Wrky transcription factors phosphorylated by mapk regulate a plant immune nadph oxidase in nicotiana benthamiana

Plant Cell

Volumn 27, Issue 9, 2015, Pages 2645-2663

  Adachi, Hiroaki ^a   Nakano, Takaaki ^a   Miyagawa, Noriko ^b   Ishihama, Nobuaki ^c   Yoshioka, Miki ^a   Katou, Yuri ^a   Yaeno, Takashi ^d   Shirasu, Ken ^c   Yoshioka, Hirofumi ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b ZEN NOH Agricultural R and D Center   (Japan)

^c RIKEN Center for Sustainable Resource Science   (Japan)

^d EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSCRIPTION FACTOR;

GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHOSPHORYLATION; PHYTOPHTHORA INFESTANS; PLANT IMMUNITY; POTATO; PROMOTER REGION; REGULATORY SEQUENCE; SIGNAL TRANSDUCTION; TOBACCO; TRANSGENIC PLANT;

GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MAP KINASE SIGNALING SYSTEM; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; PHOSPHORYLATION; PHYTOPHTHORA INFESTANS; PLANT IMMUNITY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; REGULATORY SEQUENCES, NUCLEIC ACID; SOLANUM TUBEROSUM; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84943740904     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00213     Document Type: Article

References (86)

1. Adachi, H., and Yoshioka, H. (2015). Kinase-mediated orchestration of NADPH oxidase in plant immunity. Brief. Funct. Genomics 14: 253-259.
2. Andreasson, E., et al. (2005). The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 24: 2579-2589.
3. Asai, S., Ichikawa, T., Nomura, H., Kobayashi, M., Kamiyoshihara, Y., Mori, H., Kadota, Y., Zipfel, C., Jones, J.D.G., and Yoshioka, H. (2013). The variable domain of a plant calcium-dependent protein kinase (CDPK) confers subcellular localization and substrate recognition for NADPH oxidase. J. Biol. Chem. 288: 14332-14340.
4. Asai, S., Ohta, K., and Yoshioka, H. (2008). MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20: 1390-1406.
5. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M., and Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
6. Blume, B., Nürnberger, T., Nass, N., and Scheel, D. (2000). Receptormediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12: 1425-1440.
7. Bos, J.I., Kanneganti, T.D., Young, C., Cakir, C., Huitema, E., Win, J., Armstrong, M.R., Birch, P.R., and Kamoun, S. (2006). The Cterminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J. 48: 165-176.
8. Chai, H.B., and Doke, N. (1987). Activation of the potential of potato leaf tissue to react hypersensitively to Phytophthora infestans by cytospore germination fluid and the enhancement of this potential by calcium ions. Physiol. Mol. Plant Pathol. 30: 27-37.
9. Chaparro-Garcia, A., Wilkinson, R.C., Gimenez-Ibanez, S., Findlay, K., Coffey, M.D., Zipfel, C., Rathjen, J.P., Kamoun, S., and Schornack, S. (2011). The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen phytophthora infestans in Nicotiana benthamiana. PLoS One 6: e16608.
10. Chen, C., and Chen, Z. (2000). Isolation and characterization of two pathogen- and salicylic acid-induced genes encoding WRKY DNAbinding proteins from tobacco. Plant Mol. Biol. 42: 387-396.
11. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nürnberger, T., Jones, J.D.G., Felix, G., and Boller, T. (2007). A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
12. Coll, N.S., Epple, P., and Dangl, J.L. (2011). Programmed cell deathin the plant immune system. Cell Death Differ. 18: 1247-1256.
13. de la Torre, F., Gutiérrez-Beltrán, E., Pareja-Jaime, Y., Chakravarthy, S., Martin, G.B., and del Pozo, O. (2013). The tomato calcium sensor Cbl10 and its interacting protein kinase Cipk6 define a signaling pathway in plant immunity. Plant Cell 25: 2748-2764.
14. Du, J., et al. (2015). Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat. Plants 1: 15034.
15. Eulgem, T., and Somssich, I.E. (2007). Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10: 366-371.
16. Gao, X., Chen, X., Lin, W., Chen, S., Lu, D., Niu, Y., Li, L., Cheng, C., McCormack, M., Sheen, J., Shan, L., and He, P. (2013). Bifurcation of Arabidopsis NLR immune signaling via Ca²⁺-dependent protein kinases. PLoS Pathog. 9: e1003127.
17. Glotin, A.L., Calipel, A., Brossas, J.Y., Faussat, A.M., Tréton, J., and Mascarelli, F. (2006). Sustained versus transient ERK1/2 signaling underlies the anti- and proapoptotic effects of oxidative stress in human RPE cells. Invest. Ophthalmol. Vis. Sci. 47: 4614-4623.
18. 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.
19. Hao, H., Fan, L., Chen, T., Li, R., Li, X., He, Q., Botella, M.A., and Lin, J. (2014). Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26: 1729-1745.
20. Heese, A., Hann, D.R., Gimenez-Ibanez, S., Jones, A.M., He, K., Li, J., Schroeder, J.I., Peck, S.C., and Rathjen, J.P. (2007). The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104: 12217-12222.
21. Ishihama, N., Adachi, H., Yoshioka, M., and Yoshioka, H. (2014). In vivo phosphorylation of WRKY transcription factor by MAPK. Methods Mol. Biol. 1171: 171-181.
22. Ishihama, N., Yamada, R., Yoshioka, M., Katou, S., and Yoshioka, H. (2011). Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23: 1153-1170.
23. Ishihama, N., and Yoshioka, H. (2012). Post-translational regulation of WRKY transcription factors in plant immunity. Curr. Opin. Plant Biol. 15: 431-437.
24. Jones, J.D.G., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323-329.
25. Journot-Catalino, N., Somssich, I.E., Roby, D., and Kroj, T. (2006). The transcription factors WRKY11 andWRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18: 3289-3302.
26. Kadota, Y., and Shirasu, K. (2012). The HSP90 complex of plants. Biochim. Biophys. Acta 1823: 689-697.
27. Kadota, Y., Sklenar, J., Derbyshire, P., Stransfeld, L., Asai, S., Ntoukakis, V., Jones, J.D.G., Shirasu, K., Menke, F., Jones, A., and Zipfel, C. (2014). Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54: 43-55.
28. Kamoun, S., van West P., Vleeshouwers, V.G., de Groot, K.E., and Govers, F. (1998). Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10: 1413-1426.
29. Kanneganti, T.D., Huitema, E., Cakir, C., and Kamoun, S. (2006). Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans Nepl-like protein PiNPP1.1 and INF1 elicitin. Mol. Plant Microbe Interact. 19: 854-863.
30. Kanzaki, H., Saitoh, H., Ito, A., Fujisawa, S., Kamoun, S., Katou, S., Yoshioka, H., and Terauchi, R. (2003). Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4: 383-391.
31. Kaufmann, K., Muiño, J.M., Østerås, M., Farinelli, L., Krajewski, P., and Angenent, G.C. (2010). Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat. Protoc. 5: 457-472.
32. Kobayashi, M., Ishihama, N., Yoshioka, H., Takabatake, R., Tsuda, S., Seo, S., Ohashi, Y., and Mitsuhara, I. (2010). Analyses of the cis-regulatory regions responsible for the transcriptional activation of the N resistance gene by Tobacco mosaic virus. J. Phytopathol. 158: 826-828.
33. Kobayashi, M., Kawakita, K., Maeshima, M., Doke, N., and Yoshioka, H. (2006). Subcellular localization of Strboh proteins and NADPH-dependent O2(-)-generating activity in potato tuber tissues. J. Exp. Bot. 57: 1373-1379.
34. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K., Doke, N., and Yoshioka, H. (2007). Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080.
35. Kobayashi, M., Yoshioka, M., Asai, S., Nomura, H., Kuchimura, K., Mori, H., Doke, N., and Yoshioka, H. (2012). StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst. New Phytol. 196: 223-237.
36. Le Roux, C., et al. (2015). A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161: 1074-1088.
37. Li, G., Meng, X., Wang, R., Mao, G., Han, L., Liu, Y., and Zhang, S. (2012). Dual-level regulation of ACC synthase activity by MPK3/ MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet. 8: e1002767.
38. Li, L., Li, M., Yu, L., Zhou, Z., Liang, X., Liu, Z., Cai, G., Gao, L., Zhang, X., Wang, Y., Chen, S., and Zhou, J.M. (2014). The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15: 329-338.
39. Lu, D., Lin, W., Gao, X., Wu, S., Cheng, C., Avila, J., Heese, A., Devarenne, T.P., He, P., and Shan, L. (2011). Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439-1442.
40. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., and Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23: 1639-1653.
41. Menke, F.L., Kang, H.G., Chen, Z., Park, J.M., Kumar, D., and Klessig, D.F. (2005). Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol. Plant Microbe Interact. 18: 1027-1034.
42. Mersmann, S., Bourdais, G., Rietz, S., and Robatzek, S. (2010). Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol. 154: 391-400.
43. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., Dangl, J.L., and Mittler, R. (2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2: ra45.
44. Mur, L.A., Kenton, P., Lloyd, A.J., Ougham, H., and Prats, E. (2008). The hypersensitive response; the centenary is upon us but how much do we know? J. Exp. Bot. 59: 501-520.
45. Murphy, L.O., MacKeigan, J.P., and Blenis, J. (2004). A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol. Cell. Biol. 24: 144-153.
46. Murphy, L.O., Smith, S., Chen, R.H., Fingar, D.C., and Blenis, J. (2002). Molecular interpretation of ERK signal duration by immediate early gene products. Nat. Cell Biol. 4: 556-564.
47. Nakano, M., Nishihara, M., Yoshioka, H., Takahashi, H., Sawasaki, T., Ohnishi, K., Hikichi, Y., and Kiba, A. (2013). Suppression of DS1 phosphatidic acid phosphatase confirms resistance to Ralstonia solanacearum in Nicotiana benthamiana. PLoS One 8: e75124.
48. Nakashima, A., Chen, L., Thao, N.P., Fujiwara, M., Wong, H.L., Kuwano, M., Umemura, K., Shirasu, K., Kawasaki, T., and Shimamoto, K. (2008). RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell 20: 2265-2279.
49. Noirot, E., Der, C., Lherminier, J., Robert, F., Moricova, P., Kiêu, K., Leborgne-Castel, N., Simon-Plas, F., and Bouhidel, K. (2014). Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein. J. Exp. Bot. 65: 5011-5022.
50. Pandey, S.P., and Somssich, I.E. (2009). The role of WRKY transcription factors in plant immunity. Plant Physiol. 150: 1648-1655.
51. Park, H.J., Miura, Y., Kawakita, K., Yoshioka, H., and Doke, N. (1998). Physiological mechanisms of a sub-systemic oxidative burst triggered by elicitor-induced local oxidative burst in potato tuber slices. Plant Cell Physiol. 39: 1218-1225.
52. Peart, J.R., et al. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99: 10865-10869.
53. Pedley, K.F., and Martin, G.B. (2005). Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol. 8: 541-547.
54. Popescu, S.C., Popescu, G.V., Bachan, S., Zhang, Z., Gerstein, M., Snyder, M., and Dinesh-Kumar, S.P. (2009). MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23: 80-92.
55. Ratcliff, F., Martin-Hernandez, A.M., and Baulcombe, D.C. (2001). Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 25: 237-245.
56. Ren, D., Yang, K.Y., Li, G.J., Liu, Y., and Zhang, S. (2006). Activation of Ntf4, a tobacco mitogen-activated protein kinase, during plant defense response and its involvement in hypersensitive responselike cell death. Plant Physiol. 141: 1482-1493.
57. Robatzek, S., Chinchilla, D., and Boller, T. (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20: 537-542.
58. Rushton, P.J., Somssich, I.E., Ringler, P., and Shen, Q.J. (2010). WRKY transcription factors. Trends Plant Sci. 15: 247-258.
59. Sabbagh, W., Jr., Flatauer, L.J., Bardwell, A.J., and Bardwell, L. (2001). Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol. Cell 8: 683-691.
60. Sagi, M., and Fluhr, R. (2001). Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126: 1281-1290.
61. Segonzac, C., Feike, D., Gimenez-Ibanez, S., Hann, D.R., Zipfel, C., and Rathjen, J.P. (2011). Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol. 156: 687-699.
62. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., and Ohashi, Y. (1995). Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270: 1988-1992.
63. Sheikh, A.H., Raghuram, B., Eschen-Lippold, L., Scheel, D., Lee, J., and Sinha, A.K. (2014). Agroinfiltration by cytokinin-producing Agrobacterium sp. strain GV3101 primes defense responses in Nicotiana tabacum. Mol. Plant Microbe Interact. 27: 1175-1185.
64. Shen, Q.H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Ulker, B., Somssich, I.E., and Schulze-Lefert, P. (2007). Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098-1103.
65. Smith, J.M., Salamango, D.J., Leslie, M.E., Collins, C.A., and Heese, A. (2014). Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol. 164: 440-454.
66. Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., and Mittler, R. (2011). Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14: 691-699.
67. Takahashi, A., Casais, C., Ichimura, K., and Shirasu, K. (2003). HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 11777-11782.
68. Tanaka, S., Ishihama, N., Yoshioka, H., Huser, A., O’Connell, R., Tsuji, G., Tsuge, S., and Kubo, Y. (2009). The Colletotrichum orbiculare SSD1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway. Plant Cell 21: 2517-2526.
69. Torres, M.A. (2010). ROS in biotic interactions. Physiol. Plant. 138: 414-429.
70. Torres, M.A., Dangl, J.L., and Jones, J.D.G. (2002). Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99: 517-522.
71. Traverse, S., Gomez, N., Paterson, H., Marshall, C., and Cohen, P. (1992). Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288: 351-355.
72. Tsuda, K., and Katagiri, F. (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13: 459-465.
73. Tsuda, K., Mine, A., Bethke, G., Igarashi, D., Botanga, C.J., Tsuda, Y., Glazebrook, J., Sato, M., and Katagiri, F. (2013). Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLoS Genet. 9: e1004015.
74. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
75. Wong, H.L., Pinontoan, R., Hayashi, K., Tabata, R., Yaeno, T., Hasegawa, K., Kojima, C., Yoshioka, H., Iba, K., Kawasaki, T., and Shimamoto, K. (2007). Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19: 4022-4034.
76. Yaeno, T., Li, H., Chaparro-Garcia, A., Schornack, S., Koshiba, S., Watanabe, S., Kigawa, T., Kamoun, S., and Shirasu, K. (2011). Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc. Natl. Acad. Sci. USA 108: 14682-14687.
77. Yamamizo, C., Kuchimura, K., Kobayashi, A., Katou, S., Kawakita, K., Jones, J.D.G., Doke, N., and Yoshioka, H. (2006). Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiol. 140: 681-692.
78. Yang, K.Y., Liu, Y., and Zhang, S. (2001). Activation of a mitogenactivated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98: 741-746.
79. Yoshioka, H., Mase, K., Yoshioka, M., Kobayashi, M., and Asai, S. (2011). Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity. Nitric Oxide 25: 216-221.
80. Yoshioka, H., Numata, N., Nakajima, K., Katou, S., Kawakita, K., Rowland, O., Jones, J.D.G., and Doke, N. (2003). Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706-718.
81. Yoshioka, H., Sugie, K., Park, H.J., Maeda, H., Tsuda, N., Kawakita, K., and Doke, N. (2001). Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol. Plant Microbe Interact. 14: 725-736.
82. Zhang, J., et al. (2007). A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1: 175-185.
83. Zhang, S., and Klessig, D.F. (1997). Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9: 809-824.
84. Zhang, Y., Zhu, H., Zhang, Q., Li, M., Yan, M., Wang, R., Wang, L., Welti, R., Zhang, W., and Wang, X. (2009). Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21: 2357-2377.
85. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D.G., Felix, G., and Boller, T. (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.
86. Zuo, J., Niu, Q.W., and Chua, N.H. (2000). Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24: 265-273