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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Plant defence responses: what have we learnt from Arabidopsis?

Louise F. Thatcher A B , Jonathan P. Anderson A and Karam B. Singh A C
+ Author Affiliations
- Author Affiliations

A CSIRO Plant Industry, Centre for Environment and Life Sciences, Private Bag 5, Wembley, WA 6913, Australia.

B Soil Science and Plant Nutrition, School of Earth and Geographical Sciences, The University of Western Australia, Crawley, WA 6009, Australia.

C Corresponding author. Email: Karam.Singh@csiro.au

Functional Plant Biology 32(1) 1-19 https://doi.org/10.1071/FP04135
Submitted: 4 August 2004  Accepted: 19 September 2004   Published: 21 January 2005

Abstract

To overcome the attack of invading pathogens, a plant’s defence system relies on preformed and induced responses. The induced responses are activated following detection of a pathogen, with the subsequent transmission of signals and orchestrated cellular events aimed at eliminating the pathogen and preventing its spread. Numerous studies are proving that the activated signalling pathways are not simply linear, but rather, form complex networks where considerable cross talk takes place. This review covers the recent application of powerful genetic and genomic approaches to identify key defence signalling pathways in the model plant Arabidopsis thaliana (L.) Heynh. The identification of key regulatory components of these pathways may offer new approaches to increase the defence capabilities of crop plants.

Keywords: biotic stress, ethylene, hydrogen peroxide, jasmonate, nitric oxide, pathogen, plant defense, salicylic acid.


Acknowledgments

We thank Drs Peter Dodds and Kemal Kazan for helpful comments on the manuscript, and members of the Singh laboratory for useful discussions. We apologise for not being able to cite several important references because of length limitations. Work on plant defence in the authors’ laboratory is supported in part by the Grains Research and Development Corporation (GRDC) and Department of Education, Science and Training (DEST).


References


Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signalling pathways in Arabidopsis. Proceedings of the National Academy of Sciences USA 95, 10306–10311.
Crossref | GoogleScholarGoogle Scholar | open url image1

Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148–2152.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Kazan K (2004) Antagonistic interactions between abscisic acid and jasmonate–ethylene signaling pathways modulates defence gene expression and sisease resistance in Arabidopsis. The Plant Cell 16, 3460–3479.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anderson JP, Thatcher LF, Singh KB (2005) Plant defence responses: conservation between models and crops. Functional Plant Biology 32, 21–34. open url image1

Anderson LK, Bowling SA, Dong X (2000) Cloning and characterisation of CPR5. 11th International conference on research, Madison, WI (June 2000)


Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Atkinson MM, Midland SL, Sims JJ, Keen NT (1996) Syringolide 1 triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiology 112, 297–302.
PubMed |
open url image1

Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295, 2077–2080.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369–377.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences USA 92, 8675–8679. open url image1

Berger S, Bell E, Mullet JE (1996) Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiology 111, 525–531.
PubMed |
open url image1

Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal 29, 23–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bi Y, Kenton P, Mur L, Darby R, Draper J (1995) Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. The Plant Journal 8, 235–245.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086–1089. open url image1

Bohman S, Staal J, Thomma BPHJ, Wang M, Dixelius C (2004) Characterisation of an Arabidopsis–Leptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. The Plant Journal 37, 9–20.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bonas U, Lahaye T (2002) Plant Disease resistance triggered by pathogen-derived molecules: refined models of specific recognition. Current Opinion in Microbiology 5, 44–50.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bowling SA, Guo A, Cao H, Gordon AS, Klessig DF, Dong X (1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. The Plant Cell 6, 1845–1857.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Buttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proceedings of the National Academy of Sciences USA 94, 5961–5966.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cao H, Bowling SA, Gordon S, Dong X (1994) Characterisation of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. The Plant Cell 6, 1583–1592.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57–63.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Century KS, Holub EB, Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proceedings of the National Academy of Sciences USA 92, 6597–6601. open url image1

Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278, 1963–1965.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133–1144.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chen W, Chao G, Singh KB (1996) The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. The Plant Journal 10, 955–966.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang H , et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. The Plant Cell 14, 559–574.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chen Z, Klessig DF (1991) Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease-resistance response. Proceedings of the National Academy of Sciences USA 88, 8179–8183. open url image1

Chen Z, Ricigliano JW, Klessig DF (1993) Purification and characterisation of a soluble salicylic acid-binding protein from tobacco. Proceedings of the National Academy of USA 90, 9533–9537. open url image1

Clark KL, Larsen PB, Wang X, Chang C (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proceedings of the National Academy of Sciences USA 95, 5401–5406.
Crossref | GoogleScholarGoogle Scholar | open url image1

Clarke JD, Liu Y, Klessig DF, Dong X (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6–1 mutant. The Plant Cell 10, 557–569.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong X (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. The Plant Cell 12, 2175–2190.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clarke JD, Aarts N, Feys BJ, Dong X, Parker JE (2001) Constitutive disease resistance requires EDS1 in the Arabidopsis mutants cpr1 and cpr6 and is partially EDS1-dependent in cpr5. The Plant Journal 26, 409–420.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clough SJ, Fengler KA, Yu I, Lippok B, Smith RK, Bent AF (2000) The Arabidopsis dnd1 ‘defense, no death’ gene encodes a mutated cyclic nucleotide-gated ion channel. Proceedings of the National Academy of Sciences USA 97, 9323–9328.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Delaney T, Uknes S, Vernooij B, Friedrich L, Weymann K , et al. (1994) A central role of salicylic acid in plant disease resistance. Science 266, 1247–1250. open url image1

Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proceedings of the National Academy of Sciences USA 92, 6602–6606. open url image1

Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences USA 98, 13 454–13 459.
Crossref | GoogleScholarGoogle Scholar | open url image1

del Río LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phtyochemistry 65, 783–792.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Critical Reviews in Plant Sciences 18, 547–575.
Crossref | GoogleScholarGoogle Scholar | open url image1

Desikan R, Reynolds A, Hancock JT, Neill SJ (1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. The Biochemical Journal 330, 115–120.
PubMed |
open url image1

Després C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1 / NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. The Plant Cell 12, 279–290.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Annals of Botany 92, 329–337.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dewdney J, Reuber TL, Wildermuth MC, Devoto A, Cui J, Stutius LM, Drummond EP, Ausubel FM (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. The Plant Journal 24, 205–218.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dietrich A, Mayer JE, Hahlbrock K (1990) Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. Journal of Biological Chemistry 265, 6360–6368.
PubMed |
open url image1

Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77, 565–577.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88, 685–694.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dodds PN, Schwechheimer C (2002) A breakdown in defense signaling. The Plant Cell Supplement 14, S5–S8.
PubMed |
open url image1

Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP ribose. Proceedings of the National Academy of Sciences USA 95, 10 328–10 333.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. The Plant Cell 13, 1025–1033.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. The Plant Cell 14, 1557–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiology 109, 813–820.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Eulgem T, Rushton PJ, Robatzek S, Sommssich IE (2000) The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199–206.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Eulgem T, Weigman VJ, Chang HS, McDowell JM, Holub EB, Glazebrook J, Zhu T, Dangl JL (2004) Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance. Plant Physiology 135, 1129–1144.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Falk A, Feys BJ, Frost LN, Jones JDG, Daniels MJ, Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proceedings of the National Academy of Sciences USA 96, 3292–3297.
Crossref | GoogleScholarGoogle Scholar | open url image1

Felix G, Grosskopf DG, Regenass M, Boller T (1991) Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proceedings of the National Academy of Sciences USA 88, 8831–8834. open url image1

Feys B, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. The Plant Cell 6, 751–759.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275–296.
Crossref | GoogleScholarGoogle Scholar | open url image1

Friedrich L, Vernooij B, Gaffney T, Morse A, Rylas J (1995) Characterisation of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Molecular Biology 29, 959–968.
Crossref | PubMed |
open url image1

Friedrich L, Lawton K, Ruess W, Masner P, Specker N , et al. (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. The Plant Journal 10, 61–70.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fritig B, Heitz T, Legrand M (1998) Antimicrobial proteins in induced plant defense. Current Opinion in Immunology 10, 16–22.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. The Plant Cell 10, 947–956.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proceedings of the National Academy USA 98, 373–378.
Crossref | GoogleScholarGoogle Scholar | open url image1

Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterisation of their interactions with bacterial pathogens. Proceedings of the National Academy of Sciences USA 91, 8955–8959. open url image1

Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143, 973–982.
PubMed |
open url image1

Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis — 2001 status. Current Opinion in Plant Biology 4, 301–308.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Métraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. The Plant Journal 34, 217–228.
Crossref | PubMed |
open url image1

Greenberg JT, Guo A, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77, 551–563.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guo H, Ecker JR (2004) The ethylene signalling pathway: new insights. Current Opinion in Plant Biology 7, 40–49.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gupta V, Willits MG, Glazebrook J (2000) EDS4 Contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Molecular Plant–Microbe Interactions 13, 503–511.
PubMed |
open url image1

Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. The Plant Cell 2, 513–523.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hahlbrock K, Scheel D, Logemann E, Nurnberger T, Parniske M, Reinold S, Sacks WR, Schmelzer E (1995) Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. Proceedings of the National Academy of Sciences USA 92, 4150–4157. open url image1

Hancock JT, Desikan R, Clarke A, Hurst RD, Neill SJ (2002) Cell signalling following plant / pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species. Plant Physiology and Biochemistry 40, 611–617.
Crossref | GoogleScholarGoogle Scholar | open url image1

Heath MC (2000a) Nonhost resistance and nonspecific plant defenses. Current Opinion in Plant Biology 3, 315–319.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heath MC (2000b) Hypersensitive response-related death. Plant Molecular Biology 44, 321–334.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heck S, Grau T, Buchala A, Metraux JP, Nawrath C (2003) Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the ArabidopsisPseudomonas syringae pv. tomato interaction. The Plant Journal 36, 342–352.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hilpert B, Bohlmann H, den Camp R, Przybyla D, Miersch O, Buchala A, Apel K (2001) Isolation and characterization of signal transduction mutants of Arabidopsis thaliana that constitutively activate the octadecanoid pathway and form necrotic microlesions. The Plant Journal 26, 435–446.
Crossref | PubMed |
open url image1

Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215, 914–923.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218, 938–946.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huang Y, Li H, Hutchison CE, Laskey J, Kieber JJ (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signalling in Arabidopsis. The Plant Journal 33, 221–233.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Iavicoli A, Boutet E, Buchala A, Métraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant–Microbe Interactions 10, 851–858. open url image1

Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE 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. The Plant Cell 13, 2191–2209.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. The Plant Cell 15, 2503–2513.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Pary F (2002) bZIP transcription factors in Arabidopsis. Trends in Plant Science 7, 106–111.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jensen A, Raventos D, Mundy J (2002) Fusion genetic analysis of jasmonate-signalling mutants in Arabidopsis. The Plant Journal 29, 595–606.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Molecular Biology 41, 577–585.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signalling. Proceedings of the National Academy of Sciences USA 96, 13 583–13 588.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jirage D, Zhou N, Cooper B, Clarke BC, Dong X, Glazebrook J (2001) Constitutive salicylic acid-dependent signalling in cpr1 and cpr6 mutants requires PAD4. The Plant Journal 26, 395–407.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annual Review of Genetics 32, 227–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jonak C, Ökrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Current Opinion in Plant Biology 5, 415–424.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jones JDG (2001) Putting knowledge of plant disease resistance genes to work. Current Opinion in Plant Biology 4, 281–287.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jurkowski GI, Smith RK, Yu I, Ham JH, Sharma SB, Klessig DF, Fengler KA, Bent AF (2004) Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the ‘defense, no death’ phenotype. Molecular Plant–Microbe Interactions 17, 511–520.
PubMed |
open url image1

Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proceedings of the National Academy of Sciences USA 98, 9448–9453.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003) Plastidial fatty acid signalling modulates salicylic acid and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. The Plant Cell 15, 2952–2965.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427–441.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kim HS, Delaney TP (2002) Arabidopsis SON1 Is an F-Box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. The Plant Cell 14, 1469–1482.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proceedings of the National Academy of Sciences USA 100, 16101–16106.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kunkel BN, Brooks DM (2002) Cross talk between signalling pathways in pathogen defence. Current Opinion in Plant Biology 5, 325–331.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Rylas J (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant–Microbe Interactions 8, 863–870.
PubMed |
open url image1

Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. The Plant Journal 16, 223–233.
Crossref | PubMed |
open url image1

Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1–1. Cell 98, 329–339.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. The Plant Cell 15, 165–178.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends in Plant Science 8, 263–271.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Low PS, Merida JR (1996) The oxidative burst in plant defense: function and signal transduction. Physiologia Plantarum 96, 533–542.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signalling in the Arabidopsis defense response. The Plant Cell 15, 2048–2420. open url image1

Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proceedings of the National Academy of Sciences USA 98, 771–776.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 Interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress / defense transcriptome of Arabidopsis. Genome Biology 4, R20.1–R20.14.
Crossref |
open url image1

Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399–403.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2001) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genetics 26, 403–410. open url image1

Martin C, Paz-Ares J (1997) MYB transcription factors in plants. Trends in Genetics 13, 67–73.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 23–61.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. The Plant Cell 8, 403–416.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. The Plant Cell 15, 2551–2565.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Muskett PR, Kahn K, Austin MJ, Moisan LJ, Sadanandom A, Shirasu K, Jones JD, Parker JE (2002) Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. The Plant Cell 14, 979–992.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Muskett P, Parker J (2003) Role of SGT1 in the regulation of plant R gene signalling. Microbes and Infection 5, 969–976.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mysore KS, Ryu CM (2004) Nonhost resistance: how much do we know? Trends in Plant Science 9, 97–104.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nandi A, Kachroo P, Fukushige H, Hildebrand DF, Klessig DF, Shah J (2003) Ethylene and jasmonic acid signaling affect the NPR1-independent expression of defense genes without impacting resistance to Pseudomonas syringae and Peronospora parasitica in the Arabidopsis ssi1 mutant. Molecular Plant–Microbe Interactions 16, 588–599.
PubMed |
open url image1

Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. The Plant Cell 11, 1393–1404.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, an essential component of salicylic acid-dependent signalling for disease resistance in Arabidopsis, is a member of the MATE transporter family. The Plant Cell 14, 275–286.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Current Opinion in Plant Biology 5, 388–395.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytologist 159, 11–35.
Crossref | GoogleScholarGoogle Scholar | open url image1

Neuenschwander U, Vernooij B, Friedrich L, Uknes S, Kessmann H, Ryals J (1995) Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? The Plant Journal 8, 227–233.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nibbe M, Hilpert B, Wasternack C, Miersch O, Apel K (2002) Cell death and salicylate- and jasmonate-dependent stress responses in Arabidopsis are controlled by single cet genes. Planta 216, 120–128.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nimchuk Z, Eulgem T, Holt BF, Dangl JL (2003) Recognition and response in the plant immune system. Annual Review of Genetics 37, 579–609.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301, 969–972.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nurnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78, 449–460.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. The Plant Cell 7, 173–182.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniels MJ (1996) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. The Plant Cell 8, 2033–2046.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Peck SC (2003) Early phosphorylation events in biotic stress. Current Opinion in Plant Biology 6, 334–338.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pedras MSC, Okanga FI, Zaharia IL, Khan AQ (2000) Phytoalexins from crucifers: synthesis, biosynthesis, and biotransformation. Phytochemistry 53, 161–176.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. The Plant Cell 8, 2309–2323.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Penninckx IA, Thomma BP, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell 10, 2103–2113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U , et al. (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111–1120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. The Plant Cell 10, 1571–1580.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pieterse CM, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Current Opinion in Plant Biology 7, 456–464.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Molecular Plant–Microbe Interactions 16, 1094–1105.
PubMed |
open url image1

Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. The Plant Cell 11, 1695–1708.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rate DN, Greenberg JT (2001) The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. The Plant Journal 27, 203–211.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Riechmann JL, Ratcliffe OJ (2000) A genomic perspective on plant transcription factors. Current Opinion in Plant Biology 3, 423–434.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rogers EE, Ausubel FM (1997) Arabidopsis enhances disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. The Plant Cell 9, 305–316.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Romero-Puertas MC, Delledonne M (2003) Nitric oxide signaling in plant–pathogen interactions. IUBMB Life 55, 579–583.
PubMed |
open url image1

Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. The Plant Cell 8, 1809–1819.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. The Plant Cell 12, 1041–1061.
Crossref | PubMed |
open url image1

Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences USA 97, 11 655–11 660.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schneider DS (2002) Plant immunity and film noir: what gumshoe detectives can teach us about plant–pathogen interactions. Cell 109, 537–540.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shah J, Tsui F, Klessig DF (1997) Characterisation of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Molecular Plant-Microbe Interactions 10, 69–78.
PubMed |
open url image1

Shah J, Kachroo P, Klessig DF (1999) The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. The Plant Cell 11, 191–206.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shah J, Kachroo P, Nandi A, Klessig DF (2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. The Plant Journal 25, 563–574.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230–1233.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 5, 430–436.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes and Development 12, 3703–3714.
PubMed |
open url image1

Song JT, Lu H, Greenberg JT (2004) Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. The Plant Cell 16, 353–366.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA , et al. (2003) NPR1 Modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. The Plant Cell 15, 760–770.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences USA 89, 6837–6840. open url image1

Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signalling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. The Plant Journal 15, 747–754.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. The Plant Cell 14, 1405–1415.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stintzi A, Browse J (2000) 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, 10 625–10 630.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stone, BA ,  and  Clarke, AE (1992). ‘Chemistry and biology of (1→3)-β--glucans.’ (La Trobe University Press: Melbourne)

Suzuki H, Xia Y, Cameron R, Shadle G, Blount J, Lamb C, Dixon RA (2003) Signals for local and systemic responses of plants to pathogen attack. Journal of Experimental Botany 55, 169–179.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. The Plant Journal 26, 101–112.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. The Plant Cell 15, 317–330.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Sciences USA 95, 15 107–15 111.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thomma BP, Eggermont K, Tierens KF, Broekaert WF (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiology 121, 1093–1102.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tierens KFMJ, Thomma BPHJ, Bari RP, Garmier M, Eggermont K, Brouwer M, Penninckx IAMA, Broekaert WF, Cammue BPA (2002) Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defense responses by reactive oxygen generating compounds. The Plant Journal 29, 131–140.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic / helix-loop-helix transcription factor family. The Plant Cell 15, 1749–1770.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ton J, Pieterse CM, Van Loon LC (1999) Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Molecular Plant–Microbe Interactions 12, 911–918.
PubMed |
open url image1

Ton J, Davison S, Van Wees SCM, Van Loon LC, Pieterse CMJ (2001) The Arabidopsis ISR1 Locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signalling. Plant Physiology 125, 652–661.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tor M, Gordon P, Cuzick A, Eulgem T, Sinapidou E, Mert-Turk F, Can C, Dangl JL, Holub EB (2002) Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. The Plant Cell 14, 993–1003.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl JL (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. The Plant Cell 14, 1005–1015.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. The Plant Cell Supplement 14, S153–S164.
PubMed |
open url image1

Turner, RJ (1994). ‘Immunology: a comparative approach.’ (John Wiley and Sons Ltd: London)

Uknes S, Winter A, Delaney T, Vernooij B, Morse A, Friedrich L, Nye G, Potter S, Ward E, Ryals J (1993) Biological induction of systemic acquired resistance in Arabidopsis. Molecular Plant–Microbe Interactions 6, 692–698. open url image1

Van Loon LC, Van Strein EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55, 85–97.
Crossref | GoogleScholarGoogle Scholar | open url image1

van Wees SC, Glazebrook J (2003) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. The Plant Journal 33, 733–742.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Verhagen BW, Glazebrook J, Zhu T, Chang HS, van Loon LC, Pieterse CM (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Molecular Plant-Microbe Interactions 17, 895–908.
PubMed |
open url image1

Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. The Plant Cell 6, 959–965.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vogel J, Somerville S (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proceedings of the National Academy of Sciences USA 97, 1897–1902.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vogel JP, Raab TK, Schiff C, Somerville SC (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. The Plant Cell 14, 2095–2106.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends in Plant Science 9, 203–209.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signalling networks. The Plant Cell Supplement 14, S131–S151.
PubMed |
open url image1

Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. The Plant Cell 3, 1085–1094.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152, 401–412.
PubMed |
open url image1

Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signalling and defence responses. Current Opinion in Plant Biology 7, 449–455.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weymann K, Hunt M, Uknes S, Neuenschwander U, Lawton K, Steiner HY, Ryals J (1995) Suppression and restoration of lesion formation in Arabidopsis lsd mutants. The Plant Cell 7, 2013–2022.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO Journal 23, 980–988.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yan J, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. The Plant Journal 29, 193–202.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yanagisawa S (2002) The Dof family of plant transcription factors. Trends in Plant Science 7, 555–560.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes and Development 11, 1621–1639.
PubMed |
open url image1

Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. The Plant Cell 13, 1527–1540.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yu I, Parker J, Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proceedings of the National Academy of Sciences USA 95, 7819–7824.
Crossref |
open url image1

Yu I, Fengler KA, Clough SJ, Bent AF (2000) Identification of Arabidopsis mutants exhibiting an altered hypersensitive response in gene-for-gene disease resistance. Molecular Plant–Microbe Interactions 13, 277–286.
PubMed |
open url image1

Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proceedings of the National Academy of Sciences USA 101, 15811–15816.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhang B, Chen W, Foley RC, Buttner M, Singh KB (1995) Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. The Plant Cell 7, 2241–2252.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proceedings of the National Academy of Sciences USA 96, 6523–6528.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhang Y, Tessaro MJ, Lassner M, Li X (2003) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. The Plant Cell 15, 2647–2653.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 Differentially interacts with members of the TGA / OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Molecular Plant–Microbe Interactions 13, 191–202.
PubMed |
open url image1

Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. The Plant Cell 10, 1021–1030.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. The Plant Cell 11, 2419–2428.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1