The impact of global change factors on redox signaling underpinning stress tolerance

Plant Physiology

Volumn 161, Issue 1, 2013, Pages 5-19

  Munné Bosch, Sergi ^a   Queval, Guillaume ^b   Foyer, Christine H ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84871752316     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.205690     Document Type: Article

References (123)

1. Acharya BR, Raina S, Maqbool SB, Jagadeeswaran G, Mosher SL, Appel HM, Schultz JC, Klessig DF, Raina R (2007) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J 50: 488-499
2. 3 world. Plant Physiol 147: 13-19
3. Albrecht C, Russinova E, Kemmerling B, Kwaaitaal M, de Vries SC (2008) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and-independent signaling pathways. Plant Physiol 148: 611-619
4. Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernández-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL, Heinlein M, et al (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6: e1001119
5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
6. Bartoli C, Pastori G, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123: 335-343
7. Bartoli CG, Casalongue C, Simontacchi M, Márquez-García B, Foyer CH (2012) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot (in press)
8. Bashandy T, Taconnat L, Renou JP, Meyer Y, Reichheld JP (2009) Accumulation of flavonoids in an ntra ntrb mutant leads to tolerance to UV-C. Mol Plant 2: 249-258
9. Bassel GW, Glaab E, Márquez J, Holdsworth MJ, Bacardit J (2011) Functional network construction in Arabidopsis using rule-based machine learning on large-scale data sets. Plant Cell 23: 3101-3116
10. 2 in soybean. J Exp Bot 418: 2139-2151
11. Bräutigam K, Dietzel L, Pfannschmidt T (2007) Plastid-nucleus communication: anterograde and retrograde signalling in development and function of plastids. In R Bock, ed, Cell and Molecular Biology of Plastids, Vol 19: Topics in Current Genetics. Springer, Berlin, pp 409-455
12. Burr CA, Leslie ME, Orlowski SK, Chen I, Wright CE, Daniels MJ, Liljegren SJ (2011) CAST AWAY, a membrane-associated receptor-like kinase, inhibits organ abscission in Arabidopsis. Plant Physiol 156: 1837-1850
13. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341-5351
14. Cela J, Chang C, Munné-Bosch S (2011) Accumulation of g-rather than a-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol 52: 1389-1400
15. Chaouch S, Queval G, Vanderauwera S, Mhamdi A, Vandorpe M, Langlois-Meurinne M, Van Breusegem F, Saindrenan P, Noctor G (2010) Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiol 153: 1692-1705
16. Chen K, Du L, Chen Z (2003) Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis. Plant Mol Biol 53: 61-74
17. Collins GG, Nie XL, Saltveit ME (1995) Heat shock proteins and chilling sensitivity of mung bean hypocotyls. J Exp Bot 46: 795-802
18. Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid deficient Arabidopsis thaliana mutants. Genetics 154: 847-856
19. Czernic P, Visser B, Sun W, Savoure A, Deslandes L, Marco Y, Van Montagu M, Verbruggen N (1999) Characterization of an Arabidopsis thaliana receptorlike protein kinase gene activated by oxidative stress and pathogen attack. Plant J 18: 321-327
20. D'Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-824
21. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268-281
22. Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172: 11-21
23. Desclos-Theveniau M, Arnaud D, Huang TY, Lin GJ, Chen WY, Lin YC, Zimmerli L (2012) The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 8: e1002513
24. Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172
25. Du L, Chen Z (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogen-and salicylic acid-induced WRKY DNAbinding proteins in Arabidopsis. Plant J 24: 837-847
26. Feng F, Yang F, RongW, Wu X, Zhang J, Chen S, He C, Zhou JM(2012) A Xanthomonas uridine 59-monophosphate transferase inhibits plant immune kinases. Nature 485: 114-118
27. Fey V, Wagner R, Brautigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmuller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280: 5318-5328
28. Fontes EP, Santos AA, Luz DF, Waclawovsky AJ, Chory J (2004) The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Genes Dev 18: 2545-2556
29. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63: 1637-1661
30. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28: 1056-1071
31. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxid Redox Signal 11: 862-905
32. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155: 93-100
33. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33: 691-705
34. Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng YT, Chen S, Li X, et al (2009) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6: 34-44
35. Gfeller A, Dubugnon L, Liechti R, Farmer EE (2010) Jasmonate biochemical pathway. Sci Signal 3: cm3
36. 2. Plant Cell Environ 35: 169-184
37. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66: 117-127
38. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011
39. González A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53: 814-827
40. Green MA, Fry SC (2005) Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 433: 83-87
41. 2 to activation of salicylic acid accumulation and signaling. Antioxid Redox Signal (in press)
42. Hok S, Danchin EG, Allasia V, Panabieres F, Attard A, Keller H (2011) An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease. Plant Cell Environ 34: 1944-1957
43. Huson DH, Scornavacca C (2012) Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol 61: 1061-1067
44. Hutchison CE, Li J, Argueso C, González M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, et al (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18: 3073-3087
45. Iriti M, Faoro R (2009) Chemical diversity and defense metabolism: how plants cope with pathogens and ozone pollution. Int J Mol Sci 10: 3371-3399
46. Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14: 108-117
47. 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
48. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654-657
49. Kerchev PI, Pellny TK, Vivancos PD, Kiddle G, Hedden P, Driscoll S, Vanacker H, Verrier PJ, Hancock RD, Foyer CH (2011) The transcription factor ABI-4 is required for the ascorbic acid-dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. Plant Cell 23: 3319-3334
50. Kohorn BD, Kobayashi M, Johansen S, Riese J, Huang LF, Koch K, Fu S, Dotson A, Byers N (2006) An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J 46: 307-316
51. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97: 2940-2945
52. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in PS II and related protection mechanism. Photosynth Res 98: 551-564
53. Kwezi L, Ruzvidzo O, Wheeler JI, Govender K, Iacuone S, Thompson PE, Gehring C, Irving HR (2011) The phytosulfokine (PSK) receptor is capable of guanylate cyclase activity and enabling cyclic GMP-dependent signaling in plants. J Biol Chem 286: 22580-22588
54. Lee IC, Hong SW, Whang SS, Lim PO, Nam HG, Koo JC (2011a) Agedependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant Cell Physiol 52: 651-662
55. Lee JY, Wang X, Cui W, Sager R, Modla S, Czymmek K, Zybaliov B, van Wijk K, Zhang C, Lu H, et al (2011b) A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23: 3353-3373
56. Lee KP, Kim C, Landgraf F, 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 USA 104: 10270-10275
57. Leferink NGH, van Duijn E, Barendregt A, Heck AJR, van Berkel WJH (2009) Galactonolactone dehydrogenase requires a redox-sensitive thiol for optimal production of vitamin C. Plant Physiol 150: 596-605
58. Leslie ME, Lewis MW, Youn JY, Daniels MJ, Liljegren SJ (2010) The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137: 467-476
59. Li RJ, Hua W, Lu YT (2006) Arabidopsis cytosolic glutamine synthetase AtGLN1;1 is a potential substrate of AtCRK3 involved in leaf senescence. Biochem Biophys Res Commun 342: 119-126
60. Liebler DC (1993) The role of metabolism in the antioxidant function of vitamin E. Crit Rev Toxicol 23: 147-169
61. Long SP, Ainsworth EA, Leakey ADB, Morgan PB (2005) Global food insecurity: treatment of major food crops with elevated carbon dioxide or ozone under large-scale fully open-air conditions suggests recent models may have overestimated future yields. Philos Trans R Soc Lond B Biol Sci 360: 2011-2020
62. 2 on plant abiotic stress tolerance. In JL Araus, GA Slafer, eds, Crop Stress Management and Global Climate Change. CABI, London, pp 85-104
63. Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2005) Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiol 138: 1422-1435
64. 2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287: 11717-11729
65. Meier S, Ruzvidzo O, Morse M, Donaldson L, Kwezi L, Gehring C (2010) The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. PLoS ONE 5: e8904
66. Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES (2008) Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biol 8: 76
67. 2 and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153: 1144-1160
68. Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133: 443-447
69. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133: 481-489
70. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613-19618
71. Molendijk AJ, Ruperti B, Singh MK, Dovzhenko A, Ditengou FA, Milia M, Westphal L, Rosahl S, Soellick TR, Uhrig J, et al (2008) A cysteinerich receptor-like kinase NCRK and a pathogen-induced protein kinase RBK1 are Rop GTPase interactors. Plant J 53: 909-923
72. Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid, and the NPR1 gene. Mol Plant Microbe Interact 23: 340-351
73. Munné-Bosch S (2005) The role of a-tocopherol in plant stress tolerance. J Plant Physiol 162: 743-748
74. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5: 388-395
75. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757: 742-749
76. NodineMD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev Cell 12: 943-956
77. Nowicka B, Kruk J (2012) Plastoquinol is more active than a-tocopherol in singlet oxygen scavenging during high light stress of Chlamydomonas reinhardtii. Biochim Biophys Acta 1817: 389-394
78. Osakabe Y, Mizuno S, Tanaka H, Maruyama K, Osakabe K, Todaka D, Fujita Y, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J Biol Chem 285: 9190-9201
79. Overmyer K, Broshe M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8: 335-342
80. Page M, Sultana N, Paszkiewicz K, Florance H, Smirnoff N (2012) The influence of ascorbate on anthocyanin accumulation during high light acclimation in Arabidopsis thaliana: further evidence for redox control of anthocyanin synthesis. Plant Cell Environ 35: 388-404
81. Parsons HT, Fry SC (2010) Reactive oxygen species-induced release of intracellular ascorbate in plant cell-suspension cultures and evidence for pulsing of net release rate. New Phytol 187: 332-342
82. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15: 939-951
83. Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, AlvarezME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis thaliana. Plant Physiol 139: 1291-1303
84. Pfannschmidt T, Schutze K, BrostM, Oelmuller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276: 36125-36130
85. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132: 1631-1641
86. Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 6: 379-389
87. Pineau B, Layoune O, Danon A, De Paepe R (2008) L-Galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J Biol Chem 283: 32500-32505
88. Pitorre D, Llauro C, Jobet E, Guilleminot J, Brizard JP, Delseny M, Lasserre E (2010) RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana. Planta 232: 1339-1353
89. 561 family. Planta 220: 365-375
90. Prentice IC, Farquhar GD, Fasham MJR, Goulden ML, Heimann M, Jaramillo VJ, Kheshgi HS, Le Quere C, Scholes RJ, Wallace DWR (2001) The carbon cycle and atmospheric carbon dioxide. In JT Houghton, Y Ding, DJ Griggs, M Noguer, PJ van der Linden, D Xiaosu, eds, Climate Change 2001: The Scientific Basis. Contribution ofWorking Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York, pp 183-239
91. 2+ channels. Proc Natl Acad Sci USA 107: 21193-21198
92. 2. Photosynth Res 97: 155-166
93. Queval G, Foyer CH (2012) Redox regulation of photosynthetic gene expression. Philos Trans R Soc Lond B 367: 3475-3485
94. 2-induced cell death. Plant J 52: 640-657
95. 2 in Arabidopsis. Plant Cell Environ 35: 374-387
96. Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci USA 109: 5535-5540
97. Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21: 3567-3584
98. Ryu SB, Costa A, Xin Z, Li PH (1995) Induction of cold hardiness by salt stress involves synthesis of cold and abscisic acid-responsive proteins in potato (Solanum commersonii Dun). Plant Cell Physiol 36: 1245-1251
99. Sandermann H (2008) Ecotoxicology of ozone: bioactivation of extracellular ascorbate. Biochem Biophys Res Commun 366: 271-274
100. Sandermann H, Ernst D, Heller W, Langebartels C (1998) Ozone: an abiotic elicitor of plant defense reactions. Trends Plant Sci 3: 47-50
101. Schottler MA, Kirchhoff H, Weis E (2004) The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol 136: 4265-4274
102. Shin J, Park E, Choi G (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 49: 981-994
103. Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132: 530-543
104. Short EF, North KA, Roberts MR, Hetherington AM, Shirras AD, McAinsh MR(2012) A stress-specific calcium signature regulating an ozone-responsive gene expression network in Arabidopsis. Plant J 71: 948-961
105. Sullivan JA, Gray JC (2002) Multiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. Plant J 32: 763-774
106. Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S, et al (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24: 2934-2948
107. Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16: 53-60
108. Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Abiotic stressinducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J 70: 599-613
109. Taniguchi M, Miyake H (2012) Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Curr Opin Plant Biol 15: 252-260
110. Tóth SZ, Puthur JT, Nagy V, Garab G (2009) Experimental evidence for ascorbate-dependent electron transport in leaves with inactive oxygenevolving complexes. Plant Physiol 149: 1568-1578
111. Trebst A, Depka B, Hollander-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 516: 156-160
112. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148: 960-968
113. Tzortzakis NG, Singleton I, Barnes JD (2007) Deployment of low-level ozone enrichment for the preservation of chilled fresh produce. Postharvest Biol Technol 43: 261-270
114. Tzortzakis NG, Taybi T, Roberts R, Singleton I, Borland A, Barnes JD (2011) Low-level atmospheric ozone exposure induces protection against Botrytis cinerea with down-regulation of ethylene-, jasmonate-and pathogenesisrelated genes in tomato fruit. Postharvest Biol Technol 61: 152-159
115. Vandenabeele S, Vanderauwera S, VuylstekeM, Rombauts S, Langebartels C, Seidlitz HK, ZabeauM, VanMontaguM, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39: 45-58
116. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139: 806-821
117. Veljovic-Jovanovic S, Pignocchi C, Noctor G, Foyer CH (2001) Low vitamin C in the vtc-1 mutant of Arabidopsis thaliana is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127: 426-435
118. Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, VanMontaguM, Inzé D, et al (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathionedependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97-110
119. Wagner D, Przybyla D, Camp ROD, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E, et al (2004) The genetic basis of singlet oxygeninduced stress responses of Arabidopsis thaliana. Science 306: 1183-1185
120. Won SK, Lee YJ, Lee HY, Heo YK, ChoM, Cho HT (2009) Cis-element-and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiol 150: 1459-1473
121. Wrzaczek M, Brosche M, Salojarvi J, Kangasjarvi S, Idanheimo N, Mersmann S, Robatzek S, Karpinski S, Karpinska B, Kangasjarvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptorlike protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10: 95
122. Xin Z, Wang A, Yang G, Gao P, Zheng ZL (2009) The Arabidopsis A4 subfamily of lectin receptor kinases negatively regulates abscisic acid response in seed germination. Plant Physiol 149: 434-444
123. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22: 508-522