Reprogramming of plants during systemic acquired resistance

Frontiers in Plant Science

Volumn 4, Issue JUL, 2013, Pages

  Gruner, Katrin ^a   Griebel, Thomas ^b   Návarová, Hana ^a   Attaran, Elham ^c   Zeier, Jürgen ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Defense priming; Gene classification; Gene regulation; Salicylic acid; Systemic acquired resistance; Transcriptional profiling

Indexed keywords

EID: 84886617484     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00252     Document Type: Article

References (146)

1. Adio, A. M., Casteel, C. L., De Vos, M., Kim, J. H., Joshi, V., Li, B., et al. (2011). Biosynthesis and defensive function of Nδ-acetylornithine, a jasmonate-induced Arabidopsis metabolite. Plant Cell 23, 3303-3318. doi: 10.1105/tpc.111.088989
2. Alexander, D., Goodman, R. M., Gut-Rella, M., Glascock, C., Weymann, K., Friedrich, L., et al. (1993). Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc. Natl. Acad. Sci. U.S.A. 90, 7327-7331. doi: 10.1073/pnas.90.15.7327
3. Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J. R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148-2152. doi: 10.1126/science.284.5423.2148
4. Alvarez, M. E., Pennell, R. I., Meijer, P.-J., Ishikawa, A., Dixon, R. A., and Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773-784. doi: 10.1016/S0092-8674(00)81405-1
5. Arimura, G. I., Garms, S., Maffei, M., Bossi, S., Schulze, B., Leitner, M., et al. (2008). Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta 227, 453-464. doi: 10.1007/s00425-007-0631-y
6. Attaran, E., Rostás, M., and Zeier, J. (2008). Pseudomonas syringae elicits emission of the terpenoid (E, E)-4, 8, 12-trimethyl-1, 3, 7, 11-tridecatetraene in Arabidopsis leaves via jasmonate signaling and expression of the terpene synthase TPS4. Mol. Plant-Microbe Interact. 21, 1482-1497. doi: 10.1094/MPMI-21-11-1482
7. Attaran, E., Zeier, T. E., Griebel, T., and Zeier, J. (2009). Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21, 954-971. doi: 10.1105/tpc.108.063164
8. Bartsch, M., Gobbato, E., Bednarek, P., Debey, S., Schultze, J. L., Bautor, J., et al. (2006). Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monoxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18, 1038-1051. doi: 10.1105/tpc.105.039982
9. Bell, E., and Mullet, J. E. (1993). Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol. 103, 1133-1337. doi: 10.1104/pp.103.4.1133
10. Benedetti, C. E., Costa, C. L., Turcinelli, S. R., and Arruda, P. (1998). Differential expression of a novel gene in response to coronatine, methyl jasmonate, and wounding in the Coi1 mutant of Arabidopsis. Plant Physiol. 116, 1037-1042. doi: 10.1104/pp.116.3.1037
11. Bhat, R. A., Miklis, M., Schmelzer, E., Schulze-Lefert, P., and Panstruga, R. (2005). Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl. Acad. Sci. U.S.A. 102, 3135-3140. doi: 10.1073/pnas.0500012102
12. Borevitz, J. O., Xia, Y., Blount, J., Dixon, R. A., and Lamb, C. (2000). Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12, 2383-2394.
13. Canet, J. V., Dobón, A., Roig, A., and Tornero, P. (2010). Structure-function analysis of npr1 alleles in Arabidopsis reveals a role for its paralogs in the perception of salicylic acid. Plant Cell Environ. 33, 1911-1922. doi: 10.1111/j.1365-3040.2010.02194.x
14. Celenza, J. L., Quiel, J. A., Smolen, G. A., Merrikh, H., Silvestro, A. R., Normanly, J., et al. (2005). The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol. 137, 253-262. doi: 10.1104/pp.104.054395
15. Chanda, B., Xia, Y., Mandal, M. K., Yu, K., Sekine, K.-T., Gao, Q.-M., et al. (2011). Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43, 421-427.
16. Chaturvedi, R., Venables, B., Petros, R. A., Nalam, V., Li, M., Wang, X., et al. (2012). An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 71, 161-172. doi: 10.1111/j.1365-313X.2012.04981.x
17. Chen, F., D'Auria, J. C., Tholl, D., Ross, J. R., Gershenzon, J., Noel, J. P., et al. (2003). An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 36, 577-588. doi: 10.1046/j.1365-313X.2003.01902.x
18. Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J. L., et al. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973-977. doi: 10.1038/nature02076
19. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., and Scheible, W. R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17. doi: 10.1104/pp.105.063743
20. Davletova, S., Schlauch, K., Coutu, J., and Mittler, R. (2005). The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139, 847-856. doi: 10.1104/pp.105.068254
21. Delaney, T. P., Friedrich, L., and Ryals, J. A. (1995). Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. U.S.A. 92, 6602-6606. doi: 10.1073/pnas.92.14.6602
22. Dempsey, D. A., and Klessig, D. F. (2012). SOS-too many signals for systemic acquired resistance? Trends Plant Sci. 17, 538-545. doi: 10.1016/j.tplants.2012.05.011
23. de Torres-Zabala, M., Truman, W., Bennett, M. H., Lafforgue, G., Mansfield, J. W., Rodriguez Egea, P., et al. (2007). Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 26, 1434-1443. doi: 10.1038/sj.emboj.7601575
24. Durrant, W. E., and Dong, X. (2004). Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209. doi: 10.1146/annurev.phyto.42.040803.140421
25. Fan, J., Hill, L., Crooks, C., Doerner, P., and Lamb, C. (2009). Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol. 150, 1750-1761. doi: 10.1104/pp.109.137943
26. Feys, B. J., Wiermer, M., Bhat, R. A., Moisan, L. J., Medina-Escobar, N., Neu, C., et al. (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17, 2601-2613. doi: 10.1105/tpc.105.033910
27. Fraser, C. M., and Chapple, C. (2011). The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book 9:e0152. doi: 10.1199/tab.0152
28. 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
29. Fu, Z. Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., et al. (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228-232.
30. Garcion, C., Baltensperger, R., Fournier, T., Pasquier, J., Schnetzer, M. A., Gabriel, J. P., et al. (2006). FiRe and microarrays: a fast answer to burning questions. Trends Plant Sci. 11, 320-322. doi: 10.1016/j.tplants.2006.05.009
31. Geng, X., Cheng, J., Gangadharan, A., and Mackey, D. (2012). The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense. Plant Cell 24, 4763-4774. doi: 10.1105/tpc.112.105312
32. Glawischnig, E. (2007). Camalexin. Phytochemistry 68, 401-406. doi: 10.1016/j.phytochem.2006.12.005
33. Glawischnig, E., Hansen, B. G., Olsen, C. E., and Halkier, B. A. (2004). Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 8245-8250. doi: 10.1073/pnas.0305876101
34. Goda, H., Sasaki, E., Akiyama, K., Maruyama-Nakashita, A., Nakabayashi, K., Li, W., et al. (2008). The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 55, 526-542. doi: 10.1111/j.1365-313X.2008.03510.x
35. 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
36. Griebel, T., and Zeier, J. (2010). A role for β-sitosterol to stigmasterol conversion in plant-pathogen interactions. Plant J. 63, 254-268. doi: 10.1111/j.1365-313X.2010.04235.x
37. Hamberg, M., Sanz, A., and Castresana, C. (1999). α-Oxidation of fatty acids in higher plants. Identification of a pathogen-inducible oxygenase (piox) as an α-dioxygenase and biosynthesis of 2-hydroperoxylinolenic acid. J. Biol. Chem. 274, 24503-24513. doi: 10.1074/jbc.274.35.24503
38. Heitz, T., Widemann, E., Lugan, R., Miesch, L., Ullmann, P., Désaubry, L., et al. (2012). Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone Jasmonoyl-isoleucine for catabolic turnover. J. Biol. Chem. 287, 6296-6306. doi: 10.1074/jbc.M111.316364
39. Herde, M., Gartner, K., Kollner, T. G., Fode, B., Boland, W., Gershenzon, J., et al. (2008). Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C-16-homoterpene TMTT. Plant Cell 20, 1152-1168. doi: 10.1105/tpc.106.049478
40. Hu, Y., Dong, Q., and Yu, D. (2012). Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci. 185-186, 288-297. doi: 10.1016/j.plantsci.2011.12.003
41. Humphry, M., Bednarek, P., Kemmerling, B., Koh, S., Stein, M., Göbel, U., et al. (2010). A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity. Proc. Natl. Acad. Sci. U.S.A. 107, 21896-21901. doi: 10.1073/pnas.1003619107
42. Hwang, S. G., Lin, N. C., Hsiao, Y. Y., Kuo, C. H., Chang, P. F., Deng, W. L., et al. (2012). The Arabidopsis short-chain dehydrogenase/reductase 3, an ABSCISIC ACID DEFICIENT 2 homolog, is involved in plant defense responses but not in ABA biosynthesis. Plant Physiol. Biochem. 51, 63-73. doi: 10.1016/j.plaphy.2011.10.013
43. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B., and Speed, T. P. (2003a). Summaries of affymetrix genechip probe level data. Nucleic Acids Res. 31:e15. doi: 10.1093/nar/gng015
44. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., et al. (2003b). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264. doi: 10.1093/biostatistics/4.2.249
45. Irshad, M., Canut, H., Borderies, G., Pont-Lezica, R., and Jamet, E. (2008). A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: Confirmed actors and newcomers. BMC Plant Biol. 8:94. doi: 10.1186/1471-2229-8-94
46. Ishikawa, K., Yoshimura, K., Harada, K., Fukusaki, E., Ogawa, T., Tamoi, M., et al. (2010). AtNUDX6, an ADP-ribose/NADH pyrophosphohydrolase in Arabidopsis, positively regulates NPR1-dependent salicylic acid signaling. Plant Physiol. 152, 2000-2012. doi: 10.1104/pp.110.153569
47. Jagadeeswaran, G., Raina, S., Acharya, B. R., Maqbool, S. B., Mosher, S. L., Appel, H. M., et al. (2007). Arabidopsis GH3-like defense gene 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. Plant J. 51, 234-246. doi: 10.1111/j.1365-313X.2007.03130.x
48. Jing, B., Xu, S., Xu, M., Li, Y., Li, S., Ding, J., et al. (2011). Brush and spray: a high-throughput systemic acquired resistance assay suitable for large-scale genetic screening. Plant Physiol. 157, 973-980. doi: 10.1104/pp.111.182089
49. Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., et al. (1999). Arabidopsis thaliana PAD4encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 96, 13583-13588. doi: 10.1073/pnas.96.23.13583
50. Johnson, K. L., Jones, B. J., Bacic, A., and Schultz, C. J. (2003). The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol. 133, 1911-1925. doi: 10.1104/pp.103.031237
51. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
52. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J., and Greenberg, J. T. (2009). Priming in systemic plant immunity. Science 324, 89-91. doi: 10.1126/science.1170025
53. Kadota, Y., and Shirasu, K. (2012). The HSP90 complex of plants. Biochim. Biophys. Acta 1823, 689-697. doi: 10.1016/j.bbamcr.2011.09.016
54. Kang, J., Hwang, J. U., Lee, M., Kim, Y. Y., Assmann, S. M., Martinoia, E., et al. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. U.S.A. 107, 2355-2360. doi: 10.1073/pnas.0909222107
55. Katagiri, F., Thilmony, R., and He, S. Y. (2002). The Arabidopsis thaliana-Pseudomonas syringae interaction. Arabidopsis Book 1:e0039. doi: 10.1199/tab.0039
56. Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y., and Howe, G. A. (2008). COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl. Acad. Sci. U.S.A. 105, 7100-7105. doi: 10.1073/pnas.0802332105
57. Kim, K.-C., Lai, Z., Fan, B., and Chen, Z. (2008). Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20, 2357-2371. doi: 10.1105/tpc.107.055566
58. Koo, A. J. K., Thomas, F., Cooke, T. F., and Howe, G. A. (2011). Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc. Natl. Acad. Sci. U.S.A. 108, 9298-9303. doi: 10.1073/pnas.1103542108
59. La Camera, S., L'Haridon, F., Astier, J., Zander, M., Abou-Mansour, E., Page, G., et al. (2011). The glutaredoxin ATGRXS13 is required to facilitate Botrytis cinerea infection of Arabidopsis thaliana plants. Plant J. 68, 507-519. doi: 10.1111/j.1365-313X.2011.04706.x
60. Laporte, D., Olate, E., Salinas, P., Salazar, M., Jordana, X., and Holuigue, L. (2012). Glutaredoxin GRXS13 plays a key role in protection against photooxidative stress in Arabidopsis. J. Exp. Bot. 68, 507-519.
61. Laudert, D., and Weiler, E. W. (1998). Allene oxide synthase: a major control point in Arabidopsis thalianaoctadecanoid signalling. Plant J. 15, 675-684. doi: 10.1046/j.1365-313x.1998.00245.x
62. Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., et al. (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10, 71-82. doi: 10.1046/j.1365-313X.1996.10010071.x
63. Lee, M. W., Lu, H., Jung, H. W., and Greenberg, J. T. (2007). A key role for the Arabidopsis WIN3 protein in disease resistance triggered by Pseudomonas syringae that secrete AvrRpt2. Mol. Plant-Microbe Interact. 20, 1192-1200. doi: 10.1094/MPMI-20-10-1192
64. Lee, S., Badieyan, S., Bevan, D. R., Herde, M., Gatz, C., and Tholl, D. (2010). Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 107, 21205-21210. doi: 10.1073/pnas.1009975107
65. 2+/calmodulin in Arabidopsis thaliana. Mol. Gen. Genet. 258, 412-419. doi: 10.1007/s004380050749
66. Lewis, J. D., Wan, J., Ford, R., Gong, Y., Fung, P., Nahal, H., et al. (2012). Quantitative Interactor Screening with next-generation Sequencing (QIS-Seq) identifies Arabidopsis thaliana MLO2 as a target of the Pseudomonas syringae type III effector HopZ2. BMC Genomics 13:8. doi: 10.1186/1471-2164-13-8
67. Li, J., Brader, G., Kariola, T., and Palva, E. T. (2006). WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 46, 477-491. doi: 10.1111/j.1365-313X.2006.02712.x
68. 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
69. Li, J., Hansen, B. G., Ober, J. A., Kliebenstein, D. J., and Halkier, B. A. (2008). Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol. 148, 1721-1733. doi: 10.1104/pp.108.125757
70. Li, Y., Darley, C. P., Ongaro, V., Fleming, A., Schipper, O., Baldauf, S. L., et al. (2002). Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol. 128, 854-864. doi: 10.1104/pp.010658
71. Linthorst, H. J., Meuwissen, R. L., Kauffmann, S., and Bol, J. F. (1989). Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus infection. Plant Cell 1, 285-291.
72. Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., et al. (2005). Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310, 1180-1183. doi: 10.1126/science.1119409
73. Liu, D., Raghothama, K. G., Hasegawa, P. M., and Bressan, R. A. (1994). Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad. Sci. U.S.A. 91, 1888-1892. doi: 10.1073/pnas.91.5.1888
74. Liu, P. P., von Dahl, C. C., and Klessig, D. F. (2011). The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol. 157, 2216-2226.
75. T method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
76. Maldonado, A. M., Doerner, P., Dixon, R. A., Lamb, C. J., and Cameron, R. K. (2002). A putative lipid transfer protein involved in systemic acquired resistance signalling in Arabidopsis. Nature 419, 399-403. doi: 10.1038/nature00962
77. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., et al. (2000). The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26, 403-410. doi: 10.1038/82521
78. 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. doi: 10.1105/tpc.111.084996
79. Mauch, F., Mauch-Mani, B., and Boller, T. (1988). Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and β-1, 3-glucanase. Plant Physiol. 88, 936-942. doi: 10.1104/pp.88.3.936
80. Métraux, J.-P. (2002). Recent breakthroughs in the study of salicylic acid biosynthesis. Trends Plant Sci. 7, 332-334. doi: 10.1016/S1360-1385(02)02313-0
81. Métraux, J.-P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., et al. (1990). Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004-1006. doi: 10.1126/science.250.4983.1004
82. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev, V., et al. (2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45. doi: 10.1126/scisignal.2000448
83. Mishina, T. E., Griebel, T., Geuecke, M., Attaran, E., and Zeier, J. (2008). "New insights into the molecular events underlying systemic acquired resistance, " in Biology of Plant-Microbe Interactions Vol. 6, eds. M. Lorito, S. L. Woo, and F. Scala (St. Paul, MN: International Society for Molecular Plant-Microbe Interactions), 81.
84. Mishina, T. E., and Zeier, J. (2006). The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141, 1666-1675. doi: 10.1104/pp.106.081257
85. Mishina, T. E., and Zeier, J. (2007). Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, 500-513. doi: 10.1111/j.1365-313X.2007.03067.x
86. Misyura, M., Colasanti, J., and Rothstein, S. J. (2013). Physiological and genetic analysis of Arabidopsis thalianaanthocyanin biosynthesis mutants under chronic adverse environmental conditions. J. Exp. Bot. 64, 229-240. doi: 10.1093/jxb/ers328
87. Morikawa, T., Mizutani, M., Aoki, N., Watanabe, B., Saga, H., Saito, S., et al. (2006). Cytochrome P450 CYP710Aencodes the sterol C-22 desaturase in Arabidopsis and tomato. Plant Cell 18, 1008-1022. doi: 10.1105/tpc.105.036012
88. Nakao, M., Nakamura, R., Kita, K., Inukai, R., and Ishikawa, A. (2011). Non-host resistance to penetration and hyphal growth of Magnaporthe oryzae in Arabidopsis. Sci. Rep. 1, 171. doi: 10.1038/srep00171
89. Návarová, H., Bernsdorff, F., Döring, A.-C., and Zeier, J. (2012). Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24, 5123-5141. doi: 10.1105/tpc.112.103564
90. Nawrath, C., and Métraux, J.-P. (1999). Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11, 1393-1404. doi: 10.1111/j.1365-313X.2007.03039.x
91. Ndamukong, I., Abdallat, A. A., Thurow, C., Fode, B., Zander, M., Weigel, R., et al. (2007). SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50, 128-139.
92. Neal, C. S., Fredericks, D. P., Griffiths, C. A., and Neale, A. D. (2010). The characterisation of AOP2: a gene associated with the biosynthesis of aliphatic alkenyl glucosinolates in Arabidopsis thaliana. BMC Plant Biol. 10:170. doi: 10.1186/1471-2229-10-170
93. Nickstadt, A., Thomma, B. P. H. J., Feussner, I., Kangasjärvi, J., Zeier, J., Loeffler, C., et al. (2004). The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol. Plant Pathol. 5, 425-434. doi: 10.1111/j.1364-3703.2004.00242.x
94. Niderman, T., Genetet, I., Bruyère, T., Gees, R., Stintzi, A., Legrand, M., et al. (1995). Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol. 108, 17-27. doi: 10.1104/pp.108.1.17
95. Nobuta, K., Okrent, R. A., Stoutemyer, M., Rodibaugh, N., Kempema, L., Wildermuth, M. C., et al. (2007). The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol. 144, 1144-1156. doi: 10.1104/pp.107.097691
96. Noël, L. D., Cagna, G., Stuttmann, J., Wirthmüller, L., Betsuyaku, S., Witte, C. P., et al. (2007). Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19, 4061-4076. doi: 10.1105/tpc.107.051896
97. Noutoshi, Y., Okazaki, M., Kida, T., Nishina, Y., Morishita, Y., Ogawa, T., et al. (2012). Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic acid glucosyltransferases in Arabidopsis. Plant Cell 24, 3795-3804. doi: 10.1105/tpc.112.098343
98. Okrent, R. A., Brooks, M. D., and Wildermuth, M. C. (2009). Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J. Biol. Chem. 284, 9742-9754. doi: 10.1074/jbc.M806662200
99. 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
100. Rayapuram, C., Wu, J., Haas, C., and Baldwin, I. T. (2008). PR-13/Thionin but not PR-1 mediates bacterial resistance in Nicotiana attenuata in nature, and neither influences herbivore resistance. Mol. Plant-Microbe Interact. 21, 988-1000. doi: 10.1094/MPMI-21-7-0988
101. Redman, J. C., Haas, B. J., Tanimoto, G., and Town, C. D. (2004). Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. Plant J. 38, 545-561. doi: 10.1111/j.1365-313X.2004.02061.x
102. Ren, D., Liu, Y., Yang, K.-Y., Han, L., Mao, G., Glazebrook, J., et al. (2008). A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 105, 5638-5643. doi: 10.1073/pnas.0711301105
103. Rietz, S., Stamm, A., Malonek, S., Wagner, S., Becker, D., Medina-Escobar, N., et al. (2011). Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity. New Phytol. 191, 107-119. doi: 10.1111/j.1469-8137.2011.03675.x
104. Rose, J. K., Braam, J., Fry, S. C., and Nishitani, K. (2002). The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: Current perspectives and a new unifying nomenclature. Plant Cell Physiol. 43, 1421-1435. doi: 10.1093/pcp/pcf171
105. Saito, K., Yonekura-Sakakibara, K., Nakabayashi, R., Higashi, Y., Yamazaki, M., Tohge, T., et al. (2013). The flavonoid biosynthetic pathway in Arabidopsis: Structural and genetic diversity. Plant Physiol. Biochem. doi: 10.1016/j.plaphy.2013.02.001. [Epub ahead of print].
106. Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K., Häweker, H., et al. (2009). Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28, 3439-3449. doi: 10.1038/emboj.2009.263
107. Schenk, P. M., Kazan, K., Manners, J. M., Anderson, J. P., Simpson, R. S., Wilson, I. W., et al. (2003). Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol. 132, 999-1010. doi: 10.1104/pp.103.021683
108. Schultz, C. J., Rumsewicz, M. P., Johnson, K. L., Jones, B. J., Gaspar, Y. M., and Bacic, A. (2002). Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case. Plant Physiol. 129, 1448-1463. doi: 10.1104/pp.003459
109. Shah, J., and Zeier, J. (2013). Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 4:30. doi: 10.3389/fpls.2013.00030
110. Shang, Y., Yan, L., Liu, Z. Q., Cao, Z., Mei, C., Xin, Q., et al. (2010). The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22, 1909-1935. doi: 10.1105/tpc.110.073874
111. Shulaev, V., Leon, J., and Raskin, I. (1995). Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7, 1691-1701.
112. Sønderby, I. E., Geu-Flores, F., and Halkier, B. A. (2010) Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci. 15, 283-290. doi: 10.1016/j.tplants.2010.02.005
113. Song, J., Lu, H., McDowell, J. M., and Greenberg, J. (2004a). A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 40, 200-212. doi: 10.1111/j.1365-313X.2004.02200.x
114. Song, J., Lu, H., and Greenberg, J. (2004b). 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. Plant Cell 16, 353-366. doi: 10.1105/tpc.019372
115. Spoel, S. H., and Dong, X. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12, 89-100. doi: 10.1038/nri3141
116. Spoel, S. H., Koornneef, A., Claessens, S. M., Korzelius, J. P., Van Pelt, J. A., Mueller, M. J., et al. (2003). NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15, 760-770. doi: 10.1105/tpc.009159
117. Stehle, F., Brandt, W., Stubbs, M. T., Milkowski, C., and Strack, D. (2009). Sinapoyltransferases in the light of molecular evolution. Phytochemistry 70, 1652-1662. doi: 10.1016/j.phytochem.2009.07.023
118. Sticher, L., Mauch-Mani, B., and Métraux, J. P. (1997). Systemic acquired resistance. Annu. Rev. Phytopathol. 35, 235-270.
119. Tanaka, H., Osakabe, Y., Katsura, S., Mizuno, S., Maruyama, K., Kusakabe, K., et al. (2012). Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J. 70, 599-613. doi: 10.1111/j.1365-313X.2012.04901.x
120. Thibaud-Nissen, F., Wu, H., Richmond, T., Redman, J. C., Johnson, C., Green, R., et al. (2006). Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. Plant J. 47, 152-162. doi: 10.1111/j.1365-313X.2006.02770.x
121. Thilmony, R., Underwood, W., and He, S. Y. (2006). Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J. 46, 34-53. doi: 10.1111/j.1365-313X.2006.02725.x
122. COI1 complex during jasmonate signalling. Nature 448, 661-665. doi: 10.1038/nature05960
123. Thordal-Christensen, H. (2003). Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6, 351-357. doi: 10.1016/S1369-5266(03)00063-3
124. Tognetti, V. B., Van Aken, O., Morreel, K., Vandenbroucke, K., van de Cotte, B., De Clercq, I., et al. (2010). Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22, 2660-2679. doi: 10.1105/tpc.109.071316
125. Tran, L. S., Nakashima, K., Sakuma, Y., Simpson, S. D., Fujita, Y., Maruyama, K., et al. (2004). Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16, 2481-2498. doi: 10.1105/tpc.104.022699
126. Truman, W., Bennett, M. H., Kubigsteltig, I., Turnbull, C., and Grant, M. (2007). Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. U.S.A. 104, 1075-1080. doi: 10.1073/pnas.0605423104
127. Truman, W., de Torres-Zabala, M., and Grant, M. (2006). Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J. 46, 14-33. doi: 10.1111/j.1365-313X.2006.02672.x
128. Truman, W. M., Bennett, M. H., Turnbull, C. G., and Grant, M. R. (2010). Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol. 152, 1562-1573. doi: 10.1104/pp.109.152173
129. Tsuchisaka, A., Yu, G., Jin, H., Alonso, J. M., Ecker, J. R., Zhang, X., et al. (2009). A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183, 979-1003. doi: 10.1534/genetics.109.107102
130. Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J., and Katagiri, F. (2009). Network properties of robust immunity in plants. PLoS Genet. 5:e1000772. doi: 10.1371/journal.pgen.1000772
131. von Saint Paul, V., Zhang, W., Kanawati, B., Geist, B., Faus-Keßler, T., Schmitt-Kopplin, P., et al. (2011). The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23, 4124-4145. doi: 10.1105/tpc.111.088443
132. Ward, J. L., Forcat, S., Beckmann, M., Bennett, M., Miller, S. J., Baker, J. M., et al. (2010). The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J. 63, 443-457. doi: 10.1111/j.1365-313X.2010.04254.x
133. 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. doi: 10.1371/journal.ppat.0020123
134. Wang, L., Mitra, R. M., Hasselmann, K. D., Sato, M., Lenarz-Wyatt, L., Cohen, J. D., et al. (2008). The genetic network controlling the Arabidopsis transcriptional response to Pseudomonas syringae pv. maculicola: roles of major regulators and the phytotoxin coronatine. Mol. Plant-Microbe Interact. 21, 1408-1420. doi: 10.1094/MPMI-21-11-1408
135. Wang, L., Tsuda, K., Truman, W., Sato, M., Nguyen, L. V., Katagiri, F., et al. (2011). CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J. 67, 1029-1041. doi: 10.1111/j.1365-313X.2011.04655.x
136. 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
137. Wiermer, M., Feys, B. J., and Parker, J. E. (2005), Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8, 383-389. doi: 10.1016/j.pbi.2005.05.010
138. 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
139. Wu, Y., Zhang, D., Chu, J. Y., Boyle, P., Wang, Y., Brindle, I. D., et al. (2012). The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1, 639-647. doi: 10.1016/j.celrep.2012.05.008
140. Xu, X., Chen, C., Fan, B., and Chen, Z. (2006). Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18, 1310-1326. doi: 10.1105/tpc.105.037523
141. Yamamoto, A., Bhuiyan, M. N., Waditee, R., Tanaka, Y., Esaka, M., Oba, K., et al. (2005). Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. J. Exp. Bot. 56, 1785-1796. doi: 10.1093/jxb/eri167
142. Zander, M., Chen, S., Imkampe, J., Thurow, C., and Gatz, C. (2012). Repression of the Arabidopsis thalianajasmonic acid/ethylene-induced defense pathway by TGA-interacting glutaredoxins depends on their C-terminal ALWL motif. Mol. Plant 5, 831-840. doi: 10.1093/mp/ssr113
143. Zander, M., La Camera, S., Lamotte, O., Métraux, J.-P., and Gatz, C. (2010). Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses. Plant J. 61, 200-210. doi: 10.1111/j.1365-313X.2009.04044.xc
144. 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
145. Zhou, N., Tootle, T. L., Tsui, F., Klessig, D. F., and Glazebrook, J. (1998). PAD4 functions upstream from salicylic acid to control defence responses in Arabidopsis. Plant Cell 10, 1021-1030.
146. Zoeller, M., Stingl, N., Krischke, M., Fekete, A., Waller, F., Berger, S., et al. (2012). Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol. 160, 365-378. doi: 10.1104/pp.112.202846