All hands on deck-the role of chloroplasts, endoplasmic reticulum, and the nucleus in driving plant innate immunity

Molecular Plant-Microbe Interactions

Volumn 23, Issue 11, 2010, Pages 1368-1380

  Padmanabhan, Meenu S ^a   Dinesh Kumar, S P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS; CHLOROPLAST; ENDOPLASMIC RETICULUM; IMMUNOLOGY; INNATE IMMUNITY; PHYSIOLOGY; PLANT; PLANT DISEASE; REVIEW;

CELL NUCLEUS; CHLOROPLASTS; ENDOPLASMIC RETICULUM; IMMUNITY, INNATE; PLANT DISEASES; PLANTS;

EID: 78149332806     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-05-10-0113     Document Type: Review

References (130)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B. J., Daniels, M. J., and Parker, J. E. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 95:10306-10311.
2. Anelli, T., and Sitia, R. 2008. Protein quality control in the early secretory pathway. EMBO (Eur. Mol. Biol. Organ.) J. 27:315.
3. Ausubel, F. M. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6:973.
4. Azevedo, C., Betsuyaku, S., Peart, J., Takahashi, A., Noel, L., Sadanandom, A., Casais, C., Parker, J., and Shirasu, K. 2006. Role of SGT1 in resistance protein accumulation in plant immunity. EMBO (Eur. Mol. Biol. Organ.) J. 25:2007-2016.
5. Bernoux, M., Timmers, T., Jauneau, A., Briere, C., de Wit, P. J. G. M., Marco, Y., and Deslandes, L. 2008. RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 Effector. Plant Cell 20:2252-2264.
6. Boccara, M., Schwartz, W., Guiot, E., Vidal, G., Paepe, R. D., Dubois, A., and Boccara, A.-C. 2007. Early chloroplastic alterations analysed by optical coherence tomography during a harpin-induced hypersensitive response. Plant J. 50:338-346.
7. Boller, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern- recognition receptors. Annu. Rev. Plant Biol. 60:379-406.
8. Burch-Smith, T. M., Schiff, M., Caplan, J. L., Tsao, J., Czymmek, K., and Dinesh-Kumar, S. P. 2007. A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol. 5:e68. Published online.
9. Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., and Dong, X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57.
10. Caplan, J., Padmanabhan, M., and Dinesh-Kumar, S.P. 2008a. Plant NB- LRR immune receptors: From recognition to transcriptional reprogram- ming. Cell Host Microbe 3:126-135.
11. Caplan, J. L., Mamillapalli, P., Burch-Smith, T. M., Czymmek, K., and Dinesh-Kumar, S. P. 2008b. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132:449-462.
12. Caplan, J. L., Zhu, X., Mamillapalli, P., Marathe, R., Anandalakshmi, R., and Dinesh-Kumar, S. P. 2009. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cell Host Microbe 6:457-469.
13. Chandra-Shekara, A. C., Venugopal, S. C., Barman, S. R., Kachroo, A., and Kachroo, P. 2007. Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104:7277-7282.
14. Chen, L., Hamada, S., Fujiwara, M., Zhu, T., Thao, N. P., Wong, H. L., Krishna, P., Ueda, T., Kaku, H., Shibuya, N., Kawasaki, T., and Shimamoto, K. 2010. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7:185-196.
15. Cheng, Y. T., Germain, H., Wiermer, M., Bi, D., Xu, F., Garcia, A. V., Wirthmueller, L., Despres, C., Parker, J. E., Zhang, Y., and Li, X. 2009. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21:2503-2516.
16. Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., and Felix, G. 2006. The Arabidopsis receptor kinase FLS2b binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465-476.
17. Crofts, A. J., Leborgne-Castel, N., Pesca, M., Vitale, A., and Denecke, J. 1998. BiP and calreticulin form an abundant complex that is independent of endoplasmic reticulum stress. Plant Cell 10:813-824.
18. Dangl, J. L., and Jones, J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-833.
19. Danon, A., Miersch, O., Felix, G., Camp, R. G., and Apel, K. 2005. Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J. 41:68-80.
20. Deslandes, L., Olivier, J., Theulieres F. D. R., Hirsch, J., Feng, D. X., Bittner-Eddy, P., Beynon, J., and Marco, Y. 2002. Resistance to Ralsto- nia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl. Acad. Sci. U.S.A. 99:2404-2409.
21. Deslandes, L., Olivier, J., Peeters, N., Feng, D. X., Khounlotham, M., Boucher, C., Somssich, I., Genin, S. P., and Marco, Y. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. U.S.A. 100:8024-8029.
22. Dixit, R., Cyr, R., and Gilroy, S. 2006. Using intrinsically fluorescent proteins for plant cell imaging. Plant J. 45:599-615.
23. Dong, X. 2004. NPR1, all things considered. Curr. Opin. Plant Biol. 7:547-522.
24. Ellis, J. G., Dodds, P. N., and Lawrence, G. J. 2007. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu. Rev. Phytopathol. 45:289-306.
25. Feys, B. J., Moisan, L. J., Newman, M.-A., and Parker, J. E. 2001. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO (Eur. Mol. Biol. Organ.) J. 20:5400-5411.
26. Feys, B. J., Wiermer, M., Bhat, R. A., Moisan, L. J., Medina-Escobar, N., Neu, C., Cabral, A., and Parker, J. E. 2005. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17:2601-2613.
27. Fu, Z. Q., Guo, M., Jeong, B.-R., Tian, F., Elthon, T. E., Cerny, R. L., Staiger, D., and Alfano, J. R. 2007. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284-288
28. Geisler, M., Axelsen, K. B., Harper, J. F., and Palmgren, M. G. 2000. Molecular aspects of higher plant P-type Ca2+-ATPases. Biochim. Biophys. Acta Biomembranes 1465:52-78.
29. Genoud, T., Buchala, A. J., Chua, N.-H., and Metraux, J.-P. 2002. Phyto- chrome signalling modulates the SA-perceptive pathway in Arabidop-sis. Plant J. 31:87-95.
30. Gfeller, A., Dubugnon, L., Liechti, R., and Farmer, E. E. 2010. Jasmonate biochemical pathway. Sci. Signal. 3:cm3. Published online.
31. Gómez-Gómez, L., and Boller, T. 2000. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003.
32. Greenberg, J. T., Guo, A., Klessig, D. F., and Ausubel, F. M. 1994. Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551-563.
33. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G., and Greenberg, J. T. 2002. A functional screen for the type III (Hrp) secre- tome of the plant pathogen Pseudomonas syringae. Science 295:1722-1726.
34. Halterman, D., Zhou, F., Wei, F., Wise, R. P., and Schulze-Lefert, P. 2001. The MLA6 coiled-coil, NBS-IRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J. 25:335-348.
35. Halterman, D. A., and Wise, R. P. 2004. A single-amino acid substitution in the sixth leucine-rich repeat of barley MLA6 and MLA13 alleviates dependence on RAR1 for disease resistance signaling. Plant J. 38:215-226.
36. Heath, M. C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44:321-334.
37. Hu, G., Yalpani, N., Briggs, S. P., and Johal, G. S. 1998. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095-1106.
38. Hwang, C.-F., Bhakta, A. V., Truesdell, G. M., Pudlo, W. M., and Williamson, V. M. 2000. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12:1319-1330.
39. Ishikawa, A., Okamoto, H., Iwasaki, Y., and Asahi, T. 2001. A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. Plant J. 27:89-99.
40. Jelenska, J., Yao, N., Vinatzer, B. A., Wright, C. M., Brodsky, J. L., and Greenberg, J. T. 2007. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17:499-508.
41. Jiang, C.-J., Shimono, M., Maeda, S., Inoue, H., Mori, M., Hasegawa, M., Sugano, S., and Takatsuji, H. 2009. Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol. Plant-Microbe Interact. 22:820-829.
42. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323.
43. Kachroo, A., and Kachroo, P. 2009. Fatty acid-derived signals in plant defense. Annu. Rev. Phytopathol. 47:153-176.
44. Kachroo, A., Venugopal, S. C., Lapchyk, L., Falcone, D., Hildebrand, D., and Kachroo, P. 2004. Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101:5152-5157.
45. Kachroo, A., Shanklin, J., Whittle, E., Lapchyk, L., Hildebrand, D., and Kachroo, P. 2007. The Arabidopsis stearoyl-acyl carrier protein-desatu- rase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol. Biol. 63:257-271.
46. Kachroo, A., Fu, D.-Q., Havens, W., Navarre, D., Kachroo, P., and Ghabrial, S. A. 2008. An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Mol. Plant-Microbe Interact. 21:564-575.
47. Kachroo, P., Shanklin, J., Shah, J., Whittle, E. J., and Klessig, D. F. 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc. Natl. Acad. Sci. U.S.A. 98:9448-9453.
48. Kinkema, M., Fan, W., and Dong, X. 2000. Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339-2350.
49. Kleizen, B., and Braakman, I. 2004. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16:343-349.
50. Köster, M., Frahm, T., and Hauser, H. 2005. Nucleocytoplasmic shuttling revealed by FRAP and FLIP technologies. Curr. Opin. Biotechnol. 16:28-34.
51. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. 2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496-3507.
52. Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I., and Apel, K. 2007. Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104:672-677.
53. Lee, K. P., Kim, C., Landgraf, F., and Apel, K. 2007. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104:10270-10275.
54. Li, J., Zhao-Hui, C., Batoux, M., Nekrasov, V., Roux, M., Chinchilla, D., Zipfel, C., and Jones, J. D. G. 2009. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl. Acad. Sci. U.S.A. 106:15973-15978.
55. Li, X., Clarke, J. D., Zhang, Y., and Dong, X. 2001. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant-Microbe Interact. 14:1131-1139.
56. Liu, J., and Coaker, G. 2008. Nuclear trafficking during plant innate immunity. Mol. Plant 1:411-422.
57. Liu, Y., Ren, D., Pike, S., Pallardy, S., Gassmann, W., and Zhang, S. 2007. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J. 51:941-954.
58. Lorrain, S., Vailleau, F., Balague, C., and Roby, D. 2003. Lesion mimic mutants: Keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8:263-271.
59. Lu, X., Tintor, N., Mentzel, T., Kombrink, E., Boller, T., Robatzek, S., Schulze-Lefert, P., and Saijo, Y. 2009. Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl. Acad. Sci. U.S.A. 106:22522-22527.
60. Ma, W., and Berkowitz, G. A. 2007. The grateful dead: Calcium and cell death in plant innate immunity. Cell. Microbiol. 9:2571-2585.
61. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., Dangl, J. L., and Dietrich, R. A. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26:403-410.
62. Matarasso, N., Schuster, S., and Avni, A. 2005. A novel plant cysteine protease has a dual function as a regulator of 1-aminocyclopropane-1-car- boxylic acid synthase gene expression. Plant Cell 17:1205-1216.
63. Mateo, A., Muhlenbock, P., Rusterucci, C., Chang, C. C.-C., Miszalski, Z., Karpinska, B., Parker, J. E., Mullineaux, P. M., and Karpinski, S. 2004. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol. 136:2818-2830.
64. Meier, I. 2007. Composition of the plant nuclear envelope: Theme and variations. J. Exp. Bot. 58:27-34.
65. Mesaeli, N., Nakamura, K., Zvaritch, E., Dickie, P., Dziak, E., Krause, K.- H., Opas, M., MacLennan, D. H., and Michalak, M. 1999. Calreticulin is essential for cardiac development. J. Cell Biol. 144:857-868.
66. Mestre, P., and Baulcombe, D. C. 2006. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491-501.
67. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H., and Shibuya, N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104:19613-19618.
68. Mochizuki, N., Tanaka, R., Tanaka, A., Masuda, T., and Nagatani, A. 2008. The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 105:15184-15189.
69. Mou, Z., Fan, W., and Dong, X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-944.
70. Moulin, M., McCormac, A. C., Terry, M. J., and Smith, A. G. 2008. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc. Natl. Acad. Sci. U.S.A. 105:15178-15183.
71. Nekrasov, V., Li, J., Batoux, M., Roux, M., Chu, Z.-H., Lacombe, S., Rougon, A., Bittel, P., Kiss-Papp, M., Chinchilla, D., van Esse, H. P., Jorda, L., Schwessinger, B., Nicaise, V., Thomma, B. P. H. J., Molina, A., Jones, J. D. G., and Zipfel, C. 2009. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO (Eur. Mol. Biol. Organ.) J. 28:3428-3438.
72. Nixon, P. J., Barker, M., Boehm, M., de Vries, R., and Komenda, J. 2005. FtsH-mediated repair of the photosystem II complex in response to light stress. J. Exp. Bot. 56:357-363.
73. Noutoshi, Y., Ito, T., Seki, M., Nakashita, H., Yoshida, S., Marco, Y., Shirasu, K., and Shinozaki, K. 2005. A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-IRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J. 43:873-888.
74. Oelmüller, R., and Mohr, H. 1986. Photooxidative destruction of chloro- plasts and its consequences for expression of nuclear genes. Planta 167:106-113.
75. Oliver, J., Castro, A., Gaggero, C., Cascón, T., Schmelz, E., Castresana, C., and Ponce de Leon, I. 2009. ythium infection activates conserved plant defense responses in mosses. Planta 230:569-579.
76. op den Camp, R. G. L., Przybyla, D., Ochsenbein, C., Laloi, C., Kim, C., Danon, A., Wagner, D., Hideg, E., Gobel, C., Feussner, I., Nater, M., and Apel, K. 2003. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320-2332.
77. Orgil, U., Araki, H., Tangchaiburana, S., Berkey, R., and Xiao, S. 2007. In- traspecific genetic variations, fitness cost and benefit of RPW8, a disease resistance locus in Arabidopsis thaliana. Genetics 176:2317-2333.
78. Palma, K., Zhang, Y., and Li, X. 2005. An importin [alpha] homolog, MOS6, plays an important role in plant innate immunity. Curr. Biol. 15:1129-1135.
79. Park, C.-J., Bart, R., Chern, M., Canlas, P. E., Bai, W., and Ronald, P. C. 2010. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS ONE 5:e9262. Published online
80. Pattison, R. J., and Amtmann, A. 2009. N-glycan production in the endoplasmic reticulum of plants. Trends Plant Sci. 14:92-99.
81. Postel, S., and Kemmerling, B. 2009. Plant systems for recognition of pathogen-associated molecular patterns. Semin. Cell Dev. Biol. 20:1025-1031.
82. Pruinska, A., Tanner, G., Anders, I., Roca, M., and Hartensteiner, S. 2003. hlorophyll breakdown: Pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc. Natl. Acad. Sci. U.S.A. 100:15259-15264.
83. Pruzinska, A., Tanner, G., Aubry, S., Anders, I., Moser, S., Muller, T., Ongania, K. H., Krautler, B., Youn, J. Y., Liljegren, S. J., and Hortensteiner, S. 2005. Chlorophyll breakdown in senescent Arabidop- sis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol. 139:52-63.
84. Reddy, P., Sparvoli, A., Fagioli, C., Fassina, G., and Sitia, R. 1996. Formation of reversible disulfide bonds with the protein matrix of the endo- plasmic reticulum correlates with the retention of unassembled Ig light chains. EMBO (Eur. Mol. Biol. Organ.) J. 15:2077-2085.
85. Reiko, U. 2009. The endoplasmic reticulum stress signaling pathways in plants. BioFactors 35:326-331.
86. Richardson, C. E., Kooistra, T., and Kim, D. H. 2010. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463:1092-1095.
87. Sacco, M. A., Mansoor, S., and Moffett, P. 2007. A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx- mediated viral resistance. Plant J. 52:82-93.
88. Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K., Haweker, H., Dong, X., Robatzek, S., and Schulze-Lefert, P. 2009. Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO (Eur. Mol. Biol. Organ.) J. 28:3439.
89. Seo, S., Okamoto, M., Iwai, T., Iwano, M., Fukui, K., Isogai, A., Nakajima, N., and Ohashi, Y. 2000. Reduced levels of chloroplast FtsH protein in Tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 12:917-932.
90. Shen, Q.-H., Zhou, F., Bieri, S., Haizel, T., Shirasu, K., and Schulze-Lefert, P. 2003. Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. Plant Cell 15:732-744.
91. 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.
92. Shirasu, K. 2009. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu. Rev. Plant Biol. 60:139-164.
93. Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzelius, J. P., Van Pelt, J. A., Mueller, M. J., Buchala, A. J., Metraux, J.-P., Brown, R., Kazan, K., Van Loon, L. C., Dong, X., and Pieterse, C. M. J. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760-770.
94. Spoel, S. H., Mou, Z., Tada, Y., Spivey, N. W., Genschik, P., and Dong, X. 2009. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860-872.
95. Takahashi, M., and Asada, K. 1988. Superoxide production in aprotic interior of chloroplast thylakoids. Arch. Biochem. Biophys. 267:714-722.
96. Tameling, W. I. L., and Baulcombe, D. C. 2007. Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19:1682-1694.
97. Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H.-S., Han, B., Zhu, T., Zou, G., and Katagiri, F. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317-330.
98. Torres, M. A., and Dangl, J. L. 2005. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8:397.
99. 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. U.S.A. 99:517-522.
100. 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.
101. Vembar, S. S., and Brodsky, J. L. 2008. One step at a time: Endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9:944-957.
102. Vitale, A., and Boston, R. S. 2008. Endoplasmic reticulum quality control and the unfolded protein response: Insights from plants. Traffic 9:1581-1588.
103. Vlot, A. C., Dempsey, D. M. A., and Klessig, D. F. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177-206.
104. Wagner, D., Przybyla, D., op den Camp, R., Kim, C., Landgraf, F., Lee, K. P., Wursch, M., Laloi, C., Nater, M., Hideg, E., and Apel, K. 2004. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183-1185.
105. 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.
106. Wang, D., Amornsiripanitch, N., and Dong, X. 2006. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2:e123. Published online.
107. Wang, Y., Bao, Z., Zhu, Y., and Hua, J. 2009. Analysis of temperature modulation of plant defense against biotrophic microbes. Mol. Plant- Microbe Interact. 22:498-506.
108. Wasternack, C. 2007. Jasmonates: An update on biosynthesis, signal trans- duction and action in plant stress response, growth and development. Ann. Bot. 100:681-697.
109. Weber, H. 2002. Fatty acid-derived signals in plants. Trends Plant Sci. 7:217-224.
110. Whitham, S., McCormick, S., and Baker, B. 1996. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc. Natl. Acad. Sci. U.S.A. 93:8776-8781.
111. Wiermer, M., Feys, B. J., and Parker, J. E. 2005. Plant immunity: The EDS1 regulatory node. Curr. Opin. Plant Biol. 8:383.
112. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M. 2001. Iso- chorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565.
113. Williams, D. B. 2006. Beyond lectins: The calnexin/calreticulin chaperone system of the endoplasmic reticulum. J. Cell Sci. 119:615-623.
114. Wirthmueller, L., Zhang, Y., Jones, J. D. G., and Parker, J. E. 2007. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17:2023-2029.
115. Woodson, J. D., and Chory, J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9:383-395.
116. Yaeno, T., Matsuda, O., and Iba, K. 2004. Role of chloroplast trienoic fatty acids in plant disease defense responses. Plant J. 40:931-941.
117. Yang, S., and Hua, J. 2004. A haplotype-specific resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabi- dopsis. Plant Cell 16:1060-1071.
118. Yang, Y., Liu, B., Dai, J., Srivastava, P. K., Zammit, D. J., Lefraņois, L., and Li, Z. 2007. Heat shock protein gp96 is a master chaperone for Toll-like receptors and is important in the innate function of macro- phages. Immunity 26:215-226.
119. Yao, N., and Greenberg, J. T. 2006. Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18:397-411.
120. Zhang, X., Chen, S., and Mou, Z. 2010. Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. J. Plant Physiol. 167:144-148.
121. Zhang, Y., and Li, X. 2005. A putative nucleoporin 96 is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1. Plant Cell 17:1306-1316.
122. Zhang, Y., Fan, W., Kinkema, M., Li, X., and 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. Proc. Natl. Acad. Sci. U.S.A. 96:6523-6528.
123. Zhang, Y., Goritschnig, S., Dong, X., and 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.
124. Zhou, F., Kurth, J., Wei, F., Elliott, C., Vale, G., Yahiaoui, N., Keller, B., Somerville, S., Wise, R., and Schulze-Lefert, P. 2001. Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell 13:337-350.
125. Zhu, X., Caplan, J., Mamillapalli, P., Czymmek, K., and Dinesh-Kumar, S. P. 2010. Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. EMBO (Eur. Mol. Biol. Organ.) J. 29:1007-1018.
126. Zhu, Y., Qian, W., and Hua, J. 2010. Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 6:e1000844. Published online.
127. Zipfel, C. 2008. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20:10-16.
128. Zipfel, C. 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414-420.
129. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D. G., Boller, T., and Felix, G. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749-760.
130. Zurbriggen, M. D., Carrillo, N., Tognetti, V. B., Melzer, M., Peisker, M., Hause, B., and Hajirezaei, M. R. 2009. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non- host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J. 60:962-973.