The Arabidopsis LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE3 regulates the cross talk between immunity and abscisic acid responses

Plant Physiology

Volumn 165, Issue 1, 2014, Pages 262-276

  Paparella, Chiara ^a   Savatin, Daniel Valentin ^a   Marti, Lucia ^a   De Lorenzo, Giulia ^a   Ferrari, Simone ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LYK3 PROTEIN, ARABIDOPSIS; OLIGOGALACTURONIC ACID; OLIGOSACCHARIDE; PROTEIN KINASE;

ARABIDOPSIS; BOTRYTIS; CELL MEMBRANE; DISEASE RESISTANCE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BOTRYTIS; CELL MEMBRANE; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; MUTATION; OLIGOSACCHARIDES; PHENOTYPE; PLANT DISEASES; PLANT IMMUNITY; PROTEIN KINASES; RECEPTOR CROSS-TALK; RECOMBINANT FUSION PROTEINS;

EID: 84899812833     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.233759     Document Type: Article

References (99)

1. Adie BA, Pérez-Pérez J, Pérez-Pérez MM, Godoy M, Sánchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19: 1665-1681
2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genomewide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
3. Arnaud D, Desclos-Theveniau M, Zimmerli L (2012) Disease resistance to Pectobacterium carotovorum is negatively modulated by the Arabidopsis Lectin Receptor Kinase LecRK-V.5. Plant Signal Behav 7: 1070-1072
4. Asselbergh B, Achuo AE, Höfte M, Van Gijsegem F (2008a) Abscisic acid deficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol Plant Pathol 9: 11-24
5. Asselbergh B, Curvers K, Franca SC, Audenaert K, Vuylsteke M, Van Breusegem F, Höfte M (2007) Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol 144: 1863-1877
6. Asselbergh B, De Vleesschauwer D, Höfte M (2008b) Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol Plant Microbe Interact 21: 709-719
7. Audenaert K, De Meyer GB, Höfte MM (2002a) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128: 491-501
8. Audenaert K, Pattery T, Cornelis P, Höfte M (2002b) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant Microbe Interact 15: 1147-1156
9. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473-488
10. Bateman A, Bycroft M (2000) The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 299: 1113-1119
11. Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, Petétot JM, Métraux JP, Nawrath C (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26: 2158-2168
12. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81: 1-5
13. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbeassociated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406
14. Brandizzi F, Irons SL, Johansen J, Kotzer A, Neumann U (2004) GFP is the way to glow: bioimaging of the plant endomembrane system. JMicrosc 214: 138-158
15. Brotman Y, Landau U, Pnini S, Lisec J, Balazadeh S, Mueller-Roeber B, Zilberstein A, Willmitzer L, Chet I, Viterbo A (2012) The LysM receptor-like kinase LysM RLK1 is required to activate defense and abiotic-stress responses induced by overexpression of fungal chitinases in Arabidopsis plants. Mol Plant 5: 1113-1124
16. Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plantpathogen interactions. J Plant Res 124: 489-499
17. Chassot C, Nawrath C, Métraux JP (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49: 972-980
18. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101
19. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
20. Curvers K, Seifi H, Mouille G, de Rycke R, Asselbergh B, Van Hecke A, Vanderschaeghe D, Höfte H, Callewaert N, Van Breusegem F, et al (2010) Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiol 154: 847-860
21. de las Mercedes DM, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142: 722-730
22. De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr Opin Plant Biol 5: 295-299
23. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M (2007) Pseudomonas syringae pv tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26: 1434-1443
24. Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J (2008) Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant 1: 423-445
25. Desclos-Theveniau M, Arnaud D, Huang TY, Lin GJ, Chen WY, Lin YC, Zimmerli L (2012) The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv tomato DC3000. PLoS Pathog 8: e1002513
26. Doares SH, Syrovets T, Weiler EW, Ryan CA (1995) Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci USA 92: 4095-4098
27. Dyachok JV, WiwegerM, Kenne L, von Arnold S (2002) Endogenous Nodfactor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol 128: 523-533
28. Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19: 1349
29. Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V, Flagiello A, Pucci P, Lanzetta R, Parrilli M, Molinaro A, et al (2008) Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem Biol 15: 438-448
30. Federici L, Di Matteo A, Fernandez-Recio J, Tsernoglou D, Cervone F (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 11: 65-70
31. Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144: 367-379
32. Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146: 669-681
33. Ferrari S, Galletti R, Vairo D, Cervone F, De Lorenzo G (2006) Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonaseinhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Mol Plant Microbe Interact 19: 931-936
34. Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35: 193-205
35. Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, Lorenzo GD (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4: 49
36. Galletti R, De Lorenzo G, Ferrari S (2009) Host-derived signals activate plant innate immunity. Plant Signal Behav 4: 33-34
37. Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, Ferrari S (2008) The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol 148: 1695-1706
38. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr Opin Plant Biol 4: 301-308
39. Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91: 8955-8959
40. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011
41. Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284
42. González-Guzmán M, Apostolova N, Bellés JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodríguez PL (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14: 1833-1846
43. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Götz F, Glawischnig E, Lee J, Felix G, et al (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282: 32338-32348
44. Gust AA, Willmann R, Desaki Y, Grabherr HM, Nürnberger T (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17: 495-502
45. Igarashi D, Tsuda K, Katagiri F (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71: 194-204
46. Iizasa E, Mitsutomi M, Nagano Y (2010) Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem 285: 2996-3004
47. 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. Proc Natl Acad Sci USA 103: 11086-11091
48. Karimi M, Bleys A, Vanderhaeghen R, Hilson P (2007a) Building blocks for plant gene assembly. Plant Physiol 145: 1183-1191
49. Karimi M, Depicker A, Hilson P (2007b) Recombinational cloning with plant gateway vectors. Plant Physiol 145: 1144-1154
50. Kariola T, Brader G, Helenius E, Li J, Heino P, Palva ET (2006) EARLY RESPONSIVE TO DEHYDRATION 15, a negative regulator of abscisic acid responses in Arabidopsis. Plant Physiol 142: 1559-1573
51. Kim TH, Hauser F, Ha T, Xue S, Böhmer M, Nishimura N, Munemasa S, Hubbard K, Peine N, Lee BH, et al (2011) Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr Biol 21: 990-997
52. Koornneef M, Léon-Kloosterziel KM, Schwartz SH, Zeevaart JAD (1998) The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. Plant Physiol Biochem 36: 83-89
53. Kumar V, Parkhi V, Kenerley CM, Rathore KS (2009) Defense-related gene expression and enzyme activities in transgenic cotton plants expressing an endochitinase gene from Trichoderma virens in response to interaction with Rhizoctonia solani. Planta 230: 277-291
54. L'Haridon F, Besson-Bard A, Binda M, Serrano M, Abou-Mansour E, Balet F, Schoonbeek HJ, Hess S, Mir R, Léon J, et al (2011) A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity. PLoS Pathog 7: e1002148
55. Laby RJ, Kincaid MS, Kim D, Gibson SI (2000) The Arabidopsis sugarinsensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23: 587-596
56. Lång V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20: 951-962
57. Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J, Choi J, Kang Ch, Qiu J, Stacey G (2013) Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341: 1384-1387
58. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630-633
59. Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Fan F, Wang J, Jin C, Chang J, et al (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336: 1160-1164
60. Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24: 183-193
61. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068
62. Mackey D, McFall AJ (2006) MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61: 1365-1371
63. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, et al (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640
64. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410
65. Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8: 409-414
66. Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455
67. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613-19618
68. Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH, UrquhartW, Klessig DF, Kim SK, Nambara E, Yoshioka K (2010) The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol 152: 1901-1913
69. Murashige T, Skoog F (1962) Revised medium for rapid growth and bioassays with tobacco cultures. Physiol Plant 15: 437-479
70. NewmanMA, Dow JM, Molinaro A, Parrilli M (2007) Priming, induction and modulation of plant defence responses by bacterial lipopolysaccharides. J Endotoxin Res 13: 69-84
71. Padmanabhan M, Cournoyer P, Dinesh-Kumar SP (2009) The leucine-rich repeat domain in plant innate immunity: a wealth of possibilities. Cell Microbiol 11: 191-198
72. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071
73. Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF (1996) Pathogeninduced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8: 2309-2323
74. Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, Lipka V (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitinbinding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem 285: 28902-28911
75. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45
76. Povero G, Loreti E, Pucciariello C, Santaniello A, Di Tommaso D, Di Tommaso G, Kapetis D, Zolezzi F, Piaggesi A, Perata P (2011) Transcript profiling of chitosan-treated Arabidopsis seedlings. J Plant Res 124: 619-629
77. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26: 3923-3935
78. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-yearold vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91: 11841-11843
79. Sánchez-Vallet A, López G, Ramos B, Delgado-Cerezo M, Riviere MP, Llorente F, Fernández PV, Miedes E, Estevez JM, Grant M, et al (2012) Disruption of abscisic acid signaling constitutively activates Arabidopsis resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant Physiol 160: 2109-2124
80. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, et al (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214
81. Siewers V, Smedsgaard J, Tudzynski P (2004) The P450 monooxygenase BcABA1 is essential for abscisic acid biosynthesis in Botrytis cinerea. Appl Environ Microbiol 70: 3868-3876
82. Tanaka K, Nguyen CT, Liang Y, Cao Y, Stacey G (2012) Role of LysM receptors in chitin-triggered plant innate immunity. Plant Signal Behav 8: e22598
83. 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. Plant Cell 15: 317-330
84. Ton J, Mauch-Mani B (2004) β-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38: 119-130
85. van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, de Vries SC (2001) N-Acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol 125: 1880-1890
86. Wan J, Tanaka K, Zhang XC, Son GH, Brechenmacher L, Nguyen TH, Stacey G (2012) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 160: 396-406
87. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481
88. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Freidit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1: 198-217
89. Willmann R, Lajunen HM, Erbs G, Newman MA, Kolb D, Tsuda K, Katagiri F, Fliegmann J, Bono JJ, Cullimore JV, et al (2011) Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci USA 108: 19824-19829
90. Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, et al (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20: 1678-1692
91. Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, Berkowitz G, Klessig DF (2006) The chimeric Arabidopsis CYCLIC NUCLEOTIDEGATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18: 747-763
92. Zhang B, Ramonell K, Somerville S, Stacey G (2002) Characterization of early, chitin-induced gene expression in Arabidopsis. Mol Plant Microbe Interact 15: 963-970
93. Zhang XC, Cannon SB, Stacey G (2009) Evolutionary genomics of LysM genes in land plants. BMC Evol Biol 9: 183
94. Zhang XC, Wu X, Findley S, Wan J, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144: 623-636
95. Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15: 2636-2646
96. Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11: 2419-2428
97. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632
98. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760
99. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767