In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants

Annual Review of Plant Biology

Volumn 62, Issue , 2011, Pages 273-297

  Swanson, Sarah J ^a   Choi, Won Gyu ^a   Chanoca, Alexandra ^a   Gilroy, Simon ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Arabidopsis; calcium; cameleon; fluorescence; FRET; GFP; green fluorescent protein; pH; ratio imaging; ROS

Indexed keywords

ARABIDOPSIS;

CALCIUM; FLUORESCENT DYE; HYDROGEN PEROXIDE; PHOTOPROTEIN; REACTIVE OXYGEN METABOLITE;

FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; METABOLISM; METHODOLOGY; MOLECULAR PROBE; OXIDATION REDUCTION REACTION; PH; PLANT; REVIEW;

CALCIUM; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR PROBES; OXIDATION-REDUCTION; PLANTS; REACTIVE OXYGEN SPECIES;

EID: 79955580424     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042110-103832     Document Type: Article

References (133)

1. Agati G, Matteini P, Goti A, Tattini M. 2007. Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol. 174:77-89. (Pubitemid 46333290)
2. Ahn JW, Verma R, Kim M, Lee JY, Kim YK, et al. 2006. Depletion of UDP-D-apiose/UDP-D-xylose synthases results in rhamnogalacturonan-II deficiency, cell wall thickening, and cell death in higher plants. J. Biol. Chem. 281:13708-16. (Pubitemid 43855286)
3. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, et al. 2001. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053-57. (Pubitemid 32612330)
4. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, et al. 2000. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338-42.
5. Allen GJ, Kuchitsu K, Chu SP, Murata Y, Schroeder JI. 1999. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. Plant Cell 11:1785-98.
6. Allen GJ, Murata Y, Chu SP, Nafisi M, Schroeder JI. 2002. Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell 14:1649-62. (Pubitemid 34817150)
7. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373-99. (Pubitemid 38940937)
8. Ashtamker C, Kiss V, Sagi M, Davydov O, Fluhr R. 2007. Diverse subcellular locations of cryptogeininduced reactive oxygen species production in tobacco Bright Yellow-2 cells. Plant Physiol. 143:1817-26. (Pubitemid 46849489)
9. Baek D, Jin Y, Jeong JC, Lee HJ, Moon H, et al. 2008. Suppression of reactive oxygen species by glyceraldehyde-3-phosphate dehydrogenase. Phytochemistry 69:333-38.
10. Baird GS, Zacharias DA, Tsien RY. 1999. Circular permutation and receptor insertion within green fluorescent proteins. Proc. Natl. Acad. Sci. USA 96:11241-46. (Pubitemid 29487365)
11. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, et al. 2006. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3:281-86.
12. Bi Y, Chen W, Zhang W, Zhou Q, Yun L, Xing D. 2009. Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmiuminduced cell death in Arabidopsis thaliana. Biol. Cell 101:629-43.
13. Bibikova TN, Jacob T, Dahse I, Gilroy S. 1998. Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 125:2925-34. (Pubitemid 28410216)
14. Bibikova TN, Zhigilei A, Gilroy S. 1997. Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495-505. (Pubitemid 28010177)
15. Bielski BHJ, Shiue GG, Bajuk S. 1980. Reduction of nitro blue tetrazolium by CO2- and O2-radicals. J. Phys. Chem. 84:830-33.
16. Bothwell JH, Brownlee C, Hetherington AM, Ng CK, Wheeler GL, McAinsh MR. 2006. Biolistic delivery of Ca2+ dyes into plant and algal cells. Plant J. 46:327-35. (Pubitemid 43773571)
17. Brauer D, Uknalis J, Triana R, Tu SI. 1996. Subcellular compartmentation of different lipophilic fluorescein derivatives in maize root epidermal cells. Protoplasma 192:70-79. (Pubitemid 126579737)
18. Bulgakov VP, Aminin DL, Shkryl YN, Gorpenchenko TY, Veremeichik GN, et al. 2008. Suppression of reactive oxygen species and enhanced stress tolerance in Rubia cordifolia cells expressing the rolC oncogene. Mol. Plant Microbe Interact. 21:1561-70.
19. Bush DS, Jones RL. 1987. Measurement of cytoplasmic calcium in aleurone protoplasts using Indo-1 and Fura-2. Cell Calcium 8:455-72.
20. Cardenas L, Martinez A, Sanchez F, Quinto C. 2008. Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J. 56:802-13.
21. Castro J, Aromataris EC,Rychkov GY, Barritt GJ. 2009.Asmall component of the endoplasmic reticulum is required for store-operated Ca2+ channel activation in liver cells: evidence from studies using TRPV1 and taurodeoxycholic acid. Biochem. J. 418:553-66.
22. Choi H, Kim S,Mukhopadhyay P, Cho S, Woo J, et al. 2001. Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103-13. (Pubitemid 32323920)
23. Coelho SM, Brownlee C, Bothwell JH. 2008. A tip-high, Ca2+-interdependent, reactive oxygen species gradient is associated with polarized growth in Fucus serratus zygotes. Planta 227:1037-46.
24. Costa A, Drago I, Behera S, Zottini M, Pizzo P, et al. 2010. H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2+-dependent scavenging system. Plant J. 62:760-72.
25. D'Autreaux B, Toledano MB. 2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8:813-24. (Pubitemid 47462134)
26. Dauphin A, Gerard J, Lapeyrie F, Legue V. 2007. Fungal hypaphorine reduces growth and induces cytosolic calcium increase in root hairs of Eucalyptus globulus. Protoplasma 231:83-88. (Pubitemid 47024991)
27. Dixit R, Cyr R. 2003. Cell damage and reactive oxygen species production induced by fluorescence microscopy: effect on mitosis and guidelines for non-invasive fluorescence microscopy. Plant J. 36:280-90. (Pubitemid 37293067)
28. Dixit R, Cyr R, Gilroy S. 2006. Using intrinsically fluorescent proteins for plant cell imaging. Plant J. 45:599-615. (Pubitemid 43373711)
29. Dodd AN, Kudla J, Sanders D. 2010. The language of calcium signaling. Annu. Rev. Plant Biol. 61:593-620.
30. Driever SM, Fryer MJ, Mullineaux PM, Baker NR. 2009. Imaging of reactive oxygen species in vivo. Methods Mol. Biol. 479:109-16.
31. Ehrhardt DW, Wais R, Long SR. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673-81.
32. Elliott DC, Petkoff HS. 1990. Measurement of cytoplasmic free calcium in plant protoplasts. Plant Sci. 67:125-31.
33. Elsliger M-A, WachterRM, Hanson GT,Kallio K, Remington SJ. 1999. Structural and spectral response of green fluorescent protein variants to changes in pH. Biochemistry 38:5296-301.
34. Fasano JM, Swanson SJ, Blancaflor EB, Dowd PE, Kao TH, Gilroy S. 2001. Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 13:907-21. (Pubitemid 32375909)
35. Feijó J, Sainhas J, Hackett G, Kunkel J, Hepler P. 1999. Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J. Cell Biol. 144:483-96. (Pubitemid 29234528)
36. Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, et al. 2006. Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J. Exp. Bot. 57:1725-34. (Pubitemid 43992222)
37. Floryszak-Wieczorek J, Arasimowicz M, Milczarek G, Jelen H, Jackowiak H. 2007. Only an early nitric oxide burst and the following wave of secondary nitric oxide generation enhanced effective defence responses of pelargonium to a necrotrophic pathogen. New Phytol. 175:718-30. (Pubitemid 47222632)
38. 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. (Pubitemid 36411398)
39. Fricker M, White N, Obermeyer G. 1997. pH gradients are not associated with tip growth in pollen tubes of Lilium longiflorum. J. Cell Sci. 110:1729-40. (Pubitemid 27352852)
40. FrommerWB, DavidsonMW,Campbell RE. 2009. Genetically encoded biosensors based on engineered fluorescent proteins. Chem. Soc. Rev. 38:2833-41.
41. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR. 2003. Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J. 33:691-705. (Pubitemid 36325912)
42. FryerMJ, Oxborough K, Mullineaux PM, Baker NR. 2002. Imaging of photo-oxidative stress responses in leaves. J. Exp. Bot. 53:1249-54. (Pubitemid 34544047)
43. Gao D, KnightMR, Trewavas AJ, Sattelmacher B, Plieth C. 2004. Self-reporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol. 134:898-908. (Pubitemid 38398238)
44. GaraschukO,Griesbeck O, Konnerth A. 2007. Troponin C-based biosensors: a new family of genetically encoded indicators for in vivo calcium imaging in the nervous system. Cell Calcium 42:351-61. (Pubitemid 47264000)
45. Gilroy S, Jones RL. 1992. Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc. Natl. Acad. Sci. USA 89:3591-95.
46. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. 2007. Hydrogen peroxide: A metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8:722-28. (Pubitemid 47312827)
47. Grignon C, Sentenac H. 1991. pH and ionic conditions in the apoplast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:103-28. (Pubitemid 21903927)
48. Grynkiewicz G, Poenie M, Tsien RY. 1985. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-50. (Pubitemid 15114340)
49. Heim N, Garaschuk O, Friedrich MW, Mank M, Milos RI, et al. 2007. Improved calcium imaging in transgenic mice expressing a troponin C-based biosensor. Nature Methods 4:127-29. (Pubitemid 46454679)
50. Henderson LM, Chappell JB. 1993. Dihydrorhodamine 123: A fluorescent probe for superoxide generation? Eur. J. Biochem. 217:973-80. (Pubitemid 23326880)
51. Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K. 2002. Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol. 43:1154-64. (Pubitemid 35337211)
52. Hideg E, Kos PB, Schreiber U. 2008. Imaging of NPQ and ROS formation in tobacco leaves: heat inactivation of the water-water cycle prevents down-regulation of PSII. Plant. Cell Physiol. 49:1879-86.
53. Hideg EE, OgawaK,Kalai T, HidegK. 2001. Singlet oxygen imaging in Arabidopsis thaliana leaves under photoinhibition by excess photosynthetically active radiation. Physiol. Plant. 112:10-14. (Pubitemid 32402492)
54. Hoffmann B, Kosegarten H. 1995. FITC-dextran formeasuring apoplast pHand apoplastic pHgradients between various cell types in sunflower leaves. Physiol. Plant. 95:327-35. (Pubitemid 3010114)
55. Holdaway-Clarke TL, Feijo JA, Hackett GR, Kunkel JG, Hepler PK. 1997. Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9:1999-2010. (Pubitemid 28174072)
56. Itoh RE,KurokawaK,Ohba Y,YoshizakiH,Mochizuki N, Matsuda M. 2002. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell Biol. 22:6582-91.
57. Iwano M, Entani T, Shiba H, Kakita M, Nagai T, et al. 2009. Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol. 150:1322-34.
58. Iwano M, Shiba H, Miwa T, Che FS, Takayama S, et al. 2004. Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol. 136:3562-71. (Pubitemid 41075795)
59. Jares-Erijman EA, Jovin TM. 2003. FRET imaging. Nat. Biotechnol. 21:1387-95.
60. Jekely G, Arendt D. 2007. Cellular resolution expression profiling using confocal detection ofNBT/BCIP precipitate by reflection microscopy. Biotechniques 42:751-55. (Pubitemid 47035983)
61. JiaWS, Davies WJ. 2007. Modification of leaf apoplastic pH in relation to stomatal sensitivity to rootsourced abscisic acid signals. Plant Physiol. 143:68-77. (Pubitemid 46133618)
62. Kalai T, Hideg E, Vass I, Hideg K. 1998. Double (fluorescent and spin) sensors for detection of reactive oxygen species in the thylakoid membrane. Free Radic. Biol. Med. 24:649-52. (Pubitemid 28150483)
63. Kawano T, Pinontoan R, Uozumi N, Miyake C, Asada K, et al. 2000. Aromatic monoamine-induced immediate oxidative burst leading to an increase in cytosolic Ca2+ concentration in tobacco suspension culture. Plant Cell Physiol. 41:1251-58. (Pubitemid 32003662)
64. KenworthyAK. 2001. Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24:289-96. (Pubitemid 32846434)
65. Kosuta S, Hazledine S, Sun J,MiwaH,Morris RJ, et al. 2008. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc. Natl. Acad. Sci. USA 105:9823-28. (Pubitemid 352031384)
66. Kurkdjian A, Guern J. 1989. Intracellular pH: measurement and importance in cell activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:271-303.
67. Lee Y, Bak G, Choi Y, Chuang WI, Cho HT. 2008. Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol. 147:624-35. (Pubitemid 352844310)
68. Leshem Y, Seri L, Levine A. 2007. Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J. 51:185-97. (Pubitemid 47030120)
69. Liu P, Li RL, Zhang L,Wang QL, Niehaus K, et al. 2009. Lipid microdomain polarization is required forNADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J. 60:303-13.
70. Lovy-Wheeler A, Kunkel JG, Allwood EG, Hussey PJ, Hepler PK. 2006. Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell 18:2182-93. (Pubitemid 44484719)
71. Maxwell DP, Wang Y, McIntosh L. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96:8271-76. (Pubitemid 29328444)
72. McAinsh MR, Pittman JK. 2009. Shaping the calcium signature. New Phytol. 181:275-94. (Pubitemid 352840372)
73. Messerli M, Robinson KR. 1997. Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J. Cell Sci. 110:1269-78. (Pubitemid 27273697)
74. Messerli MA, Creton R, Jaffe LF, Robinson KR. 2000. Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev. Biol. 222:84-98. (Pubitemid 30387731)
75. Michard E, Alves F, Feijo JA. 2009. The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm. Int. J. Dev. Biol. 53:1609-22.
76. MiesenbockG,De Angelis DA, Rothman JE. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-95. (Pubitemid 28325974)
77. Miwa H, Sun J,Oldroyd GE,Downie JA. 2006. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J. 48:883-94. (Pubitemid 44924349)
78. Miwa H, Sun J, Oldroyd GE, Downie JA. 2006. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol. Plant Microbe Interact. 19:914-23. (Pubitemid 44098623)
79. Miyawaki A, Griesbeck O, Heim R, Tsien RY. 1999. Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc. Natl. Acad. Sci. USA 96:2135-40. (Pubitemid 29117880)
80. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, et al. 1997. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882-87. (Pubitemid 27377061)
81. Moller IM, Jensen PE,Hansson A. 2007. Oxidativemodifications to cellular components in plants. Annu. Rev. Plant Biol. 58:459-81.
82. 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. Proc. Natl. Acad. Sci. USA 104:20996-1001.
83. 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.
84. Monshausen GB, Messerli MA, Gilroy S. 2008. Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 147:1690-98. (Pubitemid 352844213)
85. Morkunas I, BednarskiW. 2008. Fusarium oxysporum-induced oxidative stress and antioxidative defenses of yellow lupine embryo axes with different sugar levels. J. Plant Physiol. 165:262-77.
86. Moseyko N, Feldman LJ. 2001. Expression of pH-sensitive green fluorescent protein in Arabidopsis thaliana. Plant Cell Environ. 24:557-63. (Pubitemid 32442609)
87. Muhling KH, Lauchli A. 2000. Light-induced pH and K+ changes in the apoplast of intact leaves. Planta 212:9-15. (Pubitemid 32139890)
88. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20:87-90. (Pubitemid 34044921)
89. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A. 2004. Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. USA 101:10554-59. (Pubitemid 38955780)
90. Okumoto S, Takanaga H, FrommerWB. 2008. Quantitative imaging for discovery and assembly of the metabo-regulome. New Phytol. 180:271-95.
91. Orozco-Cardenas M, Ryan CA. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96:6553-57. (Pubitemid 29256704)
92. Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, et al. 2005. Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 41:831-44. (Pubitemid 40398713)
93. Palmer AE, Giacomello M, Kortemme T, Hires SA, Lev-Ram V, et al. 2006. Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem. Biol. 13:521-30. (Pubitemid 43729506)
94. Palmer AE, Tsien RY. 2006. Measuring calcium signaling using genetically targetable fluorescent indicators. Nat. Protoc. 1:1057-65.
95. Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, et al. 1994. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6:1815-28. (Pubitemid 24986956)
96. Pitann B, Kranz T, Muhling KH. 2009. The apoplastic pH and its significance in adaptation to salinity in maize (Zea mays L.): comparison of fluorescence microscopy and pH-sensitive microelectrodes. Plant Sci. 176:497-504.
97. Probes M. 2010. The Handbook. Carlsbad, NM: Invitrogen.
98. Rao MV, Davis KR. 1999. Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J. 17:603-14.
99. Rayle DL, Cleland R. 1970. Enhancement of wall loosening and elongation by acid solutions. Plant Physiol. 46:250-53.
100. Rhee SG, Chang TS, Jeong W, Kang D. 2010. Methods for detection and measurement of hydrogen peroxide inside and outside of cells. Mol. Cells 29:539-49.
101. Richter GL, Monshausen GB, Krol A, Gilroy S. 2009. Mechanical stimuli modulate lateral root organogenesis. Plant Physiol. 151:1855-66.
102. Rincon-ZacharyM, Teaster ND, Sparks JA, Valster AH, Motes CM, Blancaflor EB. 2010. Fluorescence resonance energy transfer-sensitized emission of yellow cameleon 3.60 reveals root zone-specific calcium signatures in Arabidopsis in response to aluminum and other trivalent cations. Plant Physiol. 152:1442-58.
103. Rodriguez AA, Grunberg KA, Taleisnik EL. 2002. Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiol. 129:1627-32. (Pubitemid 34923226)
104. Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, et al. 2009. Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150:229-43.
105. Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gomez M, et al. 2006. Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ. 29:1532-44. (Pubitemid 44356590)
106. Romano LA, Jacob T, Gilroy S, Assmann SM. 2000. Increases in cytosolic Ca2+ are not required for abscisic acid-inhibition of inward K+ currents in guard cells of Vicia faba L. Planta 211:209-17. (Pubitemid 30597432)
107. Scanlon M, Williams DA, Fay FS. 1987. A Ca2+-insensitive form of Fura-2 associated with polymorphonuclear leukocytes-assessment and accurate Ca2+ measurement. J. Biol. Chem. 262:6308-12. (Pubitemid 17103045)
108. Schopfer P, Plachy C, Frahry G. 2001. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol. 125:1591-602. (Pubitemid 32375744)
109. Schulte A, Lorenzen I, Bottcher M, Plieth C. 2006. A novel fluorescent pH probe for expression in plants. Plant Methods 2:7.
110. Shin R, Schachtman DP. 2004. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc. Natl. Acad. Sci. USA 101:8827-32. (Pubitemid 38745856)
111. Shkryl YN, Veremeichik GN, Bulgakov VP, Gorpenchenko TY, Aminin DL, Zhuravlev YN. 2010. Decreased ROS level and activation of antioxidant gene expression in Agrobacterium rhizogenes pRiA4- transformed calli of Rubia cordifolia. Planta 232:1023-32.
112. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, Barker DG. 2009. A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol. 151:1197-206.
113. Snapp EL. 2009. Fluorescent proteins: a cell biologist's user guide. Trends Cell Biol. 19:649-55.
114. Sobreira C, Davidson M, King MP, Miranda AF. 1996. Dihydrorhodamine 123 identifies impaired mitochondrial respiratory chain function in cultured cells harboring mitochondrial DNA mutations. J. Histochem. Cytochem. 44:571-79. (Pubitemid 26177348)
115. Sun J,Miwa H, Downie JA, Oldroyd GE. 2007. Mastoparan activates calcium spiking analogous to Nod factor-induced responses in Medicago truncatula root hair cells. Plant Physiol. 144:695-702. (Pubitemid 46944736)
116. Swanson S, Gilroy S. 2010. ROS in plant development. Physiol. Plant. 138:384-92.
117. Swanson SJ, Bethke PC, Jones RL. 1998. Barley aleurone cells contain two types of vacuoles. Characterization of lytic organelles by use of fluorescent probes. Plant Cell 10:685-98. (Pubitemid 28542178)
118. Swanson SJ, Jones RL. 1996. Gibberellic acid induces vacuolar acidification in barley aleurone. Plant Cell 8:2211-21. (Pubitemid 126446958)
119. Taylor DP, Slattery J, Leopold AC. 1996. Apoplastic pH in corn root gravitropism: a laser scanning confocal microscopy measurement. Physiol. Plant. 97:35-38. (Pubitemid 126616874)
120. Thomas D, Tovey SC,CollinsTJ, BootmanMD, Berridge MJ,LippP. 2000.Acomparison of fluorescent Ca2+ indicator properties and their use in measuring elementary and global Ca2+ signals. Cell Calcium 28:213-23.
121. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB. 1997. Subcellular localisation of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-94. (Pubitemid 27307236)
122. van Munster EB, Gadella TW. 2005. Fluorescence lifetime imaging microscopy (FLIM). Adv. Biochem. Eng. Biotechnol. 95:143-75. (Pubitemid 44641522)
123. Wallrabe H, Periasamy A. 2005. Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol. 16:19-27. (Pubitemid 40249755)
124. Watahiki MK, Trewavas AJ, Parton RM. 2004. Fluctuations in the pollen tube tip-focused calcium gradient are not reflected in nuclear calcium level: a comparative analysis using recombinant yellow cameleon calcium reporter. Sex. Plant Reprod. 17:125-30. (Pubitemid 39385100)
125. Wen F, Xing D, Zhang L. 2008. Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis. J. Exp. Bot. 59:2891-901. (Pubitemid 351957506)
126. Wymer CL, Bibikova TN, Gilroy S. 1997. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J. 12:427-39. (Pubitemid 27389630)
127. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H. 2002. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol. 128:63-72. (Pubitemid 34115310)
128. Yu Q, Kuo J, Tang C. 2001. Using confocal laser scanning microscopy to measure apoplastic pHchange in roots of Lupinus angustifolius L. in response to high pH. Ann. Bot. 87:47-52. (Pubitemid 32100585)
129. Zhang WH, Rengel Z, Kuo J. 1998. Determination of intracellular Ca2+ in cells of intact wheat roots: loading of acetoxymethyl ester of Fluo-3 under low temperature. Plant J. 15:147-51.
130. Zheng M, Aslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718-21. (Pubitemid 28164467)
131. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. 1997. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem. 253:162-68. (Pubitemid 27508167)
132. Zhu J, Alvarez S, Marsh EL, Lenoble ME, Cho IJ, et al. 2007. Cell wall proteome in the maize primary root elongation zone. II. Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiol. 145:1533-48. (Pubitemid 350276773)
133. Zielonka J, Vasquez-Vivar J, Kalyanaraman B. 2008. Detection of 2-hydroxyethidium in cellular systems: a unique marker product of superoxide and hydroethidine. Nat. Protoc. 3:8-21