural crops: a brief review , 2004 .

[26]  J. Tumlinson,et al.  Airborne signals prime plants against insect herbivore attack. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  L. Hadwiger,et al.  Molecular cloning and characterization of a pea chitinase gene expressed in response to wounding, fungal infection and the elicitor chitosan , 1995, Plant Molecular Biology.

[28]  K. Gindro,et al.  Plant-microbe interaction: the Botrytis grey mould of grapes - biology, biochemistry, epidemiology and control management. , 2004 .

[29]  J. Durner,et al.  The Role of Salicylic Acid and Nitric Oxide in Programmed Cell Death and Induced Resistance , 2004 .

[30]  A. Heyraud,et al.  Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea , 2004, Planta.

[31]  G. Pearce,et al.  Systemins: A functionally defined family of peptide signals that regulate defensive genes in Solanaceae species , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Jean-Pierre Métraux,et al.  Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas syringae pv. tomato interaction. , 2003, The Plant journal : for cell and molecular biology.

[33]  Frederick M Ausubel,et al.  Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. , 2003, The Plant journal : for cell and molecular biology.

[34]  C. Levis,et al.  Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces virulence on several host plants. , 2003, Molecular plant-microbe interactions : MPMI.

[35]  J. V. van Kan,et al.  The Role of Ethylene and Wound Signaling in Resistance of Tomato to Botrytis cinerea 1 , 2002, Plant Physiology.

[36]  C. Pieterse,et al.  Priming in plant-pathogen interactions. , 2002, Trends in plant science.

[37]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[38]  R. Solano,et al.  Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. , 2002, The Plant journal : for cell and molecular biology.

[39]  H. Schoonbeek,et al.  The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. , 2001, Molecular plant-microbe interactions : MPMI.

[40]  G. D’hallewin,et al.  Host–pathogen interactions modulated by heat treatment , 2000 .

[41]  F. Ausubel,et al.  Roles of Salicylic Acid, Jasmonic Acid, and Ethylene in cpr-Induced Resistance in Arabidopsis , 2000, Plant Cell.

[42]  A. Mayer,et al.  Enzymes of Botrytis cinerea capable of breaking down hydrogen peroxide. , 2000, FEMS microbiology letters.

[43]  J. Kuc Development and future direction of induced systemic resistance in plants , 2000 .

[44]  J. J. Grant,et al.  Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. , 2000, Plant physiology.

[45]  A. Levine,et al.  The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea , 2000, Current Biology.

[46]  P. Reymond,et al.  Differential Gene Expression in Response to Mechanical Wounding and Insect Feeding in Arabidopsis , 2000, Plant Cell.

[47]  J. Glazebrook,et al.  Arabidopsis PAD3, a Gene Required for Camalexin Biosynthesis, Encodes a Putative Cytochrome P450 Monooxygenase , 1999, Plant Cell.

[48]  B. Thomma,et al.  Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. , 1999, Plant physiology.

[49]  Jean-Pierre Métraux,et al.  Salicylic Acid Induction–Deficient Mutants of Arabidopsis Express PR-2 and PR-5 and Accumulate High Levels of Camalexin after Pathogen Inoculation , 1999, Plant Cell.

[50]  B. Thomma,et al.  Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. , 1999, The Plant journal : for cell and molecular biology.

[51]  M. Bennett,et al.  Cell wall alterations and localized accumulation of feruloyl-3-methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis , 1999 .

[52]  B. Thomma,et al.  Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J. Visser,et al.  The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. , 1998, Molecular plant-microbe interactions : MPMI.

[54]  C. Cobbett,et al.  The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. , 1998, The Plant journal : for cell and molecular biology.

[55]  S. Oeljeklaus,et al.  Purification and characterization of glucose oxidase ofBotrytis cinerea , 1998 .

[56]  C. Foyer,et al.  ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. , 1998, Annual review of plant physiology and plant molecular biology.

[57]  P. Comménil,et al.  Antilipase antibodies prevent infection of tomato leaves byBotrytis cinerea , 1998 .

[58]  E. Titarenko,et al.  Jasmonic Acid-Dependent and -Independent Signaling Pathways Control Wound-Induced Gene Activation in Arabidopsis thaliana , 1997, Plant physiology.

[59]  T. Nishiuchi,et al.  Wounding changes the spatial expression pattern of the arabidopsis plastid omega-3 fatty acid desaturase gene (FAD7) through different signal transduction pathways. , 1997, The Plant cell.

[60]  T. Jabs,et al.  Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide , 1996, Science.

[61]  K. Marrs THE FUNCTIONS AND REGULATION OF GLUTATHIONE S-TRANSFERASES IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[62]  I. Raskin,et al.  Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  A. Mayer,et al.  Putative virulence factors of Botrytis cinerea acting as a wound pathogen , 1995 .

[64]  F. Ausubel,et al.  Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[65]  F. Ausubel,et al.  Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions , 1994, Cell.

[66]  M. Bennett,et al.  The phytoalexin response of lettuce to challenge by Botrytis cinerea, Bremia lactucae and Pseudomonas syringae pv. phaseolicola , 1994 .

[67]  C. Ryan Protease Inhibitors in Plants: Genes for Improving Defenses Against Insects and Pathogens , 1990 .

[68]  J. Mansfield,et al.  The composition of wall alterations and appositions (reaction material) and their role in the resistance of onion bulb scale epidermis to colonization by Botrytis allii , 1985 .

[69]  M. Hahn,et al.  Quantitative Localization of the Phytoalexin Glyceollin I in Relation to Fungal Hyphae in Soybean Roots Infected with Phytophthora megasperma f. sp. glycinea. , 1985, Plant physiology.

[70]  J. Mansfield,et al.  Microscopical studies on fungal development and host responses in broad bean and tulip leaves inoculated with five species of Botrytis , 1980 .

[71]  K. Yamauchi,et al.  Glyceollin: its rôle in restricting fungal growth in resistant soybean hypocotyls infected with Phytophthora megasperma var. sojae , 1978 .