Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast

Plant Physiology

Volumn 171, Issue 3, 2016, Pages 1541-1550

  Dietz, Karl Josef ^a   Turkan, Ismail ^b   Krieger Liszkay, Anja ^c  

^a BIELEFELD UNIVERSITY   (Germany)

^b EGE UNIVERSITY   (Turkey)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE;

ACCLIMATIZATION; CELL NUCLEUS; CHLOROPLAST; CYTOSOL; GENE EXPRESSION PROFILING; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PEROXISOME; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; SIGNAL TRANSDUCTION;

ACCLIMATIZATION; CELL NUCLEUS; CHLOROPLASTS; CYTOSOL; GENE EXPRESSION PROFILING; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATION-REDUCTION; PEROXISOMES; PHOTOSYNTHESIS; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84977561237     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00375     Document Type: Article

References (87)

1. Akter S, Huang J, Waszczak C, Jacques S, Gevaert K, Van Breusegem F, Messens J (2015) Cysteines under ROS attack in plants: a proteomics view. J Exp Bot 66: 2935-2944
2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
3. Awad J, Stotz HU, Fekete A, Krischke M, Engert C, Havaux M, Berger S, Mueller MJ (2015) 2-Cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water-water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions. Plant Physiol 167: 1592-1603
4. Baier M, Dietz KJ (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis: evidence from transgenic Arabidopsis. Plant Physiol 119: 1407-1414
5. 2 assimilation in diatoms. Nature 524: 366-369
6. 6f complex of oxygenic photosynthesis. Biochemistry 52: 8975-8983
7. Bienert GP, Chaumont F (2014) Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 1840: 1596-1604
8. Birk J, Ramming T, Odermatt A, Appenzeller-Herzog C (2013) Green fluorescent protein-based monitoring of endoplasmic reticulum redox poise. Front Genet 4: 108
9. Blanco NE, Guinea-Díaz M, Whelan J, Strand Å (2014) Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status. Philos Trans R Soc Lond B Biol Sci 369: 20130231
10. Bollig F, Winzen R, Gaestel M, Kostka S, Resch K, Holtmann H (2003) Affinity purification of ARE-binding proteins identifies polyA-binding protein 1 as a potential substrate in MK2-induced mRNA stabilization. Biochem Biophys Res Commun 301: 665-670
11. Brunkard JO, Runkel AM, Zambryski PC (2015) Chloroplasts extend stromules independently and in response to internal redox signals. Proc Natl Acad Sci USA 112: 10044-10049
12. Brzezowski P, Wilson KE, Gray GR (2012) The PSBP2 protein of Chlamydomonas reinhardtii is required for singlet oxygen-dependent signaling. Planta 236: 1289-1303
13. Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K, Modla S, Czymmek K, Dinesh-Kumar SP (2015) Chloroplast stromules function during innate immunity. Dev Cell 34: 45-57
14. Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ (2016) Learning the languages of the chloroplast: retrograde signalling and beyond. Annu Rev Plant Biol 67: 25-53
15. Courteille A, Vesa S, Sanz-Barrio R, Cazalé AC, Becuwe-Linka N, Farran I, Havaux M, Rey P, Rumeau D (2013) Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiol 161: 508-520
16. Dietz KJ (2015) Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J Exp Bot 66: 2401-2414
17. Dietz KJ (2016) Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol Cells 39: 20-25
18. Dietz KJ, Heber U (1984) Rate limiting factors in leaf photosynthesis. 1. Carbon fluxes in the Calvin cycle. Biochim Biophys Acta 767: 432-443
19. Dixon DP, Van Lith M, Edwards R, Benham A (2003) Cloning and initial characterization of the Arabidopsis thaliana endoplasmic reticulum oxidoreductins. Antioxid Redox Signal 5: 389-396
20. Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, de Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15: 1212-1226
21. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23: 3992-4012
22. Fey V, Wagner R, Braütigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller 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
23. Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RIL (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 581: 5555-5560
24. Foyer CH, Karpinska B, Krupinska K (2014) The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis. Philos Trans R Soc Lond B Biol Sci 369: 20130226
25. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141: 436-445
26. Gläßer C, Haberer G, Finkemeier I, Pfannschmidt T, Kleine T, Leister D, Dietz KJ, Häusler RE, Grimm B, Mayer KF (2014) Meta-analysis of retrograde signaling in Arabidopsis thaliana reveals a core module of genes embedded in complex cellular signaling networks. Mol Plant 7: 1167-1190
27. Gray JC, Hansen MR, Shaw DJ, Graham K, Dale R, Smallman P, Natesan SK, Newell CA (2012) Plastid stromules are induced by stress treatments acting through abscisic acid. Plant J 69: 387-398
28. Gray JC, Sullivan JA, Hibberd JM, Hansen MR (2001) Stromules: mobile protrusions and interconnections between plastids. Plant Biol 3: 223-233
29. Hanson MR, Sattarzadeh A (2013) Trafficking of proteins through plastid stromules. Plant Cell 25: 2774-2782
30. Hebbelmann I, Selinski J, Wehmeyer C, Goss T, Voss I, Mulo P, Kangasjärvi S, Aro EM, Oelze ML, Dietz KJ, et al (2012) Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. J Exp Bot 63: 1445-1459
31. 2 signalling in Arabidopsis. Philos Trans R Soc Lond B Biol Sci 369: 20130228
32. Hiltscher H, Rudnik R, Shaikhali J, Heiber I, Mellenthin M, Meirelles Duarte I, Schuster G, Kahmann U, Baier M (2014) The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes. Front Plant Sci 5: 475
33. Holzinger A, Buchner O, Lütz C, Hanson MR (2007) Temperaturesensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana. Protoplasma 230: 23-30
34. Hosein B, Palmer G (1983) The kinetics and mechanisms of oxidation of reduced spinach ferredoxin by molecular oxygen and its reduced products. Biochim Biophys Acta 723: 383-390
35. Isemer R, Mulisch M, Schäfer A, Kirchner S, Koop HU, Krupinska K (2012) Recombinant Whirly1 translocates from transplastomic chloroplasts to the nucleus. FEBS Lett 586: 85-88
36. Johnson GN, Rutherford AW, Krieger A (1995) A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution. Biochim Biophys Acta 1229: 202-207
37. Kangasjärvi S, Lepistö A, Hännikäinen K, Piippo M, Luomala EM, Aro EM, Rintamäki E (2008) Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem J 412: 275-285
38. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K, Herrfurth C, Feussner I, Apel K (2012) Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell 24: 3026-3039
39. 2 reduction by photosystem I involves phylloquinone under steady-state illumination. FEBS Lett 588: 4364-4368
40. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98: 551-564
41. Kwok EY, Hanson MR (2003) Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J 35: 16-26
42. Kwon KC, Verma D, Jin S, Singh ND, Daniell H (2013) Release of proteins from intact chloroplasts induced by reactive oxygen species during biotic and abiotic stress. PLoS ONE 8: e67106
43. Lepistö A, Pakula E, Toivola J, Krieger-Liszkay A, Vignols F, Rintamäki E (2013) Deletion of chloroplast NADPH-dependent thioredoxin reductase results in inability to regulate starch synthesis and causes stunted growth under short-day photoperiods. J Exp Bot 64: 3843-3854
44. Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22: 2930-2942
45. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51: 941-954
46. López MA, Vicente J, Kulasekaran S, Vellosillo T, Martínez M, Irigoyen ML, Cascón T, Bannenberg G, Hamberg M, Castresana C (2011) Antagonistic role of 9-lipoxygenase-derived oxylipins and ethylene in the control of oxidative stress, lipid peroxidation and plant defence. Plant J 67: 447-458
47. Mehler AH (1951) Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. Arch Biochem Biophys 34: 339-351
48. Mehrshahi P, Stefano G, Andaloro JM, Brandizzi F, Froehlich JE, DellaPenna D (2013) Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. Proc Natl Acad Sci USA 110: 12126-12131
49. Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51: 245-266
50. Michelet L, Roach T, Fischer BB, Bedhomme M, Lemaire SD, Krieger-Liszkay A (2013) Down-regulation of catalase activity allows transient accumulation of a hydrogen peroxide signal in Chlamydomonas reinhardtii. Plant Cell Environ 36: 1204-1213
51. Miret JA, Munné-Bosch S (2015) Redox signaling and stress tolerance in plants: a focus on vitamin E. Ann N Y Acad Sci 1340: 29-38
52. Mock HP, Dietz KJ (2016) Redox proteomics for the assessment of redoxrelated posttranslational regulation in plants. Biochim Biophys Acta 1864: 967-973
53. Moore M, Gossmann N, Dietz KJ (2016) Redox regulation of cytosolic translation in plants. Trends Plant Sci 21: 388-397
54. Moustafa K, AbuQamar S, Jarrar M, Al-Rajab AJ, Trémouillaux-Guiller J (2014) MAPK cascades and major abiotic stresses. Plant Cell Rep 33: 1217-1225
55. Mubarakshina MM, Ivanov BN (2010) The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes. Physiol Plant 140: 103-110
56. Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281: 38697-38704
57. Natesan SKA, Sullivan JA, Gray JC (2005) Stromules: a characteristic cellspecific feature of plastid morphology. J Exp Bot 56: 787-797
58. Nath K, Jajoo A, Poudyal RS, Timilsina R, Park YS, Aro EM, Nam HG, Lee CH (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Lett 587: 3372-3381
59. Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8: 87-99
60. Oelze ML, Muthuramalingam M, Vogel MO, Dietz KJ (2014) The link between transcript regulation and de novo protein synthesis in the retrograde high light acclimation response of Arabidopsis thaliana. BMC Genomics 15: 320
61. Oikawa K, Matsunaga S, Mano S, Kondo M, Yamada K, Hayashi M, Kagawa T, Kadota A, Sakamoto W, Higashi S, et al (2015) Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat Plants 1: 15035
62. op den Camp RG, 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
63. Ozgur R, Turkan I, Uzilday B, Sekmen AH (2014) Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana. J Exp Bot 65: 1377-1390
64. Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8: 1757-1764
65. Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817: 218-231
66. Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8: 546-553
67. 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
68. Ramel F, Mialoundama AS, Havaux M (2013) Nonenzymic carotenoid oxidation and photooxidative stress signalling in plants. J Exp Bot 64: 799-805
69. 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
70. Rosenwasser S, Fluhr R, Joshi JR, Leviatan N, Sela N, Hetzroni A, Friedman H (2013) ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiol 163: 1071-1083
71. Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26: 648-653
72. Schattat M, Barton K, Baudisch B, Klösgen RB, Mathur J (2011) Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiol 155: 1667-1677
73. 2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol Plant 7: 1191-1210
74. Shao N, Duan GY, Bock R (2013) A mediator of singlet oxygen responses in Chlamydomonas reinhardtii and Arabidopsis identified by a luciferasebased genetic screen in algal cells. Plant Cell 25: 4209-4226
75. Shirao M, Kuroki S, Kaneko K, Kinjo Y, Tsuyama M, Förster B, Takahashi S, Badger MR (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54: 1152-1163
76. Shumbe L, Chevalier A, Legeret B, Taconnat L, Monnet F, Havaux M (2016) Singlet oxygen-induced cell death in Arabidopsis under high light stress is controlled by OXI1 kinase. Plant Physiol 170: 1757-1771
77. Simková K, Moreau F, Pawlak P, Vriet C, Baruah A, Alexandre C, Hennig L, Apel K, Laloi C (2012) Integration of stress-related and reactive oxygen species-mediated signals by topoisomerase VI in Arabidopsis thaliana. Proc Natl Acad Sci USA 109: 16360-16365
78. Strand DD, Fisher N, Davis GA, Kramer DM (2016) Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids. Biochim Biophys Acta 1857: 1-6
79. Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM (2015) Activation of cyclic electron flow by hydrogen peroxide in vivo. Proc Natl Acad Sci USA 112: 5539-5544
80. Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2: 477
81. Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci USA 103: 19587-19592
82. Takagi D, Takumi S, Hashiguchi M, Sejima T, Miyake C (2016) Superoxide and singlet oxygen produced within the thylakoid membrane both cause photosystem I photoinhibition. Plant Physiol 171: 1626-1634
83. Tomaz T, Bagard M, Pracharoenwattana I, Lindén P, Lee CP, Carroll AJ, Ströher E, Smith SM, Gardeström P, Millar AH (2010) Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis. Plant Physiol 154: 1143-1157
84. Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J, Dietz KJ (2014) Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell 26: 1151-1165
85. Walley J, Xiao Y, Wang JZ, Baidoo EE, Keasling JD, Shen Z, Briggs SP, Dehesh K (2015) Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proc Natl Acad Sci USA 112: 6212-6217
86. Yoshida K, Terashima I, Noguchi K (2006) Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. Plant Cell Physiol 47: 22-31
87. Yu Q, Feilke K, Krieger-Liszkay A, Beyer P (2014) Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim Biophys Acta 1837: 1284-1292