ROS, calcium, and electric signals: Key mediators of rapid systemic signaling in plants

Plant Physiology

Volumn 171, Issue 3, 2016, Pages 1606-1615

  Gilroy, Simon ^a   Białasek, Maciej ^b   Suzuki, Nobuhiro ^c   Górecka, Magdalena ^b   Devireddy, Amith R ^d   Karpiński, Stanisław ^b   Mittler, Ron ^d  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^c SOPHIA UNIVERSITY   (Japan)

^d UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM; CALCIUM CHANNEL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESPIRATORY BURST OXIDASE HOMOLOG D, ARABIDOPSIS;

CALCIUM SIGNALING; CELL COMMUNICATION; ELECTRICITY; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; SIGNAL TRANSDUCTION;

ARABIDOPSIS PROTEINS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL COMMUNICATION; ELECTRICITY; NADPH OXIDASES; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84977536735     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00434     Document Type: Article

References (101)

1. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, et al (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289: 2338-2342
2. Beyhl D, Hörtensteiner S, Martinoia E, Farmer EE, Fromm J, Marten I, Hedrich R (2009) The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J 58: 715-723
3. Bonaventure G, Gfeller A, Proebsting WM, Hörtensteiner S, Chételat A, Martinoia E, Farmer EE (2007) A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J 49: 889-898
4. Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, et al (2016) The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Curr Biol 26: 286-295
5. 2+ waves are associated with rapid, long-distance root-toshoot signaling in plants. Proc Natl Acad Sci USA 111: 6497-6502
6. Ciszak K, Kulasek M, Barczak A, Grzelak J, Maćkowski S, Karpiński S (2015) PsbS is required for systemic acquired acclimation and postexcess-light-stress optimization of chlorophyll fluorescence decay times in Arabidopsis. Plant Signal Behav 10: e982018
7. Considine MJ, Sandalio LM, Foyer CH (2015) Unravelling how plants benefit from ROS and NO reactions, while resisting oxidative stress. Ann Bot (Lond) 116: 469-473
8. Dadacz-Narloch B, Beyhl D, Larisch C, López-Sanjurjo EJ, Reski R, Kuchitsu K, Müller TD, Becker D, Schönknecht G, Hedrich R (2011) A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. Plant Cell 23: 2696-2707
9. Davies E, Stankovic B (2006) Electrical signals, the cytoskeleton, and gene expression: a hypothesis on the coherence of the cellular responses to environmental insult. In F Baluška, S Mancuso, D Volkmann, eds, Communication in Plants. Springer, Berlin, pp 309-320
10. de Pinto MC, Locato V, Sgobba A, Romero-Puertas MdelC, Gadaleta C, Delledonne M, De Gara L (2013) S-Nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163: 1766-1775
11. Del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66: 2827-2837
12. 2+ channels. Plant J 49: 377-386
13. Dempsey DA, Klessig DF (2012) SOS-too many signals for systemic acquired resistance? Trends Plant Sci 17: 538-545
14. Dietz KJ (2015) Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J Exp Bot 66: 2401-2414
15. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61: 593-620
16. Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6: 559-569
17. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA 110: 8744-8749
18. Dziubińska H, Trębacz K, Zawadzki T (2001) Transmission route for action potentials and variation potentials in Helianthus annuus L. J Plant Physiol 158: 1167-1172
19. Farmer EE, Gasperini D, Acosta IF (2014) The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol 204: 282-288
20. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446
21. Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18: 2087-2090
22. Fromm J, Hajirezaei MR, Becker VK, Lautner S (2013) Electrical signaling along the phloem and its physiological responses in the maize leaf. Front Plant Sci 4: 239
23. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30: 249-257
24. 2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba. Plant Cell 21: 2118-2132
25. Furch AC, Zimmermann MR, Will T, Hafke JB, van Bel AJ (2010) Remotecontrolled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61: 3697-3708
26. Gallé A, Lautner S, Flexas J, Ribas-Carbo M, Hanson D, Roesgen J, Fromm J (2013) Photosynthetic responses of soybean (Glycine max L.) to heat-induced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO(2). Plant Cell Environ 36: 542-552
27. 2. J Biol Chem 285: 29286-29294
28. Gawroński P, Górecka M, Bederska M, Rusaczonek A, Ślesak I, Kruk J, Karpiński S (2013) Isochorismate synthase 1 is required for thylakoid organization, optimal plastoquinone redox status, and state transitions in Arabidopsis thaliana. J Exp Bot 64: 3669-3679
29. Gawroński P,Witoń D, Vashutina K, BederskaM, Betliński B, Rusaczonek A, Karpiński S (2014) Mitogen-activated protein kinase 4 is a salicylic acidindependent regulator of growth but not of photosynthesis in Arabidopsis. Mol Plant 7: 1151-1166
30. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19: 623-630
31. Glauser G, Dubugnon L, Mousavi SA, Rudaz S, Wolfender JL, Farmer EE (2009) Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J Biol Chem 284: 34506-34513
32. Guo J, Zeng W, Chen Q, Lee C, Chen L, Yang Y, Cang C, Ren D, Jiang Y (2016) Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature 531: 196-201
33. Gutla PV, Boccaccio A, De Angeli A, Gambale F, Carpaneto A (2012) Modulation of plant TPC channels by polyunsaturated fatty acids. J Exp Bot 63: 6187-6197
34. Hamilton ES, Schlegel AM, Haswell ES (2015) United in diversity: mechanosensitive ion channels in plants. Annu Rev Plant Biol 66: 113-137
35. Hedrich R, Marten I (2011) TPC1-SV channels gain shape. Mol Plant 4: 428-441
36. Hedrich R, Salvador-Recatalà V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends Plant Sci 21: 376-387
37. Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, Kang H (2012) Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res 125: 147-153
38. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59: 41-66
39. 2+ signaling. Plant Physiol 163: 459-470
40. Kachroo A, Robin GP (2013) Systemic signaling during plant defense. Curr Opin Plant Biol 16: 527-533
41. Karpiński 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
42. Karpiński S, Szechyńska-Hebda M, Wituszyńska W, Burdiak P (2013) Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ 36: 736-744
43. 2+) elevation is activated upon wounding and herbivory in Arabidopsis. New Phytol 207: 996-1004
44. 2+ and reactive oxygen species. Biochim Biophys Acta 1823: 398-405
45. Kintzer AF, Stroud RM (2016) Structure, inhibition and regulation of twopore channel TPC1 from Arabidopsis thaliana. Nature 531: 258-262
46. 2+ level to counteract effect of abscisic acid in seed germination. Plant Physiol 167: 1630-1642
47. 2 uptake in Mimosa pudica upon heat stimulation. Plant Cell Environ 37: 254-260
48. Latz A, Becker D, Hekman M, Müller T, Beyhl D, Marten I, Eing C, Fischer A, Dunkel M, Bertl A, et al (2007) TPK1, a Ca(2+)-regulated Arabidopsis vacuole two-pore K(+) channel is activated by 14-3-3 proteins. Plant J 52: 449-459
49. Lew R (1994) Regulation of electrical coupling between Arabidopsis root hairs. Planta 193: 67-73
50. Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, et al (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15: 329-338
51. Marten I, Deeken R, Hedrich R, Roelfsema MR (2010) Light-induced modification of plant plasma membrane ion transport. Plant Biol (Stuttg) (Suppl 1) 12: 64-79
52. Matsuo M, Johnson JM, Hieno A, Tokizawa M, Nomoto M, Tada Y, Godfrey R, Obokata J, Sherameti I, Yamamoto YY, et al (2015) High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 levels result in accumulation of reactive oxygen species in Arabidopsis thaliana shoots and roots. Mol Plant 8: 1253-1273
53. Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, Van Breusegem F, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot http://dx.doi.org/10.1093/jxb/erw080
54. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2: ra45
55. Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27: 64-70
56. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16: 300-309
57. Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A, Segonzac C, Malinovsky FG, Rathjen JP, MacLean D, Romeis T, et al (2014) The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16: 605-615
58. 2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21: 2341-2356
59. Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500: 422-426
60. Mühlenbock P, Szechyńska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20: 2339-2356; erratum
61. Mühlenbock P, Szechyńska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Plant Cell 20: 3480
62. Návarová H, Bernsdorff F, Döring AC, Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24: 5123-5141
63. Ordoñez NM, Marondedze C, Thomas L, Pasqualini S, Shabala L, Shabala S, Gehring C (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS Lett 588: 1008-1015
64. Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63: 2089-2103
65. Palmieri MC, Lindermayr C, Bauwe H, Steinhauser C, Durner J (2010) Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol 152: 1514-1528
66. Pavlovic A, Slováková L, Pandolfi C, Mancuso S (2011) On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). J Exp Bot 62: 1991-2000
67. Peiter E (2011) The plant vacuole: emitter and receiver of calcium signals. Cell Calcium 50: 120-128
68. Ping Z, Mimura T, Tazawa M (1990) Jumping transmission of action potential between separately placed internodal cells of Chora corallina. Plant Cell Physiol 31: 299-302
69. 2+ release during intracellular signaling. FEBS Lett 583: 921-926
70. 2+ signals induced by abiotic and biotic stresses. Plant J 53: 287-299
71. Rasul S, Dubreuil-Maurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S (2012) Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ 35: 1483-1499
72. 2-induced calcium signature in Arabidopsis thaliana roots. Plant J 77: 136-145
73. Salvador-Recatalà V (2016) New roles for the GLUTAMATE RECEPTORLIKE 3.3, 3.5, and 3.6 genes as on/off switches of wound-induced systemic electrical signals. Plant Signal Behav 11: e1161879
74. Salvador-Recatalà V, Tjallingii WF, Farmer EE (2014) Real-time, in vivo intracellular recordings of caterpillar-induced depolarization waves in sieve elements using aphid electrodes. New Phytol 203: 674-684
75. 2+-dependent activation in the plant twopore channel TPC1. Plant J 68: 424-432
76. Shah J, Zeier J (2013) Long-distance communication and signal amplification in systemic acquired resistance. Front Plant Sci 4: 30
77. Shih HW, Miller ND, Dai C, Spalding EP, Monshausen GB (2014) The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr Biol 24: 1887-1892
78. Singh SK, Chien CT, Chang IF (2016) The Arabidopsis glutamate receptorlike gene GLR3.6 controls root development by repressing the Kiprelated protein gene KRP4. J Exp Bot 67: 1853-1869
79. Stahlberg R, Cleland R, Van Volkenburgh E (2006) Slow wave potentials-a propagating electrical signal unique to higher plants. In F Baluška, S Mancuso, D Volkmann, eds, Communication in Plants. Springer, Berlin, pp 291-308
80. Steinhorst L, Kudla J (2014) Signaling in cells and organisms-calcium holds the line. Curr Opin Plant Biol 22: 14-21
81. Stephens NR, Qi Z, Spalding EP (2008) Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol 146: 529-538
82. Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo X, Shah J, Schlauch K, et al (2013) Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25: 3553-3569
83. Szechyńska-Hebda M, Kruk J, Górecka M, Karpińska B, Karpiński S (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 22: 2201-2218
84. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319: 1241-1244
85. 3 pathway in Arabidopsis. Science 315: 1423-1426
86. Toyota M, Gilroy S (2013) Gravitropism and mechanical signaling in plants. Am J Bot 100: 111-125
87. Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J (2014) Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal 21: 1422-1441
88. 2+ signals along the phloem pathway. J Exp Bot 65: 1761-1787
89. 2+) conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 159: 40-46
90. Vincill ED, Clarin AE, Molenda JN, Spalding EP (2013) Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis. Plant Cell 25: 1304-1313
91. Volkov AG, Foster JC, Ashby TA, Walker RK, Johnson JA, Markin VS (2010) Mimosa pudica: electrical and mechanical stimulation of plant movements. Plant Cell Environ 33: 163-173
92. Wang C, El-Shetehy M, Shine MB, Yu K, Navarre D, Wendehenne D, Kachroo A, Kachroo P (2014) Free radicals mediate systemic acquired resistance. Cell Reports 7: 348-355
93. + channels and calciuminduced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6: 669-683
94. Wendehenne D, Gao QM, Kachroo A, Kachroo P (2014) Free radicalmediated systemic immunity in plants. Curr Opin Plant Biol 20: 127-134
95. Wituszyńska W, Ślesak I, Vanderauwera S, Szechyńska-Hebda M, Kornaś A, Van Der Kelen K, Mühlenbock P, Karpińska B, Maćkowski S, Van Breusegem F, et al (2013) Lesion simulating disease1, enhanced disease susceptibility1, and phytoalexin deficient4 conditionally regulate cellular signaling homeostasis, photosynthesis, water use efficiency, and seed yield in Arabidopsis. Plant Physiol 161: 1795-1805
96. Xiong TC, Ronzier E, Sanchez F, Corratgé-Faillie C, Mazars C, Thibaud JB (2014) Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Front Plant Sci 5: 43
97. Yun BW, Feechan A, YinM, Saidi NB, Le Bihan T, YuM,Moore JW, Kang JG, Kwon E, Spoel SH, et al (2011) S-Nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264-268
98. 2+ increases vital for osmosensing in Arabidopsis. Nature 514: 367-371
99. Zaffagnini M, Bedhomme M, Lemaire SD, Trost P (2012) The emerging roles of protein glutathionylation in chloroplasts. Plant Sci 185-186: 86-96
100. Zhao DJ, Wang ZY, Huang L, Jia YP, Leng JQ (2014) Spatio-temporal mapping of variation potentials in leaves of Helianthus annuus L. seedlings in situ using multi-electrode array. Sci Rep 4: 5435
101. Zimmermann MR, Maischak H, Mithöfer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149: 1593-1600