[en] Studies of the singlet oxygen ((1)O2)-overproducing flu and chlorina1 (ch1) mutants of Arabidopsis (Arabidopsis thaliana) have shown that (1)O2-induced changes in gene expression can lead to either programmed cell death (PCD) or acclimation. A transcriptomic analysis of the ch1 mutant has allowed the identification of genes whose expression is specifically affected by each phenomenon. One such gene is OXIDATIVE SIGNAL INDUCIBLE1 (OXI1) encoding an AGC kinase that was noticeably induced by excess light energy and (1)O2 stress conditions leading to cell death. Photo-induced oxidative damage and cell death were drastically reduced in the OXI1 null mutant (oxi1) and in the double mutant ch1*oxi1 compared with the wild type and the ch1 single mutant, respectively. This occurred without any changes in the production rate of (1)O2 but was cancelled by exogenous applications of the phytohormone jasmonate. OXI1-mediated (1)O2 signaling appeared to operate through a different pathway from the previously characterized OXI1-dependent response to pathogens and H2O2 and was found to be independent of the EXECUTER proteins. In high-light-stressed plants, the oxi1 mutation was associated with reduced jasmonate levels and with the up-regulation of genes encoding negative regulators of jasmonate signaling and PCD. Our results show that OXI1 is a new regulator of (1)O2-induced PCD, likely acting upstream of jasmonate.
Abuqamar S, Chai MF, Luo H, Song F, Mengiste T (2008) Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell 20: 1964-1983
Alonso-Peral MM, Li J, Li Y, Allen RS, Schnippenkoetter W, Ohms S, White RG, Millar AA (2010) The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol 154: 757-771
Anthony RG, Henriques R, Helfer A, Mészáros T, Rios G, Testerink C, Munnik T, Deák M, Koncz C, Bögre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23: 572-581
Anthony RG, Khan S, Costa J, Pais MS, Bögre L (2006) The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281: 37536-37546
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
Armbruster U, Hertle A, Makarenko E, Zühlke J, Pribil M, Dietzmann A, Schliebner I, Aseeva E, Fenino E, Scharfenberg M, et al (2009) Chloroplast proteins without cleavable transit peptides: rare exceptions or a major constituent of the chloroplast proteome? Mol Plant 2: 1325-1335
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141: 391-396
Birtic S, Ksas B, Genty B, Mueller MJ, Triantaphylidès C, Havaux M (2011) Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. Plant J 67: 1103-1115
Bisby RH, Morgan CG, Hamblett I, Gorman AA (1999) Quenching of singlet oxygen by Trolox C, ascorbate, and amino acids: effects of pH and temperature. J Phys Chem A 103: 7454-7459
Bögre L, Okrész L, Henriques R, Anthony RG (2003) Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 8: 424-431
Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmüller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7: e1002051
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217: 67-75
Cominelli E, Gusmaroli G, Conti L, Allegra D, Petroni K, Tonelli C (2000) Role of Arabidopsis MYB transcription factors in osmotic stress. In JH Cherry, RD Locy, A Rychter, eds, Plant Tolerance to Abiotic Stresses: Role of Genetic Engineering. Kluwer, Dordrecht, The Netherlands, pp 181-194
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671
Dall’Osto L, Cazzaniga S, Havaux M, Bassi R (2010) Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol Plant 3: 576-593
Danon A, Miersch O, Felix G, Camp RG, Apel K (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41: 68-80
Danon A, Rotari VI, Gordon A, Mailhac N, Gallois P (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J Biol Chem 279: 779-787
Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19: 2225-2245
Douce R, Joyard J (1980) Plant galactolipids. In PK Stumpf, ed, The Biochemistry of Plants, Vol 4. Academic Press, New York, pp 321-362
Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RESactivated signaling. Annu Rev Plant Biol 64: 429-450
Fischer BB, Ledford HK, Wakao S, Huang SG, Casero D, Pellegrini M, Merchant SS, Koller A, Eggen RIL, Niyogi KK (2012) SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 109: E1302-E1311
Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, Mullineaux PM, Nonell S, Wilson MT, Baker NR (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J Exp Bot 57: 1725-1734
Forzani C, Carreri A, de la Fuente van Bentem S, Lecourieux D, Lecourieux F, Hirt H (2011) The Arabidopsis protein kinase Pto-interacting 1-4 is a common target of the oxidative signal-inducible 1 and mitogen-activated protein kinases. FEBS J 278: 1126-1136
Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperaturedependent resistance to wheat stripe rust. Science 323: 1357-1360
Gadjev I, Stone JM, Gechev TS (2008) Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int Rev Cell Mol Biol 270: 87-144
Garcia AV, Al-Yousif M, Hirt H (2012) Role of AGC kinases in plant growth and stress responses. Cell Mol Life Sci 69: 3259-3267
González-Pérez S, Gutiérrez J, García-García F, Osuna D, Dopazo J, Lorenzo Ó, Revuelta JL, Arellano JB (2011) Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiol 156: 1439-1456
Gutiérrez J, González-Pérez S, García-García F, Daly CT, Lorenzo O, Revuelta JL, McCabe PF, Arellano JB (2014) Programmed cell death activated by Rose Bengal in Arabidopsis thaliana cell suspension cultures requires functional chloroplasts. J Exp Bot 65: 3081-3095
Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145: 1506-1520
Havaux M, Triantaphylidès C, Genty B (2006) Autoluminescence imaging: a non-invasive tool for mapping oxidative stress. Trends Plant Sci 11: 480-484
Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B, et al (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res 14: 2176-2189
Hirashima M, Tanaka R, Tanaka A (2009) Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol 50: 719-729
Hirt H, Garcia AV, Oelmüller R (2011) AGC kinases in plant development and defense. Plant Signal Behav 6: 1030-1033
Huang W, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
Huang W, Sherman BT, Lempicki RA (2009b) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13
Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acidinduced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6: 462
Kim C, Apel K (2013) Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynth Res 116: 455-464
Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56: 337-346
Laloi C, Havaux M (2015) Key players of singlet oxygen-induced cell death in plants. Front Plant Sci 6: 39
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
Li H, Melø TB, Arellano JB, Razi Naqvi K (2012) Temporal profile of the singlet oxygen emission endogenously produced by photosystem II reaction centre in an aqueous buffer. Photosynth Res 112: 75-79
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60: 239-260
Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165-178
Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, et al (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103
Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57: 1795-1807
Matsui H, Yamazaki M, Kishi-Kaboshi M, Takahashi A, Hirochika H (2010) AGC kinase OsOxi1 positively regulates basal resistance through suppression of OsPti1a-mediated negative regulation. Plant Cell Physiol 51: 1731-1744
Mène-Saffrané L, Dubugnon L, Chételat A, Stolz S, Gouhier-Darimont C, Farmer EE (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284: 1702-1708
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51: 245-266
Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826-12831
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
Montillet JL, Cacas JL, Garnier L, Montané MH, Douki T, Bessoule JJ, Polkowska-Kowalczyk L, Maciejewska U, Agnel JP, Vial A, et al (2004) The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant J 40: 439-451
Mor A, Koh E, Weiner L, Rosenwasser S, Sibony-Benyamini H, Fluhr R (2014) Singlet oxygen signatures are detected independent of light or chloroplasts in response to multiple stresses. Plant Physiol 165: 249-261
Mueller MJ, Berger S (2009) Reactive electrophilic oxylipins: pattern recognition and signalling. Phytochemistry 70: 1511-1521
op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, et al (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15: 2320-2332
Petersen LN, Ingle RA, Knight MR, Denby KJ (2009) OXI1 protein kinase is required for plant immunity against Pseudomonas syringae in Arabidopsis. J Exp Bot 60: 3727-3735
Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11: 9-22
Przybyla D, Göbel C, Imboden A, Hamberg M, Feussner I, Apel K (2008) Enzymatic, but not non-enzymatic, 1O2-mediated peroxidation of polyunsaturated fatty acids forms part of the EXECUTER1-dependent stress response program in the flu mutant of Arabidopsis thaliana. Plant J 54: 236-248
Rademacher EH, Offringa R (2012) Evolutionary adaptations of plant AGC kinases: from light signaling to cell polarity regulation. Front Plant Sci 3: 250
Ragàs X, Jiménez-Banzo A, Sánchez-García D, Batllori X, Nonell S (2009) Singlet oxygen photosensitisation by the fluorescent probe Singlet Oxygen Sensor Green. Chem Commun (Camb) 20: 2920-2922
Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat JL, Havaux M (2012a) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158: 1267-1278
Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M (2012b) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci USA 109: 5535-5540
Ramel F, Ksas B, Akkari E, Mialoundama AS, Monnet F, Krieger-Liszkay A, Ravanat JL, Mueller MJ, Bouvier F, Havaux M (2013a) Lightinduced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. Plant Cell 25: 1445-1462
Ramel F, Ksas B, Havaux M (2013b) Jasmonate: a decision maker between cell death and acclimation in the response of plants to singlet oxygen. Plant Signal Behav 8: e26655
Redmond RW, Kochevar IE (2006) Spatially resolved cellular responses to singlet oxygen. Photochem Photobiol 82: 1178-1186
Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, et al (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427: 858-861
Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA, Zuo J (2007) Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res 17: 1030-1040
Shumbe L, Bott R, Havaux M (2014) Dihydroactinidiolide, a high lightinduced b-carotene derivative that can regulate gene expression and photoacclimation in Arabidopsis. Mol Plant 7: 1248-1251
Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3
Stingl N, Krischke M, Fekete A, Mueller MJ (2013) Analysis of defense signals in Arabidopsis thaliana leaves by ultra-performance liquid chromatography/tandem mass spectrometry: jasmonates, salicylic acid, abscisic acid. Methods Mol Biol 1009: 103-113
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445
Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130: 887-894
Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14: 219-228
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
Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147: 978-984
Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141: 384-390
Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306: 1183-1185
Xu Y, Chang P, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6: 1077-1085
Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15
Zhu X, Yang K, Wei X, Zhang Q, Rong W, Du L, Ye X, Qi L, Zhang Z (2015) The wheat AGC kinase TaAGC1 is a positive contributor to host resistance to the necrotrophic pathogen Rhizoctonia cerealis. J Exp Bot 66: 6591-6603
