1932

Abstract

As fixed organisms, plants are especially affected by changes in their environment and have consequently evolved extensive mechanisms for acclimation and adaptation. Initially considered by-products from aerobic metabolism, reactive oxygen species (ROS) have emerged as major regulatory molecules in plants and their roles in early signaling events initiated by cellular metabolic perturbation and environmental stimuli are now established. Here, we review recent advances in ROS signaling. Compartment-specific and cross-compartmental signaling pathways initiated by the presence of ROS are discussed. Special attention is dedicated to established and hypothetical ROS-sensing events. The roles of ROS in long-distance signaling, immune responses, and plant development are evaluated. Finally, we outline the most challenging contemporary questions in the field of plant ROS biology and the need to further elucidate mechanisms allowing sensing, signaling specificity, and coordination of multiple signals.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042817-040322
2018-04-29
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/arplant/69/1/annurev-arplant-042817-040322.html?itemId=/content/journals/10.1146/annurev-arplant-042817-040322&mimeType=html&fmt=ahah

Literature Cited

  1. Ahlfors R, Lång S, Overmyer K, Jaspers P, Brosché M. 1.  et al. 2004. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–37 [Google Scholar]
  2. Arnaud D, Lee S, Takebayashi Y, Choi D, Choi J. 2.  et al. 2017. Cytokinin-mediated regulation of reactive oxygen species homeostasis modulates stomatal immunity in Arabidopsis. Plant Cell 29:543–59 [Google Scholar]
  3. Asada K.3.  2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–96 [Google Scholar]
  4. Attacha S, Solbach D, Bela K, Moseler A, Wagner S. 4.  et al. 2017. Glutathione peroxidase-like enzymes cover five distinct cell compartments and membrane surfaces in Arabidopsis thaliana. Plant Cell Environ 40:1281–95 [Google Scholar]
  5. Awad J, Stotz HU, Fekete A, Krischke M, Engert C. 5.  et al. 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 167:1592–603 [Google Scholar]
  6. Bienert GP, Chaumont F. 6.  2014. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta 1840:1596–604 [Google Scholar]
  7. Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T. 7.  et al. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47:851–63 [Google Scholar]
  8. Bleier L, Dröse S. 8.  2013. Superoxide generation by complex III: from mechanistic rationales to functional consequences. Biochim. Biophys. Acta 1827:1320–31 [Google Scholar]
  9. Bohrer A-S, Kopriva S, Takahashi H. 9.  2015. Plastid-cytosol partitioning and integration of metabolic pathways for APS/PAPS biosynthesis in Arabidopsis thaliana. Front. Plant Sci 5:751 [Google Scholar]
  10. Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U. 10.  2013. ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLOS Biol 11:e1001719 [Google Scholar]
  11. Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J. 11.  et al. 2015. Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLOS Genet 11:e1005373 [Google Scholar]
  12. Brandt B, Munemasa S, Wang C, Nguyen D, Yong T. 12.  et al. 2015. Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4:e03599 [Google Scholar]
  13. Brosché M, Blomster T, Salojärvi J, Cui F, Sipari N. 13.  et al. 2014. Transcriptomics and functional genomics of ROS-induced cell death regulation by RADICAL-INDUCED CELL DEATH1. PLOS Genet 10:e1004112 [Google Scholar]
  14. Brunkard JO, Runkel AM, Zambryski PC. 14.  2015. Chloroplasts extend stromules independently and in response to internal redox signals. PNAS 112:10044–49 [Google Scholar]
  15. Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K. 15.  et al. 2015. Chloroplast stromules function during innate immunity. Dev. Cell 34:45–57Demonstrated the function and role of stromules in response to bacterial effectors in H2O2 translocation from the chloroplast to the nucleus. [Google Scholar]
  16. Chan KX, Mabbitt PD, Phua SY, Mueller JW, Nisar N. 16.  et al. 2016. Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase. PNAS 113:4567–76Identified a chloroplastic ROS/redox sensor through redox- or H2O2-dependent oxidative inactivation of the PAP phosphatase, SAL1. [Google Scholar]
  17. Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ. 17.  2016. Learning the languages of the chloroplast: retrograde signaling and beyond. Annu. Rev. Plant Biol. 67:25–53 [Google Scholar]
  18. Chaouch S, Queval G, Vanderauwera S, Mhamdi A, Vandorpe M. 18.  et al. 2010. Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiol 153:1692–705 [Google Scholar]
  19. Chater C, Peng K, Movahedi M, Dunn JA, Walker HJ. 19.  et al. 2015. Elevated CO2-induced responses in stomata require ABA and ABA signaling. Curr. Biol. 25:2709–16 [Google Scholar]
  20. Chen Z, Silva H, Klessig D. 20.  1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–86 [Google Scholar]
  21. Cheng F, Blackburn K, Lin Y, Goshe MB, Williamson JD. 21.  2009. Absolute protein quantification by LC/MSE for global analysis of salicylic acid-induced plant protein secretion responses. J. Proteome Res. 8:82–93 [Google Scholar]
  22. Chew O, Whelan J, Millar AH. 22.  2003. Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem. 278:46869–77 [Google Scholar]
  23. Choi W-G, Miller G, Wallace I, Harper J, Mittler R, Gilroy S. 23.  2017. Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J 90:698–707 [Google Scholar]
  24. Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S. 24.  2014. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. PNAS 111:6497–502 [Google Scholar]
  25. Costa A, Drago I, Behera S, Zottini M, Pizzo P. 25.  et al. 2010. H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2+-dependent scavenging system. Plant J 62:760–72 [Google Scholar]
  26. Couto D, Zipfel C. 26.  2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52 [Google Scholar]
  27. Daudi A, Cheng Z, O'Brien JA, Mammarella N, Khan S. 27.  et al. 2012. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–87 [Google Scholar]
  28. De Clercq I, Vermeirssen V, Van Aken O, Vandepoele K, Murcha MW. 28.  et al. 2013. The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell 25:3472–90Characterized the ER-localized transcription factor ANAC013 during mitochondrial retrograde stress signaling. [Google Scholar]
  29. de Souza A, Wang J-Z, Dehesh K. 29.  2017. Retrograde signals: integrators of interorganellar communication and orchestrators of plant development. Annu. Rev. Plant Biol. 68:85–108 [Google Scholar]
  30. de Torres Zabala M, Littlejohn G, Jayaraman S, Studholme D, Bailey T. 30.  et al. 2015. Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat. Plants. 1:15074 [Google Scholar]
  31. Del Rio LA, Lopez-Huertas E. 31.  2016. ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol 57:1364–76 [Google Scholar]
  32. Delaunay A, Pflieger D, Barrault M-B, Vinh J, Toledano MB. 32.  2002. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–81 [Google Scholar]
  33. Denecker J, Hoeberichts F, Muhlenbock P, Van Breusegem F, Van Der Kelen K. 33.  2013. Means and methods for the reduction of photorespiration in crops WO Patent No. 2014147249A1 [Google Scholar]
  34. Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P. 34.  et al. 2011. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol 156:1364–74 [Google Scholar]
  35. Dietz K-J.35.  2011. Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal. 15:1129–59 [Google Scholar]
  36. Dietz K-J.36.  2014. Redox regulation of transcription factors in plant stress acclimation and development. Antioxid. Redox Signal. 21:1356–72 [Google Scholar]
  37. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY. 37.  2004. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279:22284–93 [Google Scholar]
  38. Drazic A, Miura H, Peschek J, Le Y, Bach NC. 38.  et al. 2013. Methionine oxidation activates a transcription factor in response to oxidative stress. PNAS 110:9493–98 [Google Scholar]
  39. Dubiella U, Seybold H, Durian G, Komander E, Lassig R. 39.  et al. 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. PNAS 110:8744–49Demonstrated MAMP- and ROS-induced phosphorylation of RBOHD via the Ca2+ sensor CPK5. [Google Scholar]
  40. Erickson JL, Kantek M, Schattat MH. 40.  2017. Plastid-nucleus distance alters the behavior of stromules. Front. Plant Sci. 8:1135 [Google Scholar]
  41. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D. 41.  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 [Google Scholar]
  42. Evans MJ, Choi W-G, Gilroy S, Morris RJ. 42.  2016. A ROS-assisted calcium wave dependent on AtRBOHD and TPC1 propagates the systemic response to salt stress. Plant Physiol 171:1771–84 [Google Scholar]
  43. Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM. 43.  2017. Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat. Commun. 8:49Identified a novel retrograde mechanism for direct nuclear transport of H2O2 from chloroplasts in close proximity to nuclei. [Google Scholar]
  44. Farmer EE, Mueller MJ. 44.  2013. ROS-mediated lipid peroxidation and RES-activated signaling. Annu. Rev. Plant Biol. 64:429–50 [Google Scholar]
  45. Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ. 45.  2005. The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J. Biol. Chem. 280:12168–80 [Google Scholar]
  46. Fischer BB, Hideg É, Krieger-Liszkay A. 46.  2013. Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid. Redox Signal. 18:2145–62 [Google Scholar]
  47. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H. 47.  et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–46 [Google Scholar]
  48. Foyer C, Noctor G. 48.  2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–71 [Google Scholar]
  49. Foyer CH, Noctor G. 49.  2016. Stress-triggered redox signalling: What's in pROSpect?. Plant. Cell Environ. 39:951–64 [Google Scholar]
  50. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G. 50.  et al. 2008. The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147:595–610 [Google Scholar]
  51. Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C. 51.  2015. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27:1945–54 [Google Scholar]
  52. Hamann T, Bennett M, Mansfield J, Somerville C. 52.  2009. Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J 57:1015–26 [Google Scholar]
  53. Hanson MR, Sattarzadeh A. 53.  2013. Trafficking of proteins through plastid stromules. Plant Cell 25:2774–82 [Google Scholar]
  54. Hiltscher H, Rudnik R, Shaikhali J, Heiber I, Mellenthin M. 54.  et al. 2014. The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes. Front. Plant Sci. 5:475 [Google Scholar]
  55. Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH. 55.  2016. The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiol 171:1551–59 [Google Scholar]
  56. Iglesias-Baena I, Barranco-Medina S, Sevilla F, Lázaro J-J. 56.  2011. The dual-targeted plant sulfiredoxin retroreduces the sulfinic form of atypical mitochondrial peroxiredoxin. Plant Physiol 155:944–55 [Google Scholar]
  57. Ishiga Y, Ishiga T, Wangdi T, Mysore KS, Uppalapati SR. 57.  2012. NTRC and chloroplast-generated reactive oxygen species regulate Pseudomonas syringae pv. tomato disease development in tomato and Arabidopsis. Mol. Plant-Microbe Interact 25:294–306 [Google Scholar]
  58. Ishiga Y, Watanabe M, Ishiga T, Tohge T, Matsuura T. 58.  et al. 2017. The SAL-PAP chloroplast retrograde pathway contributes to plant immunity by regulating glucosinolate pathway and phytohormone signaling. Mol. Plant-Microbe Interact. 30:829–41 [Google Scholar]
  59. Jacques S, Ghesquière B, De Bock P-J, Demol H, Wahni K. 59.  et al. 2015. Protein methionine sulfoxide dynamics in Arabidopsis thaliana under oxidative stress. Mol. Cell. Proteom. 14:1217–29 [Google Scholar]
  60. Jarsch IK, Konrad SSA, Stratil TF, Urbanus SL, Szymanski W. 60.  et al. 2014. Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698–711 [Google Scholar]
  61. Jaspers P, Blomster T, Brosche M, Salojärvi J, Ahlfors R. 61.  et al. 2009. Unequally redundant RCD1 and SRO1 mediate stress and developmental responses and interact with transcription factors. Plant J 60:268–79 [Google Scholar]
  62. Jones AM, Xuan Y, Xu M, Wang R-S, Ho C-H. 62.  et al. 2014. Border control—a membrane-linked interactome of Arabidopsis. Science 344:711–16 [Google Scholar]
  63. Jones MA, Raymond MJ, Yang Z, Smirnoff N. 63.  2007. NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J. Exp. Bot. 58:1261–70 [Google Scholar]
  64. Kadota Y, Shirasu K, Zipfel C. 64.  2015. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56:1472–80 [Google Scholar]
  65. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S. 65.  et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell. 54:43–55Demonstrated direct activation of the NADPH oxidase RBOHD by the protein kinase BIK1. [Google Scholar]
  66. Kangasjärvi J, Jaspers P, Kollist H. 66.  2005. Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28:1021–36 [Google Scholar]
  67. Kangasjärvi J, Talvinen J, Utriainen M, Karjalainen R. 67.  1994. Plant defence systems induced by ozone. Plant Cell Environ 17:783–94 [Google Scholar]
  68. Karpińska B, Zhang K, Rasool B, Pastok D, Morris J. 68.  et al. 2017. The redox state of the apoplast influences the acclimation of photosynthesis and leaf metabolism to changing irradiance. Plant. Cell Environ. In press. https://doi.org/10.1111/pce.12960 [Crossref] [Google Scholar]
  69. Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S. 69.  et al. 2014. Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–80 [Google Scholar]
  70. Kerchev P, Waszczak C, Lewandowska A, Willems P, Shapiguzov A. 70.  et al. 2016. Lack of GLYCOLATE OXIDASE1, but not GLYCOLATE OXIDASE2, attenuates the photorespiratory phenotype of CATALASE2-deficient Arabidopsis. Plant Physiol 171:1704–19 [Google Scholar]
  71. Khokon MA, Hossain MA, Munemasa S, Uraji M, Nakamura Y. 71.  et al. 2010. Yeast elicitor-induced stomatal closure and peroxidase-mediated ROS production in Arabidopsis. Plant Cell Physiol 51:1915–21 [Google Scholar]
  72. Khokon MA, Uraji M, Munemasa S, Okuma E, Nakamura Y. 72.  et al. 2010. Chitosan-induced stomatal closure accompanied by peroxidase-mediated reactive oxygen species production in Arabidopsis. Biosci. Biotechnol. Biochem 74:2313–15 [Google Scholar]
  73. Kimura S, Waszczak C, Hunter K, Wrzaczek M. 73.  2017. Bound by fate: reactive oxygen species in receptor-like kinase signaling. Plant Cell 29:638–54 [Google Scholar]
  74. Kneeshaw S, Keyani R, Delorme-Hinoux V, Imrie L, Loake GJ. 74.  et al. 2017. Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes. PNAS 114:8414–19 [Google Scholar]
  75. Kong D, Hu HC, Okuma E, Lee Y, Lee HS. 75.  et al. 2016. l-Met activates Arabidopsis GLR Ca2+ channels upstream of ROS production and regulates stomatal movement. Cell Rep 17:2553–61 [Google Scholar]
  76. Krieger-Liszkay A, Trebst A. 76.  2006. Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre. J. Exp. Bot. 57:1677–84 [Google Scholar]
  77. Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA. 77.  et al. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–33 [Google Scholar]
  78. Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T. 78.  2014. Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106 [Google Scholar]
  79. Lee S-H, Li C-W, Koh KW, Chuang H-Y, Chen Y-R. 79.  et al. 2014. MSRB7 reverses oxidation of GSTF2/3 to confer tolerance of Arabidopsis thaliana to oxidative stress. J. Exp. Bot. 65:5049–62 [Google Scholar]
  80. Lee Y, Rubio MC, Alassimone J, Geldner N. 80.  2013. A mechanism for localized lignin deposition in the endodermis. Cell 153:402–12 [Google Scholar]
  81. Leister D.81.  2017. Piecing the puzzle together: the central role of ROS and redox hubs in chloroplast retrograde signaling. Antioxid. Redox Signal. In press. https://doi.org/10.1089/ars.2017.7392 [Crossref] [Google Scholar]
  82. Li J, Liu J, Wang G, Cha J-Y, Li G. 82.  et al. 2015. A chaperone function of NO CATALASE ACTIVITY1 is required to maintain catalase activity and for multiple stress responses in Arabidopsis. Plant Cell 27:908–25 [Google Scholar]
  83. Li L, Li M, Yu L, Zhou Z, Liang X. 83.  et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–38 [Google Scholar]
  84. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. 84.  2007. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51:941–54 [Google Scholar]
  85. Macho AP, Boutrot F, Rathjen JP, Zipfel C. 85.  2012. Aspartate oxidase plays an important role in Arabidopsis stomatal immunity. Plant Physiol 159:1845–56 [Google Scholar]
  86. Martinez C, Montillet JL, Bresson E, Agnel JP, Dai GH. 86.  et al. 1998. Apoplastic peroxidase generates superoxide anions in cells of cotton cotyledons undergoing the hypersensitive reaction to Xanthomonas campestris pv. malvacearum Race 18. Mol. Plant-Microbe Interact. 11:1038–47 [Google Scholar]
  87. Mattila H, Khorobrykh S, Havurinne V, Tyystjärvi E. 87.  2015. Reactive oxygen species: reactions and detection from photosynthetic tissues. J. Photochem. Photobiol. 152:176–214 [Google Scholar]
  88. Meinhard M, Rodriguez PL, Grill E. 88.  2002. The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214:775–82 [Google Scholar]
  89. Mersmann S, Bourdais G, Rietz S, Robatzek S. 89.  2010. Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 154:391–400 [Google Scholar]
  90. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N. 90.  et al. 2007. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–86 [Google Scholar]
  91. Meyer Y, Belin C, Delorme-Hinoux V, Reichheld J-P, Riondet C. 91.  2012. Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid. Redox Signal. 17:1124–60 [Google Scholar]
  92. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G. 92.  2010. Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J. Exp. Bot. 61:4197–220 [Google Scholar]
  93. Miao Y, Lv D, Wang P, Wang X-C, Chen J. 93.  et al. 2006. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–66 [Google Scholar]
  94. Miller G, Schlauch K, Tam R, Cortes D, Torres MA. 94.  et al. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45Identified RBOHD as a key component in a self-propagating cell-to-cell signaling mechanism and H2O2 as a systemic signal molecule. [Google Scholar]
  95. Mishina NM, Tyurin-Kuzmin PA, Markvicheva KN, Vorotnikov AV, Tkachuk VA. 95.  et al. 2011. Does cellular hydrogen peroxide diffuse or act locally?. Antioxid. Redox Signal. 14:1–7 [Google Scholar]
  96. Møller IM, Sweetlove LJ. 96.  2010. ROS signalling–specificity is required. Trends Plant Sci 15:370–74 [Google Scholar]
  97. Morales J, Kadota Y, Zipfel C, Molina A, Torres M-A. 97.  2016. The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J. Exp. Bot. 67:1663–76 [Google Scholar]
  98. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD. 98.  et al. 2008. Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–24 [Google Scholar]
  99. Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 99.  2013. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422–26 [Google Scholar]
  100. Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A. 100.  2010. Production and diffusion of chloroplastic H2O2 and its implication to signalling. J. Exp. Bot. 61:3577–87 [Google Scholar]
  101. Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V. 101.  et al. 2006. The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J. Exp. Bot. 57:3033–42 [Google Scholar]
  102. Ng S, Ivanova A, Duncan O, Law SR, Van Aken O. 102.  et al. 2013. A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25:3450–71Characterized the ER-localized transcription factor ANAC017 during mitochondrial and chloroplast redox-related retrograde signaling. [Google Scholar]
  103. Noctor G, Mhamdi A, Foyer CH. 103.  2016. Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant. Cell Environ. 39:1140–60 [Google Scholar]
  104. Nomura H, Komori T, Uemura S, Kanda Y, Shimotani K. 104.  et al. 2012. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Commun 3:926Demonstrated the requirement of chloroplastic CAS in mediating Ca2+ signals for the activation of immune signaling. [Google Scholar]
  105. O'Shea C, Kryger M, Stender EGP, Kragelund BB, Willemoës M, Skriver K. 105.  2015. Protein intrinsic disorder in Arabidopsis NAC transcription factors: transcriptional activation by ANAC013 and ANAC046 and their interactions with RCD1. Biochem. J. 465:281–94 [Google Scholar]
  106. Overmyer K, Brosché M, Pellinen R, Kuittinen T, Tuominen H. 106.  et al. 2005. Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol 137:1092–104 [Google Scholar]
  107. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B. 107.  et al. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–34 [Google Scholar]
  108. Pornsiriwong W, Estavillo GM, Chan KX, Tee EE, Ganguly D. 108.  et al. 2017. A chloroplast retrograde signal, 3′-phosphoadenosine 5′-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. eLife 6:e23361 [Google Scholar]
  109. Price AH.109.  1990. A possible role for calcium in oxidative plant stress. Free Radic. Res. Commun. 10:345–49 [Google Scholar]
  110. Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakière B. 110.  et al. 2007. Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J 52:640–57 [Google Scholar]
  111. Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat J-L, Havaux M. 111.  2012. Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158:1267–78 [Google Scholar]
  112. Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M. 112.  2012. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. PNAS 109:5535–40Identified a novel 1O2 retrograde signaling pathway utilizing the breakdown product of β-carotene. [Google Scholar]
  113. Raymond J, Segré D. 113.  2006. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–67 [Google Scholar]
  114. Rey P, Bécuwe N, Barrault M-B, Rumeau D, Havaux M. 114.  et al. 2007. The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J 49:505–14 [Google Scholar]
  115. Rodrigues O, Reshetnyak G, Grondin A, Saijo Y, Leonhardt N. 115.  et al. 2017. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. PNAS 114:9200–5 [Google Scholar]
  116. Roos G, Foloppe N, Messens J. 116.  2013. Understanding the pKa of redox cysteines: the key role of hydrogen bonding. Antioxid. Redox Signal. 18:94–127 [Google Scholar]
  117. Roos G, Messens J. 117.  2011. Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic. Biol. Med. 51:314–26 [Google Scholar]
  118. Schürmann P, Buchanan BB. 118.  2008. The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid. Redox Signal. 10:1235–74 [Google Scholar]
  119. Sierla M, Waszczak C, Vahisalu T, Kangasjärvi J. 119.  2016. Reactive oxygen species in the regulation of stomatal movements. Plant Physiol 171:1569–80 [Google Scholar]
  120. Sobotta MC, Liou W, Stöcker S, Talwar D, Oehler M. 120.  et al. 2014. Peroxiredoxin-2 and STAT3 form a redox relay for H2O2 signaling. Nat. Chem. Biol. 11:64–70 [Google Scholar]
  121. Steinhorst L, Kudla J. 121.  2013. Calcium and reactive oxygen species rule the waves of signaling. Plant Physiol 163:471–85 [Google Scholar]
  122. Steinhorst L, Kudla J. 122.  2014. Signaling in cells and organisms—calcium holds the line. Curr. Opin. Plant Biol. 22:14–21 [Google Scholar]
  123. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. 123.  2011. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14:691–99 [Google Scholar]
  124. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. 124.  2008. Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–44 [Google Scholar]
  125. Tarrago L, Laugier E, Rey P. 125.  2009. Protein-repairing methionine sulfoxide reductases in photosynthetic organisms: gene organization, reduction mechanisms, and physiological roles. Mol. Plant. 2:202–17 [Google Scholar]
  126. Tavladoraki P, Cona A, Angelini R. 126.  2016. Copper-containing amine oxidases and FAD-dependent polyamine oxidases are key players in plant tissue differentiation and organ development. Front. Plant Sci. 7:824 [Google Scholar]
  127. Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue BPA. 127.  2015. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27:2095–118 [Google Scholar]
  128. Tian S, Wang X, Li P, Wang H, Ji H. 128.  et al. 2016. Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–50 [Google Scholar]
  129. Torres MA, Dangl JL, Jones JDG. 129.  2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. PNAS 99:517–22 [Google Scholar]
  130. Torres MA, Jones JDG, Dangl JL. 130.  2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet 37:1130–34 [Google Scholar]
  131. Umbach AL, Fiorani F, Siedow JN. 131.  2005. Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol 139:1806–20 [Google Scholar]
  132. Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J. 132.  2014. Specificity in ROS signaling and transcript signatures. Antioxid. Redox Signal. 21:1422–41 [Google Scholar]
  133. Vahisalu T, Puzõrjova I, Brosché M, Valk E, Lepiku M. 133.  et al. 2010. Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62:442–53 [Google Scholar]
  134. Vainonen JP, Kangasjärvi J. 134.  2014. Plant signalling in acute ozone exposure. Plant. Cell Environ. 38:240–52 [Google Scholar]
  135. Van Aken O, De Clercq I, Ivanova A, Law SR, Van Breusegem F. 135.  et al. 2016. Mitochondrial and chloroplast stress responses are modulated in distinct touch and chemical inhibition phases. Plant Physiol 171:2150–65 [Google Scholar]
  136. Van Aken O, Pogson BJ. 136.  2017. Convergence of mitochondrial and chloroplastic ANAC017/PAP-dependent retrograde signalling pathways and suppression of programmed cell death. Cell Death Differ 24:955–60 [Google Scholar]
  137. Vanderauwera S, Suzuki N, Miller G, van de Cotte B, Morsa S. 137.  et al. 2011. Extranuclear protection of chromosomal DNA from oxidative stress. PNAS 108:1711–16 [Google Scholar]
  138. Vestergaard CL, Flyvbjerg H, Møller IM. 138.  2012. Intracellular signaling by diffusion: Can waves of hydrogen peroxide transmit intracellular information in plant cells?. Front. Plant Sci. 3:295 [Google Scholar]
  139. Warren EAK, Netterfield TS, Sarkar S, Kemp ML, Payne CK. 139.  2015. Spatially-resolved intracellular sensing of hydrogen peroxide in living cells. Sci. Rep. 5:16929 [Google Scholar]
  140. Waszczak C, Akter S, Eeckhout D, Persiau G, Wahni K. 140.  et al. 2014. Sulfenome mining in Arabidopsis thaliana. PNAS 111:11545–50 [Google Scholar]
  141. Willems P, Mhamdi A, Simon S, Storme V, Kerchev PI. 141.  et al. 2016. The ROS wheel: refining ROS transcriptional footprints. Plant Physiol 171:1720–33 [Google Scholar]
  142. Woo HA, Yim SH, Shin DH, Kang D, Yu DY, Rhee SG. 142.  2010. Inactivation of peroxiredoxin I by phosphorylation allows localized H2O2 accumulation for cell signaling. Cell 140:517–28 [Google Scholar]
  143. Wood ZA, Poole LB, Karplus PA. 143.  2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650–53 [Google Scholar]
  144. Wrzaczek M, Brosché M, Kollist H, Kangasjärvi J. 144.  2009. Arabidopsis GRI is involved in the regulation of cell death induced by extracellular ROS. PNAS 106:5412–17 [Google Scholar]
  145. Wrzaczek M, Brosché M, Salojärvi J, Idänheimo N, Kangasjärvi S. 145.  et al. 2010. Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:95 [Google Scholar]
  146. Wrzaczek M, Vainonen JP, Stael S, Tsiatsiani L, Help-Rinta-Rahko H. 146.  et al. 2015. GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis. EMBO J 34:55–66 [Google Scholar]
  147. Xu E, Vaahtera L, Brosché M. 147.  2015. Roles of defense hormones in the regulation of ozone-induced changes in gene expression and cell death. Mol. Plant. 8:1776–94 [Google Scholar]
  148. Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S. 148.  2014. A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. Plant J 77:222–34 [Google Scholar]
  149. Yadeta KA, Elmore JM, Creer AY, Feng B, Franco JY. 149.  et al. 2017. A cysteine-rich protein kinase associates with a membrane immune complex and the cysteine residues are required for cell death. Plant Physiol 173:771–87 [Google Scholar]
  150. Yang T, Poovaiah BW. 150.  2002. Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. PNAS 99:4097–102 [Google Scholar]
  151. Yoda H.151.  2006. Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206 [Google Scholar]
  152. Yoda H, Yamaguchi Y, Sano H. 152.  2003. Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–81 [Google Scholar]
  153. Yuan H-M, Liu W-C, Lu Y-T. 153.  2017. CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses. Cell Host Microbe 21:143–55 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040322
Loading
/content/journals/10.1146/annurev-arplant-042817-040322
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error