Crosstalk between intracellular and extracellular salicylic acid signaling events leading to long-distance spread of signals

Plant Cell Reports

Volumn 32, Issue 7, 2013, Pages 1125-1138

  Kawano, Tomonori ^a,b,c   Bouteau, François ^b,c,d  

^a UNIVERSITY OF KITAKYUSHU   (Japan)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Calcium; Long distance signaling; Phloem mobile signal; Reactive oxygen species; Salicylic acid; Signal transduction

Indexed keywords

EID: 84878986815     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1451-0     Document Type: Review

References (127)

1. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773-784.
2. Antoniw JF, White RF (1980) The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopathol Z 98: 331-341.
3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
4. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63: 3523-3544.
5. Baker A, Graham IA, Holdsworth M, Smith SM, Theodouloue FL (2006) Chewing the fat: β-oxidation in signalling and development. Trends Plant Sci 11: 124-132.
6. Barbehenn R, Dukatz C, Holt C, Reese A, Martiskainen O, Salminen JP, Yip L, Tran L, Constabel CP (2010) Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. Oecologia 164: 993-1004.
7. Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43: 421-427.
8. Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Roth MR, Welti R, Shah J (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.
9. Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, Wang X, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71: 161-172.
10. 2+-dependent excretion of salicylic acid in tobacco cell suspension culture. Bot Bull Acad Sin 40: 267-273.
11. Chen Z, Ricigliano JR, Klessig DF (1993a) Purification and characterization of soluble salicylic acid binding protein from tobacco. Proc Natl Acad Sci USA 90: 9533-9537.
12. Chen Z, Silva H, Klessig DF (1993b) Active oxygen species in the induction of plant systemic acquired resistance induced by salicylic acid. Science 262: 1883-1886.
13. 2+-independent excretion modes of salicylic acid in tobacco cell suspension culture. J Exp Bot 52: 1219-1226.
14. Clarke A, Mur LAJ, Darby RM, Kenton P (2005) Harpin modulates the accumulation of salicylic acid by Arabidopsis cells via apoplastic alkalization. J Exp Bot 56: 3129-3136.
15. Cline E (2006) Phytophthora infestans. Systemic Mycology and Microbiology Laboratory, ARS, USDA. http://sbmlweb/OnlineResources/FungiOnline. cfm. Retrieved 20 Nov 2012.
16. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247-1256.
17. Conrath U, Chen Z, Ricigliano JR, Klessig DF (1995) Two inducers of plant defense response, 2, 6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activities in tobacco. Proc Natl Acad Sci USA 92: 7143-7147.
18. Dadacz-Narloch B, Beyhl D, Larisch C, López-Sanjurjo EJ, Reski R, Kuchitsu K, Müller TD, Becker D, Schönknecht G, Hedrich R (2011) A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. Plant Cell 23: 2696-2707.
19. Del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53: 1255-1272.
20. Delaney TP (2004) Salicylic acid. In: Davies PJ (ed) Plant hormones. Biosynthesis, signal transduction, action! Kluwer Academic Publishers, Dordrecht, pp 635-653.
21. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9: e0156.
22. Doke N (1983a) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23: 345-357.
23. Doke N (1983b) Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiol Plant Pathol 23: 359-367.
24. Drzewiecka K, Borowiak K, Bandurska H, Golinski P (2012) Salicylic acid-a potential biomarker of tobacco Bel-W3 cell death developed as a response to ground level ozone under ambient conditions. Acta Biol Hung 63: 231-249.
25. Du H, Klessig DF (1997) Identification of a soluble, high-affinity salicylic acid-binding protein in tobacco. Plant Physiol 113: 1319-1327.
26. Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2, 6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci USA 92: 11312-11316.
27. Durner J, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 272: 28492-28501.
28. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, Klessig DF, Tong L (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci USA 102: 1773-1778.
29. Fu ZQ, Yan Y, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong X (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486: 228-232.
30. 2+ flux in Arabidopsis leaf cells. Plant Cell Physiol 42: 900-905.
31. Furuichi T, Kawano T, Tatsumi H, Sokabe M (2007) Roles of ion channels in environmental responses of plants. In: Martinac B (ed) Sensing with ion channels. Springer series in biophysics, vol 11. Springer, Berlin, pp 47-62.
32. Gaupels F, Kuruthukulangarakoola GT, Durner J (2011) Upstream and downstream signals of nitric oxide in pathogen defence. Curr Opin Plant Biol 14: 707-714.
33. Gechev TS, van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28: 1091-1101.
34. Glauser G, Grata E, Dubugnon L, Rudaz S, Farmer EE, Wolfender JL (2008) Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. J Biol Chem 283: 16400-16407.
35. Goodwin SB, Cohen BA, Fry WE (1994) Panglobal distribution of a single clonal lineage of Irish potato famine fungus. Proc Natl Acad Sci USA 91: 11591-11595.
36. Gozzo F (2003) Systemic acquired resistance in crop protection: from nature to a chemical approach. J Agric Food Chem 51: 4487-4503.
37. 2+ influx and production of phytoalexins by a putative voltage-gated cation channel, OsTPC1, in cultured rice cells. J Biol Chem 287: 9931-9939.
38. 2+ channel, OsTPC1, in rice. Plant Biotechnol 22: 235-923.
39. Hause B, Hause G, Kutter C, Miersch O, Wasternack C (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44: 643-648.
40. Hedrich R, Marten I (2011) TPC1-SV channels gain shape. Mol Plant 4: 428-441.
41. Ishibashi K, Suzuki M, Imai M (2000) Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem Biophys Res Commun 270: 370-376.
42. Jammes F, Hu HC, Villiers F, Bouten R, Kwak JM (2011) Calcium-permeable channels in plant cells. FEBS J 278: 4262-4276.
43. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324: 89-91.
44. Kadono T, Tran D, Errakhi R, Hiramatsu T, Meimoun P, Briand J, Iwaya-Inoue M, Kawano T, Bouteau F (2010) Increased anion channel activity is an unavoidable event in ozone-induced programmed cell death. PLoS ONE 5: e13373.
45. 2+ transients and defense responses in tobacco BY-2 Cells. Biochem Biophys Res Commun 317: 823-830.
46. Karsch (1855) Die Kartoffelkrankheit. Natur und Offenbarung 1: 60-71.
47. Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21: 829-837.
48. Kawano T, Furuichi T (2007) Salicylic acid as a defense-related plant hormone: roles of oxidative and calcium signaling paths in salicylic acid biology. In: Hayat S, Ahmad A (eds) Salicylic acid-a plant hormone. Springer, Dordrecht, pp 277-321.
49. Kawano T, Muto S (2000) Mechanism of peroxidase actions for salicylic acid-induced generation of active oxygen species and an increase in cytosolic calcium in tobacco suspension culture. J Exp Bot 51: 685-693.
50. Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S (1998) Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transduction. Plant Cell Physiol 39: 721-730.
51. 2+ increase in tobacco suspension culture. Plant Peroxide Newsl 14: 117-124.
52. Kawano T, Muto S, Adachi M, Hosoya H, Lapeyrie F (2002) Spectroscopic evidence in support of horseradish peroxidase compound II-catalyzed oxidation of salicylic acid but not of phenylethylamine. Biosci Biotechnol Biochem 66: 651-654.
53. Kawano T, Kadono T, Furuichi T, Muto S, Lapeyrie F (2003) Aluminum-induced distortion in calcium signaling involving oxidative bursts and channel regulations in tobacco BY-2 cells. Biochem Biophys Res Commun 308: 35-42.
54. Kawano T, Furuichi T, Muto S (2004a) Controlled free salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotechnol 21: 319-335.
55. Kawano T, Tanaka S, Kadono T, Muto S (2004b) Salicylic acid glucoside acts as a slow inducer of oxidative burst in tobacco suspension culture. Z Naturforsch 59c: 684-692.
56. 2+ channels. Biochem Biophys Res Commun 324: 40-45.
57. Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756.
58. Khokon MAR, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environ 34: 434-443.
59. Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytosolic calcium. Nature 352: 524-526.
60. Koo AJK, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59: 974-986.
61. Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA 100: 16101-16106.
62. Kunihiro S, Hiramatsu T, Kawano T (2011) Involvement of salicylic acid signal transduction in aluminum-responsive oxidative burst in Arabidopsis thaliana cell suspension culture. Plant Signal Behav 6: 611-616.
63. 2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J 42: 798-809.
64. Kvaratskhelia M, George SJ, Thorneley RNF (1997) Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase. J Biol Chem 272: 20998-21001.
65. Lee JS (1998) The mechanism of stomatal closing by salicylic acid in Commelina communis L. J Plant Biol 41: 97-102.
66. Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Taylor ATS, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution or reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol 121: 147-152.
67. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12: 451-458.
68. Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99: 6416-6421.
69. Lin C, Yu Y, Kadono T, Iwata M, Umemura K, Furuichi T, Kuse M, Isobe M, Yamamoto Y, Mastumoto H, Yoshizuka K, Kawano T (2005) Action of aluminum, novel TPC1-type channel inhibitor, against salicylate-induced and cold shock-induced calcium influx in tobacco BY-2 cells. Biochem Biophys Res Commun 332: 823-830.
70. Liu N, You J, Shi W, Liu W, Yang Z (2012) Salicylic acid involved in the process of aluminum induced citrate exudation in Glycine max L. Plant Soil 352: 85-97.
71. Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002-1004.
72. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419: 399-403.
73. Manthe B, Schulz M, Schnable H (1992) Effects of salicylic acid on growth and stomatal movement on Vicia faba L.: evidence for salicylic acid metabolism. J Chem Ecol 18: 1525-1539.
74. McGurl B, Pearce G, Orozco-Cardenas M, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255: 1570-1573.
75. Métraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004-1006.
76. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2: ra45.
77. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16: 300-309.
78. Mitton FM, Pinedo ML, de la Canal L (2009) Phloem sap of tomato plants contains a DIR1 putative ortholog. J Plant Physiol 166: 543-547.
79. Miyake C, Sano S, Asada K (1996) A new assay of ascorbate peroxidase using the coupled system with monodehydroascorbate radical reductase. In: Obinger C, Burner U, Ebermann R, Penel C, Greppin H (eds) Plant peroxidases: biochemistry and physiology. University of Geneva, Vienna, pp 386-389.
80. Mölders W, Buchala A, Métraux JP (1996) Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiol 112: 787-792.
81. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591.
82. Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58: 459-481.
83. Moreau M, Tian M, Klessig DF (2012) Salicylic acid binds NPR3 and NPR4 to regulate NPR1-dependent defense responses. Cell Res 2012: 1-3. doi: 10. 1038/cr. 2012. 100.
84. Mori IC, Pinontoan R, Kawano T, Muto S (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol 42: 1383-1388.
85. Mou Z, Fan WH, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944.
86. Nandi A, Welti R, 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.
87. 14C-labeled organic acids across isolated plant cuticles. Plant Physiol 116: 117-123.
88. Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12: 125-134.
89. Nomura H, Komori T, Uemura S, Kanda Y, Shimotani K, Nakai K, Furuichi T, Takebayashi K, Sugimoto T, Sano S, Suwastika IN, Fukusaki E, Yoshioka H, Nakahira Y, Shiina T (2012) Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat Commun 3: Article number 926. doi: 10. 1038/ncomms1926.
90. Ohashi Y, Murakami T, Mitsuhara I, Seo S (2004) Rapid down and upward translocation of salicylic acid in tobacco plants. Plant Biotechnol 21: 95-101.
91. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318: 113-116.
92. Pastor V, Vicent C, Cerezo M, Mauch-Mani B, Dean J, Flors V (2012) Detection, characterization and quantification of salicylic acid conjugates in plant extracts by ESI tandem mass spectrometric techniques. Plant Physiol Biochem 53: 19-26.
93. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434: 404-408.
94. 2+ signals induced by abiotic and biotic stresses. Plant J 53: 287-299.
95. Rasmussen JB, Hammerschmidt R, Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol 97: 1342-1347.
96. Raz V, Fluhr R (1992) Calcium requirement for ethylene-dependent responses. Plant Cell 4: 1123-1130.
97. Rhodes JD, Thain JF, Wildon DC (1996) The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200: 50-57.
98. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49: 317-343.
99. Rocher F, Chollet JF, Jousse C, Bonnemain JL (2006) Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiol 141: 1684-1693.
100. Rocher F, Chollet JF, Legros S, Jousse C, Lemoine R, Faucher M, Bush DR, Bonnemain JL (2009) Salicylic acid transport in Ricinus communis involves a pH-dependent carrier system in addition to diffusion. Plant Physiol 150: 2081-2091.
101. Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143: 1282-1292.
102. 2+ in the induction of chitinase activity in carrot suspension culture. Physiol Mol Plant Pathol 45: 101-109.
103. Seo S, Ichizawa K, Ohashi Y (1995) Induction of salicylic acid-β-glucosidase in tobacco leaves by exogenous salicylic acid. Plant Cell Physiol 36: 447-453.
104. Shah J (2003) The salicylic acid loop in plant defense. Curr Opin Plant Biol 6: 365-371.
105. Shulaev V, Leon J, Raskin I (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7: 1691-1701.
106. Slaymaker DH, Navarre DA, Clark D, Del Pozo O, Martin GB, Klessig DF (2002) The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci USA 99: 11640-11645.
107. Song F, Goodman RM (2001) Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol Plant Microbe Interact 14: 1458-1462.
108. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770.
109. Suzuki N, Miller G, Morales J, Shulaev V, Torres A, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signalling. Curr Opin Plant Biol 14: 691-699.
110. Takayama A, Kadono T, Kawano T (2012) Heme redox cycling in soybean peroxidase: hypothetical model and supportive data. Sens Mater 24: 87-97.
111. Tenhaken R, Rübel C (1997) Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol 115: 291-298.
112. Thompson GA, van Bel AJE, Gaupels F, Vlot AC (2012) Plant defense and Long-distance signaling in the phloem, in: Phloem. Molecular Cell Biology, Systemic Communication, Biotic Interactions, Thompson GA, van Bel AJE, Eds., Wiley-Blackwell, Oxford, pp 227-248.
113. Tran D, Kadono T, Molas ML, Errakhi R, Briand J, Biligui B, Kawano T, Bouteau F (2013) A role for oxalic acid generation in ozone-induced signalization in Arabidopsis cells. Plant Cell Environ 36: 569-578.
114. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 104: 1075-1080.
115. Umemura K, Satoh J, Iwata M, Uiozumi N, Koga J, Kawano T, Koshiba T, Anzai H, Mitomi M (2009) Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J 57: 463-472.
116. Vlot AC, Klessig DF, Park SW (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11: 436-442.
117. Vlot AC, Dempsey DM, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47: 177-206.
118. 2+ channel gene TaTPC1 from wheat. J Exp Bot 56: 3051-3060.
119. White RF (1979) Acetylsalicylic acid induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410-412.
120. Wildon DC, Doherty HM, Eagles G, Bowles DJ, Thain JF (1989) Systemic responses arising from localized heat stimuli in tomato plants. Ann Bot 64: 691-695.
121. Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O'Donnell PJ, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360: 62-65.
122. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1: 639-647.
123. Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J 23: 980-988.
124. Yalpani N, Siverman P, Wilson TMA, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3: 809-818.
125. Yoshioka H, Sugie K, Park HJ, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp91phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol Plant Microbe Interact 14: 725-736.
126. Yoshioka H, Bouteau F, Kawano T (2008) Discovery of oxidative burst in the field of plant immunity: looking back at the early pioneering works and towards the future development. Plant Signal Behav 3: 153-155.
127. 2+ mobilization from acidic organelles triggered by NAADP. FEBS Lett 584: 1966-1974.