Phosphoinositide-signaling is one component of a robust plant defense response

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Hung, Chiu Yueh ^a,b   Aspesi, Peter ^a,c   Hunter, Melissa R ^a,d   Lomax, Aaron W ^a,e   Perera, Imara Y ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Arabidopsis; Ca2+; InsP3; Phosphoinositides; Plant defense signaling; Salicylic acid; SAR

Indexed keywords

EID: 84979598521     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00267     Document Type: Article

References (97)

1. Andersson, M. X., Kourtchenko, O., Dangl, J. L., Mackey, D., and Ellerström, M. (2006). Phospholipase−dependent signalling during the AvrRpm1−and AvrRpt2−induced disease resistance responses in Arabidopsis thaliana. Plant J. 47, 947-959. doi: 10.1111/j.1365-313X.2006.02844.x
2. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W.-L., Gomez-Gomez, L., et al. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983. doi: 10.1038/415977a
3. Boudsocq, M., and Sheen, J. (2013). CDPKs in immune and stress signaling. Trends Plant Sci. 18, 30-40. doi: 10.1016/j.tplants.2012.08.008
4. 2+sensor protein kinases. Nature 464, 418-422. doi: 10.1038/nature08794
5. Canonne, J., Froidure-Nicolas, S., and Rivas, S. (2011). Phospholipases in action during plant defense signaling. Plant Signal. Behav. 6, 13-18. doi: 10.4161/psb.6.1.14037
6. Cao, F. Y., Yoshioka, K., and Desveaux, D. (2011). The roles of ABA in plant-pathogen interactions. J. Plant Res. 124, 489-499. doi: 10.1007/s10265-011-0409-y
7. Carvalho, H. H., Silva, P. A., Mendes, G. C., Brustolini, O. J., Pimenta, M. R., Gouveia, B. C., et al. (2014). The endoplasmic reticulum binding protein BiP displays dual function in modulating cell death events. Plant Physiol. 164, 654-670. doi: 10.1104/pp.113.231928
8. Chan, C. W., Wohlbach, D. J., Rodesch, M. J., and Sussman, M. R. (2008). Transcriptional changes in response to growth of Arabidopsis in high external calcium. FEBS Lett. 582, 967-976. doi: 10.1016/j.febslet.2008.02.043
9. Chaturvedi, R., Krothapalli, K., Makandar, R., Nandi, A., Sparks, A. A., Roth, M. R., et al. (2008). Plastid ω3−fatty acid desaturase−dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J. 54, 106-117. doi: 10.1111/j.1365-313X.2007.03400.x
10. Delage, E., Puyaubert, J., Zachowski, A., and Ruelland, E. (2013). Signal transduction pathways involving phosphatidylinositol 4-phosphate and phosphatidylinositol 4, 5-bisphosphate: convergences and divergences among eukaryotic kingdoms. Prog. Lipid Res. 52, 1-14. doi: 10.1016/j.plipres.2012.08.003
11. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al. (1994). A central role of salicylic acid in plant disease resistance. Science 266, 1247-1250. doi: 10.1126/science.266.5188.1247
12. Delledonne, M. (2005). NO news is good news for plants. Curr. Opin. Plant Biol. 8, 390-396. doi: 10.1016/j.pbi.2005.05.002
13. de Torres Zabala, M., Bennett, M. H., Truman, W. H., and Grant, M. R. (2009). Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J. 59, 375-386. doi: 10.1111/j.1365-313X.2009.03875.x
14. Dewdney, J., Reuber, T. L., Wildermuth, M. C., Devoto, A., Cui, J., Stutius, L. M., et al. (2000). Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 24, 205-218. doi: 10.1046/j.1365-313x.2000.00870.x
15. Dodd, A. N., Kudla, J., and Sanders, D. (2010). The language of calcium signaling. Annu. Rev. Plant Biol. 61, 593-620. doi: 10.1146/annurev-arplant-070109-104628
16. Dong, X. (2004). NPR1, all things considered. Curr. Opin. Plant Biol. 7, 547-552. doi: 10.1016/j.pbi.2004.07.005
17. 2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457, 1154-1158. doi: 10.1038/nature07612
18. Dubiella, U., Seybold, H., Durian, G., Komander, E., Lassig, R., Witte, C. P., et al. (2013). Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. U.S.A. 110, 8744-8749. doi: 10.1073/pnas.1221294110
19. Durrant, W. E., and Dong, X. (2004). Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209. doi: 10.1146/annurev.phyto.42.040803.140421
20. Felix, G., Duran, J. D., Volko, S., and Boller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276. doi: 10.1046/j.1365-313X.1999.00265.x
21. Finkler, A., Ashery-Padan, R., and Fromm, H. (2007). CAMTAs: calmodulin-binding transcription activators from plants to human. FEBS Lett. 581, 3893-3898. doi: 10.1016/j.febslet.2007.07.051
22. Fu, Z. Q., and Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839-863. doi: 10.1146/annurev-arplant-042811-105606
23. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., et al. (1993). Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754-756. doi: 10.1126/science.261.5122.754
24. Galon, Y., Nave, R., Boyce, J. M., Nachmias, D., Knight, M. R., and Fromm, H. (2008). Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett. 582, 943-948. doi: 10.1016/j.febslet.2008.02.037
25. Gao, Q. M., Kachroo, A., and Kachroo, P. (2014). Chemical inducers of systemic immunity in plants. J. Exp. Bot. 65, 849-1855. doi: 10.1093/jxb/eru010
26. Gillaspy, G. E. (2011). The cellular language of myo−inositol signaling. New Phytol. 192, 823-839. doi: 10.1111/j.1469-8137.2011.03939.x
27. Gillaspy, G. E. (2013). “The role of phosphoinositides and inositol phosphates in plant cell signaling,” in Lipid-Mediated Protein Signaling, ed D. G. S. Capelluto (Dordrecht: Springer), 141-157. doi: 10.1007/978-94-007-6331-9_8
28. Gimenez-Ibanez, S., and Rathjen, J. P. (2010). The case for the defense: plants versus Pseudomonas syringae. Microbes Infect. 12, 428-437. doi: 10.1016/j.micinf.2010.03.002
29. Gomez-Gomez, L., Felix, G., and Boller, T. (1999). A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277-284. doi: 10.1046/j.1365-313X.1999.00451.x
30. Grant, M., Brown, I., Adams, S., Knight, M., Ainslie, A., and Mansfield, J. (2000). The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 23, 441-450. doi: 10.1046/j.1365-313x.2000.00804.x
31. Gust, A. A., Biswas, R., Lenz, H. D., Rauhut, T., Ranf, S., Kemmerling, B., et al. (2007). Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 282, 32338-32348. doi: 10.1074/jbc.M704886200
32. Im, Y. J., Heilmann, I., and Perera, I. Y. (2011). “The hull of fame: lipid signaling in the plasma membrane,” in The Plant Plasma Membrane, Plant Cell Monographs, Vol. 19, eds A. S. Murphy, B. Schulz, and W. Peer (Berlin; Heidelberg: Springer), 437-455.
33. Im, Y. J., Phillippy, B. Q., and Perera, I. Y. (2010). “InsP3 in plant cells,” in Lipid Signaling in Plants, ed T. Munnik (Berlin; Heidelberg: Springer), 145-160.
34. 2+-associated opening of plasma membrane anion channels. Plant J. 62, 367-378. doi: 10.1111/j.1365-313X.2010.04155.x
35. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
36. Kachroo, A., and Kachroo, P. (2009). Fatty acid-derived signals in plant defense. Annu. Rev. Phytopathol. 47, 153-176. doi: 10.1146/annurev-phyto-080508-081820
37. Kadota, Y., Sklenar, J., Derbyshire, P., Stransfeld, L., Asai, S., Ntoukakis, V., et al. (2014). Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell. 54, 43-55. doi: 10.1016/j.molcel.2014.02.021
38. Katagiri, F., Thilmony, R., and He, S. Y. (2002). “The Arabidopsis thaliana-Pseudomonas syringae interaction,” in The Arabidopsis Book, eds C. R. Somerville and E. M. Meyerowitz (Rockville, MD: American Society of Plant Biologists), 1:e0039. Available online at: http://www.aspb.org/publications/arabidopsis
39. Kim, M. C., Chung, W. S., Yun, D. J., and Cho, M. J. (2009). Calcium and calmodulin-mediated regulation of gene expression in plants. Mol. Plant 2, 13-21. doi: 10.1093/mp/ssn091
40. Knight, H., Trewavas, A. J., and Knight, M. R. (1996). Cold calcium signalling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8, 489-503.
41. König, S., Mosblech, A., and Heilmann, I. (2007). Stress-inducible and constitutive phosphoinositide pools have distinctive fatty acid patterns in Arabidopsis thaliana. FASEB J. 21, 1958-1967. doi: 10.1096/fj.06-7887com
42. Krinke, O., Flemr, M., Vergnolle, C., Collin, S., Renou, J. P., Taconnat, L., et al. (2009). Phospholipase D activation is an early component of the salicylic acid signaling pathway in Arabidopsis cell suspensions. Plant Physiol. 150, 424-436. doi: 10.1104/pp.108.133595
43. Krinke, O., Novotná, Z., Valentová, O., and Martinec, J. (2007a). Inositol trisphosphate receptor in higher plants: is it real?. J. Exp. Bot. 58, 361-376. doi: 10.1093/jxb/erl220
44. Krinke, O., Ruelland, E., Valentová, O., Vergnolle, C., Renou, J. P., Taconnat, L., et al. (2007b). Phosphatidylinositol 4-kinase activation is an early response to salicylic acid in Arabidopsis suspension cells. Plant Physiol. 144, 1347-1359. doi: 10.1104/pp.107.100842
45. Lamb, C., and Dixon, R. A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Biol. 48, 251-275. doi: 10.1146/annurev.arplant.48.1.251
46. Lemtiri-Chlieh, F., MacRobbie, E. A., Webb, A. A., Manison, N. F., Brownlee, C., and Skepper, J. N. (2003). Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc. Natl. Acad. Sci. U.S.A. 100, 10091-10095. doi: 10.1073/pnas.1133289100
47. Li, J., Brader, G., and Palva, E. T. (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16, 319-331. doi: 10.1105/tpc.016980
48. Li, L., Li, M., Yu, L., Zhou, Z., Liang, X., Liu, Z., et al. (2014). The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329-338. doi: 10.1016/j.chom.2014.02.009
49. Lu, H. (2009). Dissection of salicylic acid-mediated defense signaling networks. Plant Signal. Behav. 4. 713-717. doi: 10.4161/psb.4.8.9173
50. Ma, W., and Berkowitz, G. A. (2007). The grateful dead: calcium and cell death in plant innate immunity. Cell. Microbial. 9, 2571-2585. doi: 10.1111/j.1462-5822.2007.01031.x
51. 2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytol. 190, 566-572. doi: 10.1111/j.1469-8137.2010.03577.x
52. 2+ elevation and downstream immune signaling in plants. Proc. Natl. Acad. Sci. U.S.A. 109, 19852-19857. doi: 10.1073/pnas.1205448109
53. Maldonado, A. M., Doerner, P., Dixon, R. A., Lamb, C. J., and Cameron, R. K. (2002). A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399-403. doi: 10.1038/nature00962
54. Manzoor, H., Chiltz, A., Madani, S., Vatsa, P., Schoefs, B., Pugin, A., et al. (2012). Calcium signatures and signaling in cytosol and organelles of tobacco cells induced by plant defense elicitors. Cell Calcium 51, 434-444. doi: 10.1016/j.ceca.2012.02.006
55. McAinsh, M. R., and Pittman, J. K. (2009). Shaping the calcium signature. New Phytol. 181, 275-294. doi: 10.1111/j.1469-8137.2008.02682.x
56. Meijer, H. J., and Munnik, T. (2003). Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 54, 265-306. doi: 10.1146/annurev.arplant.54.031902.134748
57. Mosblech, A., König, S., Stenzel, I., Grzeganek, P., Feussner, I., and Heilmann, I. (2008). Phosphoinositide and inositolpolyphosphate signalling in defense responses of Arabidopsis thaliana challenged by mechanical wounding. Mol. Plant 1, 249-261. doi: 10.1093/mp/ssm028
58. Mosblech, A., Thurow, C., Gatz, C., Feussner, I., and Heilmann, I. (2011). Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J. 65, 949-957. doi: 10.1111/j.1365-313X.2011.04480.x
59. Munnik, T., and Nielsen, E. (2011). Green light for polyphosphoinositide signals in plants. Curr. Opin. Plant Biol. 14, 489-497. doi: 10.1016/j.pbi.2011.06.007
60. Murphy, A. M., Otto, B., Brearley, C. A., Carr, J. P., and Hanke, D. E. (2008). A role for inositol hexakisphosphate in the maintenance of basal resistance to plant pathogens. Plant J. 56, 638-652. doi: 10.1111/j.1365-313X.2008.03629.x
61. Nandi, A., Welti, R., and Shah, J. (2004). The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell 16, 465-477. doi: 10.1105/tpc.016907
62. Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T., et al. (2004). The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113-1128. doi: 10.1104/pp.103.036749
63. Ng, G., Seabolt, S., Zhang, C., Salimian, S., Watkins, T. A., and Lu, H. (2011). Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis. Genetics 189, 851-859. doi: 10.1534/genetics.111.132332
64. Nishimura, M. T., and Dangl, J. L. (2010). Arabidopsis and the plant immune system. Plant J. 61, 1053-1066. doi: 10.1111/j.1365-313X.2010.04131.x
65. Nomura, H., Komori, T., Uemura, S., Kanda, Y., Shimotani, K., Nakai, K., et al. (2012). Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Commun. 3, 926. doi: 10.1038/ncomms1926
66. Nürnberger, T., Brunner, F., Kemmerling, B., and Piater, L. (2004). Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249-266. doi: 10.1111/j.0105-2896.2004.0119.x
67. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987-D991. doi: 10.1093/nar/gkn807
68. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-116. doi: 10.1126/science.1147113
69. Perera, I. Y., Hung, C.-Y., Brady, S., Muday, G. K., and Boss, W. F. (2006). A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol. 140, 746-760. doi: 10.1104/pp.105.075119
70. Perera, I. Y., Hung, C.-Y., Moore, C. D., Stevenson-Paulik, J., and Boss, W. F. (2008). Transgenic Arabidopsis plants expressing the type 1 inositol 5-phosphatase exhibit increased drought tolerance and altered abscisic acid signaling. Plant Cell 20, 2876-2893. doi: 10.1105/tpc.108.061374
71. Perera, I. Y., Love, J., Heilmann, I., Thompson, W. F., and Boss, W. F. (2002). Up-regulation of phosphoinositide metabolism in tobacco cells constitutively expressing the human type I inositol polyphosphate 5-phosphatase. Plant Physiol. 129, 1795-1806. doi: 10.1104/pp.003426
72. Pokotylo, I., Kolesnikov, Y., Kravets, V., Zachowski, A., and Ruelland, E. (2014). Plant phosphoinositide-dependent phospholipases C: variations around a canonical theme. Biochimie 96, 144-157. doi: 10.1016/j.biochi.2013.07.004
73. Postel, S., and Kemmerling, B. (2009). Plant systems for recognition of pathogen-associated molecular patterns. Semin. Cell Dev. Biol. 20, 1025-1031. doi: 10.1016/j.semcdb.2009.06.002
74. 2+ channels. Proc. Natl. Acad. Sci. U.S.A. 107, 21193-21198. doi: 10.1073/pnas.1000191107
75. Qutob, D., Kemmerling, B., Brunner, F., Küfner, I., Engelhardt, S., Gust, A. A., et al. (2006). Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18, 3721-3744. doi: 10.1105/tpc.106.044180
76. Ranf, S., Eschen-Lippold, L., Pecher, P., Lee, J., and Scheel, D. (2011). Interplay between calcium signalling and early signaling elements during defence responses to microbe-or damage-associated molecular patterns. Plant J. 68, 100-113. doi: 10.1111/j.1365-313X.2011.04671.x
77. Reddy, A. S., Ali, G. S., Celesnik, H., and Day, I. S. (2011). Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 23, 2010-2032. doi: 10.1105/tpc.111.084988
78. Romeis, T., and Herde, M. (2014). From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Curr. Opin. Plant Biol. 20, 1-10. doi: 10.1016/j.pbi.2014.03.002
79. Sagi, M., and Fluhr, R. (2006). Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336-340. doi: 10.1104/pp.106.078089
80. Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108. doi: 10.1038/nprot.2008.73
81. Shah, J. (2005). Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annu. Rev. Phytol. 43, 229-260. doi: 10.1146/annurev.phyto.43.040204.135951
82. Sheard, L. B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T. R., et al. (2010). Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400-405. doi: 10.1038/nature09430
83. Stevenson, J. M., Perera, I. Y., Heilmann, I. I., Persson, S., and Boss, W. F. (2000). Inositol signaling and plant growth. Trends Plant Sci. 5, 252-258. doi: 10.1016/S1360-1385(00)01652-6
84. Tan, X., Calderon-Villalobos, L. I. A., Sharon, M., Zheng, C., Robinson, C. V., Estelle, M., et al. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645. doi: 10.1038/nature05731
85. Testerink, C., and Munnik, T. (2011). Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 62, 2349-2361. doi: 10.1093/jxb/err079
86. Torres, M. A., Jones, J. D. G., and Dangl, J. L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378. doi: 10.1104/pp.106.079467
87. Truman, W., and Glazebrook, J. (2012). Co-expression analysis identifies putative targets for CBP60g and SARD1 regulation. BMC Plant Biol. 12:216. doi: 10.1186/1471-2229-12-216
88. Tsuda, K., and Katagiri, F. (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13, 459-465. doi: 10.1016/j.pbi.2010.04.006
89. Vossen, J. H., Abd-El-Haliem, A., Fradin, E. F., van den Berg, G., Ekengren, S. K., Meijer, H. J., et al. (2010). Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J. 62, 224-239. doi: 10.1111/j.1365-313X.2010.04136.x
90. Walley, J. W., Kliebenstein, D. J., Bostock, R. M., and Dehesh, K. (2013). Fatty acids and early detection of pathogens. Curr. Opin. Plant Biol. 16, 520-526. doi: 10.1016/j.pbi.2013.06.011
91. Wang, D., Weaver, N. D., Kesarwani, M., and Dong, X. (2005). Induction of protein secretory pathway is required for systemic acquired resistance. Science 308, 1036-1040. doi: 10.1126/science.1108791
92. Weigel, R. R., Pfitzner, U. M., and Gatz, C. (2005). Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17, 1279-1291. doi: 10.1105/tpc.104.027441
93. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562-565. doi: 10.1038/35107108
94. Wurzinger, B., Mair, A., Pfister, B., and Teige, M. (2011). Cross-talk of calcium-dependent protein kinase and MAP kinase signaling. Plant Signal. Behav. 6, 8-12. doi: 10.4161/psb.6.1.14012
95. Zhang, Y., Xu, S., Ding, P., Wang, D., Cheng, Y. T., He, J., et al. (2010). Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. U.S.A. 107, 18220-18225. doi: 10.1073/pnas.1005225107
96. Zhou, N., Tootle, T. L., Tsui, F., Klessig, D. F., and Glazebrook, J. (1998). PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10, 1021-1030. doi: 10.1105/tpc.10.6.1021
97. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D., Felix, G., et al. (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764-767 doi: 10.1038/nature02485