Rapid, Long-Distance Electrical and Calcium Signaling in Plants

Annual Review of Plant Biology

Volumn 67, Issue , 2016, Pages 287-307

  Choi, Won Gyu ^a   Hilleary, Richard ^a   Swanson, Sarah J ^a   Kim, Su Hwa ^a   Gilroy, Simon ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Calcium; Electrical signaling; Reactive oxygen species; Systemic acquired acclimation; Systemic acquired resistance

Indexed keywords

CALCIUM; REACTIVE OXYGEN METABOLITE;

CALCIUM SIGNALING; ELECTRICITY; METABOLISM; PLANT; SIGNAL TRANSDUCTION;

CALCIUM; CALCIUM SIGNALING; ELECTRICITY; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84968777302     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-043015-112130     Document Type: Review

References (123)

1. Acosta IF, Farmer EE. 2010. Jasmonates. Arabidopsis Book 8:e0129
2. AlvarezME, Pennell RI,Meijer PJ, Ishikawa A,Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773-84
3. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA. 2006. Volatile signaling in plant-plant interactions: "talking trees" in the genomics era. Science 311:812-15
4. Bedard K, Krause KH. 2007. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:245-313
5. Beyhl D, Hörtensteiner S, Martinoia E, Farmer EE, Fromm J, et al. 2009. The fou2 mutation in the major vacuolar cation channel TPC1 confers tolerance to inhibitory luminal calcium. Plant J. 58:715-23
6. Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, et al. 2007. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282:1183-92
7. Bonaventure G, Gfeller A, ProebstingWM,Hörtensteiner S, Chételat A, et al. 2007. A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J. 49:889-98
8. Campbell AK, Trewavas AJ, Knight MR. 1996. Calcium imaging shows differential sensitivity to cooling and communication in luminous transgenic plants. Cell Calcium 19:211-18
9. Canton J, Grinstein S. 2014. Priming and activation of NADPH oxidases in plants and animals. Trends Immunol. 35:405-7
10. Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, et al. 2011. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43:421-27
11. Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, et al. 2008. Plastid 3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J. 54:106-17
12. Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, et al. 2012. An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 71:161-72
13. Chauvin A, Caldelari D, Wolfender JL, Farmer EE. 2013. Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol. 197:566-75
14. Choi WG, Swanson SJ, Gilroy S. 2012. High-resolution imaging of Ca2+, redox status, ROS and pH using GFP biosensors. Plant J. 70:118-28
15. Choi WG,ToyotaM, Kim SH,Hilleary R,Gilroy S. 2014. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. PNAS 111:6497-502
16. Christmann A, Grill E, Huang J. 2013. Hydraulic signals in long-distance signaling. Curr. Opin. Plant Biol. 16:293-300
17. Conrath U. 2011. Molecular aspects of defence priming. Trends Plant Sci. 16:524-31
18. Demidchik V, Shabala SN, Davies JM. 2007. Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J. 49:377-86
19. Dempsey DA, Klessig DF. 2012. SOS-too many signals for systemic acquired resistance Trends Plant Sci. 17:538-45
20. Dengler NC. 2006. The shoot apical meristem and development of vascular architecture. Can. J. Bot. 84:1660-71
21. Dodd AN, Kudla J, Sanders D. 2010. The language of calcium signaling. Annu. Rev. Plant Biol. 61:593-620
22. Drerup MM, Schlucking K, Hashimoto K, Manishankar P, Steinhorst L, et al. 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 6:559-69
23. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, et al. 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. PNAS 110:8744-49
24. Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U. 2008. Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem. J. 414:53-61
25. Farmer EE, Gasperini D, Acosta IF. 2014. The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol. 204:282-88
26. Favre P, Greppin H, Degli Agosti R. 2001. Repetitive action potentials induced in Arabidopsis thaliana leaves by wounding and potassium chloride application. Plant Physiol. Biochem. 39:961-69
27. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-46
28. Fromm J, Bauer T. 1994. Action potentials in maize sieve tubes change phloem translocation. J. Exp. Bot. 45:463-69
29. 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
30. Fromm J, Lautner S. 2007. Electrical signals and their physiological significance in plants. Plant Cell Environ. 30:249-57
31. Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, et al. 2007. Arabidopsis protein kinase PKS5 inhibits the plasma membraneH+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617-34
32. Fuglsang AT, Kristensen A, Cuin TA, Schulze WX, Persson J, et al. 2014. Receptor kinase-mediated control of primary active proton pumping at the plasma membrane. Plant J. 80:951-64
33. Furch AC, van Bel AJ, Fricker MD, Felle HH, Fuchs M, Hafke JB. 2009. Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba. Plant Cell 21:2118-32
34. Gil PM, Gurovich L, Schaffer B, Alcayaga J, Rey S, Iturriaga R. 2008. Root to leaf electrical signaling in avocado in response to light and soil water content. J. Plant Physiol. 165:1070-78
35. Gil PM, Saavedra J, Schaffer B, Navarro R, Fuentealba C, Minoletti F. 2014. Quantifying effects of irrigation and soil water content on electrical potentials in grapevines (Vitis vinifera) using multivariate statistical methods. Sci. Horticult. 173:71-78
36. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, et al. 2014. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci. 19:623-30
37. Glauser G, Grata E, Dubugnon L, Rudaz S, Farmer EE, Wolfender JL. 2008. Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. J. Biol. Chem. 283:16400-7
38. Grams TE, Koziolek C, Lautner S, Matyssek R, Fromm J. 2007. Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. Plant Cell Environ. 30:79-84
39. Grams TE, Lautner S, Felle HH, Matyssek R, Fromm J. 2009. Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant Cell Environ. 32:319-26
40. Hanson J, Smeekens S. 2009. Sugar perception and signaling-an update. Curr. Opin. Plant Biol. 12:562-67
41. Hedrich R, Becker D. 1994. Green circuits-the potential of plant specific ion channels. Plant Mol. Biol. 26:1637-50
42. Hedrich R, Marten I. 2011. TPC1-SV channels gain shape. Mol. Plant 4:428-41
43. Hlavackova V, Krchnak P, Naus J, Novak O, Spundova M, Strnad M. 2006. Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta 225:235-44
44. Horikawa K, Yamada Y, Matsuda T, Kobayashi K, Hashimoto M, et al. 2010. Spontaneous network activity visualized by ultrasensitive Ca2+ indicators, yellow Cameleon-Nano. Nat. Methods 7:729-32
45. Jaffe LF. 2010. Fast calcium waves. Cell Calcium 48:102-13
46. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT. 2009. Priming in systemic plant immunity. Science 324:89-91
47. KadotaY, Shirasu K, Zipfel C. 2015. Regulation of theNADPHoxidaseRBOHDduring plant immunity. Plant Cell Physiol. 56:1472-80
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 284:654-57
49. Katicheva L, Sukhov V, Akinchits E, Vodeneev V. 2014. Ionic nature of burn-induced variation potential in wheat leaves. Plant Cell Physiol. 55:1511-19
50. Kiep V, Vadassery J, Lattke J, Maass JP, Boland W, et al. 2015. Systemic cytosolic Ca2+ elevation is activated upon wounding and herbivory in Arabidopsis. New Phytol. 207:996-1004
51. Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, et al. 2012. Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim. Biophys. Acta 1823:398-405
52. Koo AJ, Gao X, Jones AD, Howe GA. 2009. A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J. 59:974-86
53. Lake JA, Quick WP, Beerling DJ, Woodward FI. 2001. Plant development: signals from mature to new leaves. Nature 411:154
54. Lang RD, Volkov AG. 2008. Solitary waves in soybean induced by localized thermal stress. Plant Signal. Behav. 3:224-28
55. Lautner S, Grams TE, Matyssek R, Fromm J. 2005. Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol. 138:2200-9
56. Li F, Wang J, Ma C, Zhao Y, Wang Y, et al. 2013. Glutamate receptor-like channel3.3 is involved in mediating glutathione-triggered cytosolic calcium transients, transcriptional changes, and innate immunity responses in Arabidopsis. Plant Physiol. 162:1497-509
57. Li L, Li M, Yu L, Zhou Z, LiangX, et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329-38
58. Lino B, Baizabal-Aguirre VM, Gonzalez de la Vara LE. 1998. The plasma-membraneH+-ATPase from beet root is inhibited by a calcium-dependent phosphorylation. Planta 204:352-59
59. Liu PP, von Dahl CC, Klessig DF. 2011. The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol. 157:2216-26
60. Lomax TL, Muday GK, Rubery PH. 1995. Auxin transport. In Plant Hormones: Physiology, Biochemistry and Molecular Biology, ed. PJ Davies, pp. 509-30. Dordrecht, Neth.: Kluwer Acad.
61. Luna E, Bruce TJ, Roberts MR, Flors V, Ton J. 2012. Next-generation systemic acquired resistance. Plant Physiol. 158:844-53
62. Maischak H, ZimmermannMR, Felle HH, BolandW,Mithofer A. 2010. Alamethicin-induced electrical long distance signaling in plants. Plant Signal. Behav. 5:988-90
63. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399-403
64. Manzoor H, Kelloniemi J, Chiltz A,Wendehenne D, Pugin A, et al. 2013. Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis. Plant J. 76:466-80
65. Matzke AJ, Matzke M. 2013. Membrane "potential-omics": toward voltage imaging at the cell population level in roots of living plants. Front. Plant Sci. 4:311
66. Metraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, et al. 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004-6
67. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, et al. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45
68. Monaghan J, Matschi S, Romeis T, Zipfel C. 2015. The calcium-dependent protein kinase CPK28 negatively regulates the BIK1-mediated PAMP-induced calcium burst. Plant Signal. Behav. 10:e1018497
69. Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A, et al. 2014. The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16:605-15
70. Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S. 2007. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. PNAS 104:20996-1001
71. Monshausen GB, Bibikova TN, Weisenseel MH,Gilroy S. 2009. Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21:2341-56
72. Monshausen GB, Gilroy S. 2009. Feeling green: mechanosensing in plants. Trends Cell Biol. 19:228-35
73. Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. GLUTAMATE RECEPTORLIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422-26
74. Mullendore DL, Windt CW, Van As H, Knoblauch M. 2010. Sieve tube geometry in relation to phloem flow. Plant Cell 22:579-93
75. Naqvi SM, Gordon SA. 1966. Auxin transport in Zea mays L. coleoptiles I. Influence of gravity on the transport of indoleacetic acid-2-14C. Plant Physiol. 41:1113-18
76. Navarova H, Bernsdorff F, Doring AC, Zeier J. 2012. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123-41
77. Notaguchi M, Okamoto S. 2015. Dynamics of long-distance signaling via plant vascular tissues. Front. Plant Sci. 6:161
78. Ookura T, Komatsu S, Kawamura Y, Kasamo K. 2005. A 55-kDa calcium dependent protein kinase phosphorylated Thr residues from the auto-regulatory domain of plasma membrane H+-ATPase in rice. Jpn. Agric. Res. Q. 39:99-104
79. Orozco-Cardenas M, Ryan CA. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. PNAS 96:6553-57
80. Oyarce P, Gurovich L. 2011. Evidence for the transmission of information through electric potentials in injured avocado trees. J. Plant Physiol. 168:103-8
81. Park SW, Kaimoyo E, Kumar D, Mosher S, KlessigDF. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113-16
82. Pei ZM, Murata Y, Benning G, Thomine S, Kl üsener B, et al. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731-34
83. Peiter E. 2011. The plant vacuole: emitter and receiver of calcium signals. Cell Calcium 50:120-28
84. Peiter E, Maathuis FJ,Mills LN, Knight H, Pelloux J, et al. 2005. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404-8
85. Petrasek J, Friml J. 2009. Auxin transport routes in plant development. Development 136:2675-88
86. Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H, et al. 2013. Arabidopsis phospholipase Dis involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol. 163:896-906
87. Poltronieri P, Santino A. 2012. Non-coding RNAs in intercellular and systemic signaling. Front. Plant Sci. 3:141
88. Pottosin I,Wherrett T, Shabala S. 2009. SV channels dominate the vacuolar Ca2+ release during intracellular signaling. FEBS Lett. 583:921-26
89. Qi Z, Stephens NR, Spalding EP. 2006. Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol. 142:963-71
90. Rentel MC, Knight MR. 2004. Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135:1471-79
91. Rutschmann F, Stalder U, Piotrowski M, Oecking C, Schaller A. 2002. LeCPK1, a calcium-dependent protein kinase from tomato. Plasma membrane targeting and biochemical characterization. Plant Physiol. 129:156-68
92. SaitoK,HatsugaiN,HorikawaK,KobayashiK,Matsu-Ura T, et al. 2010. Auto-luminescent geneticallyencoded ratiometric indicator for real-time Ca2+ imaging at the single cell level. PLOS ONE 5:e9935
93. Salvador-Recatala 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. 203:674-84
94. Sato EM, Hijazi H, Bennett MJ, Vissenberg K, Swarup R. 2015. New insights into root gravitropic signalling. J. Exp. Bot. 66:2155-65
95. Shah J, Zeier J. 2013. Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 4:30
96. Shrestha R, G? omez-Ariza J, Brambilla V, Fornara F. 2014. Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals. Ann. Bot. 114:1445-58
97. Speth C, Jaspert N, Marcon C, Oecking C. 2010. Regulation of the plant plasma membraneH+-ATPase by its C-terminal domain:What do we know for sure Eur. J. Cell Biol. 89:145-51
98. Stahlberg R, Cosgrove DJ. 1997. The propagation of slow wave potentials in pea epicotyls. Plant Physiol. 113:209-17
99. Stahlberg R, Stephens NR, Cleland RE, Van Volkenburgh E. 2006. Shade-induced action potentials in Helianthus annuus L. originate primarily from the epicotyl. Plant Signal. Behav. 1:15-22
100. Stankovíc B, Davies E. 1996. Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett. 390:275-79
101. 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. 146:529-38
102. Stetson DS, Albers JW, Silverstein BA, Wolfe RA. 1992. Effects of age, sex, and anthropometric factors on nerve conduction measures. Muscle Nerve 15:1095-104
103. Sukhov V, Sherstneva O, Surova L, Katicheva L, Vodeneev V. 2014. Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant Cell Environ. 37:2532-41
104. Suzuki N, MillerG, Salazar C, Mondal HA, Shulaev E, et al. 2013. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25:3553-69
105. 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 319:1241-44
106. Tang RH, Han S,Zheng H, CookCW,ChoiCS, et al. 2007. Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315:1423-26
107. Thomas PW, Woodward FI, Quick WP. 2004. Systemic irradiance signalling in tobacco. New Phytol. 161:193-98
108. Traw MB, Kniskern JM, Bergelson J. 2007. SAR increases fitness of Arabidopsis thaliana in the presence of natural bacterial pathogens. Evolution 61:2444-49
109. Tsang EW, Bowler C, Herouart D, Van Camp W, Villarroel R, et al. 1991. Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3:783-92
110. Tucker EB, Lee M, Alli S, Sookhdeo V, Wada M, et al. 2005. UV-A induces two calcium waves in Physcomitrella patens. Plant Cell Physiol. 46:1226-36
111. Uraji M, Katagiri T, Okuma E, Ye W, Hossain MA, et al. 2012. Cooperative function of PLD and PLD1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 159:450-60
112. Vernooij B, Friedrich L, Morse A, Reist R, Kolditz-Jawhar R, et al. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959-65
113. Vincill ED, Bieck AM, Spalding EP. 2012. Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol. 159:40-46
114. Vincill ED, Clarin AE, Molenda JN, Spalding EP. 2013. Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis. Plant Cell 25:1304-13
115. Ward JM, Schroeder JI. 1994. Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6:669-83
116. WildermuthMC,Dewdney J,WuG, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-65
117. Windt CW, Vergeldt FJ, de Jager PA, Van As H. 2006. MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ. 29:1715-29
118. XiongTC, RonzierE, Sanchez F, Corratge-Faillie C, MazarsC,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
119. Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, et al. 2006. Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol. 140:558-79
120. Zhang W, Jeon BW, Assmann SM. 2011. Heterotrimeric G-protein regulation of ROS signalling and calcium currents in Arabidopsis guard cells. J. Exp. Bot. 62:2371-79
121. Zhang Y, Zhu H, ZhangQ, LiM, Yan M, et al. 2009. PhospholipaseD1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357-77
122. Zhao J, Devaiah SP,Wang C, LiM,Welti R, Wang X. 2013. Arabidopsis phospholipaseD1modulates defense responses to bacterial and fungal pathogens. New Phytol. 199:228-40
123. Zimmermann MR, Maischak H, Mithofer A, Boland W, Felle HH. 2009. System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol. 149:1593-600