Smaller, faster, brighter: Advances in optical imaging of living plant cells

Annual Review of Plant Biology

Volumn 64, Issue , 2013, Pages 351-375

  Shaw, Sidney L ^a   Ehrhardt, David W ^b  

^a INDIANA UNIVERSITY   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

Author keywords

Detection; Fluorescence; Microscopy; Resolution; Sensor

Indexed keywords

PHOTOPROTEIN;

CHEMISTRY; CONFOCAL MICROSCOPY; EQUIPMENT; FLUORESCENCE IMAGING; METHODOLOGY; PHYSIOLOGY; PLANT CELL; REVIEW;

LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; OPTICAL IMAGING; PLANT CELLS;

EID: 84877641397     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042110-103843     Document Type: Review

References (160)

1. Ai HW, Henderson JN, Remington SJ, Campbell RE. 2006. Directed evolution of a monomeric bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem. J. 400:531-40
2. Anderson CT,Carroll A, Akhmetova L, Somerville C. 2010. Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol. 152:787-96
3. Anderson CT, Wallace IS, Somerville CR. 2012. Metabolic click-labeling with a fucose analog reveals pectin delivery, architecture, and dynamics in Arabidopsis cell walls. Proc.Natl. Acad. Sci. USA109:1329-34
4. Augustine RC, Pattavina KA, Tuzel E, Vidali L, Bezanilla M. 2011. Actin interacting protein1 and actin depolymerizing factor drive rapid actin dynamics in Physcomitrella patens. Plant Cell 23:3696-710
5. Axelrod D, Burghardt TP, Thompson NL. 1984. Total internal reflection fluorescence. Annu. Rev. Biophys. Bioeng. 13:247-68
6. BadieirostamiM, Lew MD, ThompsonMA, MoernerWE. 2010. Three-dimensional localization precision of the double-helix point spread function versus astigmatism and biplane. Appl. Phys. Lett. 97:161103
7. Barondeau DP, Kassmann CJ, Tainer JA, Getzoff ED. 2002. Structural chemistry of a green fluorescent protein Zn biosensor. J. Am. Chem. Soc. 124:3522-24
8. 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
9. BerendzenKW,Bohmer M, WallmerothN, Peter S, VesicM, et al. 2012. Screening for in planta proteinprotein interactions combining bimolecular fluorescence complementation with flow cytometry. Plant Methods 8:25
10. Berg J, Hung YP, Yellen G. 2009. A genetically encoded fluorescent reporter of ATP:ADP ratio. Nat. Methods 6:161-66
11. Bermejo C, Ewald J, Lanquar V, Jones A, Frommer WB. 2011. In vivo biochemistry: quantifying ion and metabolite levels in individual cells or cultures of yeast. Biochem. J. 438:1-10
12. Bermejo C,Haerizadeh F, Takanaga H, ChermakD, FrommerWB. 2010. Dynamic analysis of cytosolic glucose and ATP levels in yeast using optical sensors. Biochem. J. 432:399-406
13. BermejoC,Haerizadeh F, Takanaga H, ChermakD, Frommer WB. 2011. Optical sensors for measuring dynamic changes in steady state levels of cytosolic glucose in yeast. Nat. Protoc. 6:1806-17
14. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-45
15. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R. 2005. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl. Acad. Sci. USA 102:3135-40
16. Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, et al. 2010. Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 22:1264-80
17. Bove J, Vaillancourt B, Kroeger J, Hepler PK,Wiseman PW, Geitmann A. 2008. Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiol. 147:1646-58
18. Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser MT, Persson S. 2012. POM-POM2/ CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24:163-77
19. Brunoud G, Wells DM,OlivaM, Larrieu A, Mirabet V, et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482:103-6
20. Busch W, Moore BT, Martsberger B, Mace DL, Twigg RW, et al. 2012. A microfluidic device and computational platform for high-throughput live imaging of gene expression. Nat. Methods 9:1101-6
21. Caesar K, Elgass K, Chen Z, Huppenberger P, Witthoft J, et al. 2011. A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. Plant J. 66:528-40
22. Cella Zanacchi F, Lavagnino Z, Perrone Donnorso M, Del Bue A, Furia L, et al. 2011. Live-cell 3D super-resolution imaging in thick biological samples. Nat. Methods 8:1047-49
23. Chapman S, Faulkner C, Kaiserli E, Garcia-Mata C, Savenkov EI, et al. 2008. The photoreversible fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection. Proc. Natl. Acad. Sci. USA 105:20038-43
24. Cheezum MK, Walker WF, Guilford WH. 2001. Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys. J. 81:2378-88
25. Cole NB, Donaldson JG. 2012. Releasable SNAP-tag probes for studying endocytosis and recycling. ACS Chem. Biol. 7:464-69
26. Dalgarno PA, Dalgarno HI, Putoud A, Lambert R, Paterson L, et al. 2010. Multiplane imaging and three dimensional nanoscale particle tracking in biological microscopy. Opt. Express 18:877-84
27. DavidsonMW, Campbell RE. 2009. Engineered fluorescent proteins: innovations and applications. Nat. Methods 6:713-17
28. Day RN, Davidson MW. 2009. The fluorescent protein palette: tools for cellular imaging. Chem. Soc. Rev. 38:2887-921
29. Deisseroth K. 2011. Optogenetics. Nat. Methods 8:26-29
30. Denk W, Strickler JH, Webb WW. 1990. Two-photon laser scanning fluorescence microscopy. Science 248:73-76
31. Ding SY, Xu Q, Ali MK, Baker JO, Bayer EA, et al. 2006. Versatile derivatives of carbohydrate-binding modules for imaging of complex carbohydrates approaching the molecular level of resolution. BioTechniques 41:435-43
32. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY. 2004. Imaging dynamic redox changes inmammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279:22284-93
33. Dutta D, Williamson C, Cole N, Donaldson J. 2012. Pitstop 2 is a potent inhibitor of clathrinindependent endocytosis. PLoS ONE 7:e45799
34. Ehrhardt DW, FrommerWB. 2012. New technologies for 21st century plant science. Plant Cell 24:374-94
35. Eli P, Chakrabartty A. 2006. Variants of DsRed fluorescent protein: development of a copper sensor. Protein Sci. 15:2442-47
36. Estevez JM, Somerville C. 2006. FlAsH-based live-cell fluorescent imaging of synthetic peptides expressed in Arabidopsis and tobacco. BioTechniques 41:569-74
37. Feij ́o JA, Moreno N. 2004. Imaging plant cells by two-photon excitation. Protoplasma 223:1-32
38. Fitzgibbon J, Bell K, King E, Oparka K. 2010. Superresolution imaging of plasmodesmata using threedimensional structured illumination microscopy. Plant Physiol. 153:1453-63
39. Forster T. 1948. Intermolecular energy migration and fluorescence. Ann. Phys. 2:55-75
40. Fricker M, Runions J, Moore I. 2006. Quantitative fluorescence microscopy: from art to science. Annu. Rev. Plant Biol. 57:79-107
41. FrommerWB, DavidsonMW,Campbell RE. 2009. Genetically encoded biosensors based on engineered fluorescent proteins. Chem. Soc. Rev. 38:2833-41
42. Gautier A, Juillerat A, Heinis C, Correa IR Jr, Kindermann M, et al. 2008. An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15:128-36
43. Grashoff C, Hoffman BD, BrennerMD, Zhou R, ParsonsM, et al. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263-66
44. Green PB, Chapman GB. 1955. On the development and structure of the cell wall in Nitella. Am. J. Bot. 42:685-93
45. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY. 2001. Reducing the environmental sensitivity of yellow fluorescent protein: mechanism and applications. J. Biol. Chem. 276:29188-94
46. Griffin BA, Adams SR, Jones J, Tsien RY. 2000. Fluorescent labeling of recombinant proteins in living cells with FlAsH. Methods Enzymol. 327:565-78
47. Grossmann G, Guo WJ, Ehrhardt DW, Frommer WB, Sit VS, Quake SR. 2011. The RootChip: an integrated microfluidic chip for plant science. Plant Cell 23:4234-40
48. Grossmann G, Meier M, Cartwright HN, Sosso D, Quake SR, et al. 2012. Time-lapse fluorescence imaging ofArabidopsis root growth with rapidmanipulation of the root environment using theRootChip. J. Vis. Exp. 65:e4290
49. Gustafsson MG. 2005. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. Proc. Natl. Acad. Sci. USA 102:13081-86
50. GustafssonMG, Shao L,Carlton PM,WangCJ, Golubovskaya IN, et al. 2008. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94:4957-70
51. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AMC, Ehrhardt DW. 2009. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11:797-806
52. Halet G. 2005. Imaging phosphoinositide dynamics using GFP-tagged protein domains. Biol. Cell 97:501-18
53. Hamamura Y, Saito C, Awai C, Kurihara D, Miyawaki A, et al. 2011. Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr. Biol. 21:497-502
54. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. 2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334:1401-4
55. Heintzmann R, Jovin TM, Cremer C. 2002. Saturated patterned excitation microscopy - a concept for optical resolution improvement. J. Opt. Soc. Am. A 19:1599-609
56. HellSW,Wichmann J. 1994. Breaking the diffraction resolution limit by stimulated emission: stimulatedemission-depletion fluorescence microscopy. Opt. Lett. 19:780-82
57. Henriques R, Lelek M, Fornasiero EF, Valtorta F, Zimmer C, et al. 2010. 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat. Methods 7:339-40
58. Hess ST, Gould TJ, Gudheti MV, Maas SA, Mills KD, Zimmerberg J. 2007. Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc. Natl. Acad. Sci. USA 104:17370-75
59. Hink MA, deVries SC, Visser AJ. 2011. Fluorescence fluctuation analysis of receptor kinase dimerization. Methods Mol. Biol. 779:199-215
60. Hink MA, Shah K, Russinova E, de Vries SC, Visser AJ. 2008. Fluorescence fluctuation analysis of Arabidopsis thaliana somatic embryogenesis receptor-like kinase and brassinosteroid insensitive 1 receptor oligomerization. Biophys. J. 94:1052-62
61. Hooke R. 1665. Micrographia; or, Some Physiological Descriptions of Minute Bodies Made by Magnifying Glasses. London: J. Martin and J. Allestry
62. Immink RG, Gadella TW Jr, Ferrario S, Busscher M, Angenent GC. 2002. Analysis of MADS box protein-protein interactions in living plant cells. Proc. Natl. Acad. Sci. USA 99:2416-21
63. Jares-Erijman EA, Jovin TM. 2006. Imaging molecular interactions in living cells by FRET microscopy. Curr. Opin. Chem. Biol. 10:409-16
64. Jayaraman S, Haggie P, Wachter RM, Remington SJ, Verkman AS. 2000. Mechanism and cellular applications of a green fluorescent protein-based halide sensor. J. Biol. Chem. 275:6047-50
65. Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A. 2011. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem. Biol. 18:1042-52
66. Keller PJ, Schmidt AD, Santella A, Khairy K, Bao Z, et al. 2010. Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nat. Methods 7:637-42
67. Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EH. 2008. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322:1065-69
68. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. 2003. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21:86-89
69. Kerppola TK. 2008. Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu. Rev. Biophys. 37:465-87
70. Kleine-Vehn J,Wabnik K, Martiniere A, Langowski L,Willig K, et al. 2011. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7:540
71. Kogure T, Kawano H, Abe Y, Miyawaki A. 2008. Fluorescence imaging using a fluorescent protein with a large Stokes shift. Methods 45:223-26
72. Komatsu T, Johnsson K, Okuno H, Bito H, Inoue T, et al. 2011. Real-time measurements of protein dynamics using fluorescence activation-coupled protein labelingmethod. J. Am. Chem. Soc. 133:6745-51
73. Konopka CA, Backues SK, Bednarek SY. 2008. Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20:1363-80
74. Konopka CA, Bednarek SY. 2008. Variable-angle epifluorescence microscopy: a new way to look at protein dynamics in the plant cell cortex. Plant J. 53:186-96
75. Lacayo CI, Malkin AJ, Holman HY, Chen L, Ding SY, et al. 2010. Imaging cell wall architecture in single Zinnia elegans tracheary elements. Plant Physiol. 154:121-33
76. Lalonde S, Ehrhardt DW, Loque D, Chen J, Rhee SY, Frommer WB. 2008. Molecular and cellular approaches for the detection of protein-protein interactions: latest techniques and current limitations. Plant J. 53:610-35
77. Lanni F, Keller E. 2000. Microscopy and microscope optical systems. In Imaging Neurons: A Laboratory Manual, ed. R Yuste, F Lanni, A Konnerth, pp. 1-72. Cold Spring Harbor,NY: Cold Spring Harb. Lab
78. Lee LY, Wu FH,Hsu CT, Shen SC, YehHY, et al. 2012. Screening a cDNA library for protein-protein interactions directly in planta. Plant Cell 24:1746-59
79. LeungDW, OtomoC,Chory J, RosenMK. 2008. Genetically encoded photoswitching of actin assembly through the Cdc42-WASP-Arp2/3 complex pathway. Proc. Natl. Acad. Sci. USA 105:12797-802
80. Levoy M, Ng R, Adams A, Footer A, Horowitz M. 2006. Light field microscopy. ACM Trans. Graph. 25:924-34
81. Levskaya A, Weiner OD, Lim WA, Voigt CA. 2009. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461:997-1001
82. Li XJ, Wang XH, Yang Y, Li RL, He QH, et al. 2011. Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23:3780-97
83. Littlejohn GR, Gouveia JD, Edner C, Smirnoff N, Love J. 2010. Perfluorodecalin enhances in vivo confocal microscopy resolution of Arabidopsis thaliana mesophyll. New Phytol. 186:1018-25
84. Magde D, Elson EL, Webb WW. 1974. Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers 13:29-61
85. Maizel A, von Wangenheim D, Federici F, Haseloff J, Stelzer EH. 2011. High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J. 68:377-85
86. Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, et al. 2008. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5:805-11
87. Mann DG, Abercrombie LL, Rudis MR, Millwood RJ, Dunlap JR, Stewart CN Jr. 2012. Very bright orange fluorescent plants: endoplasmic reticulum targeting of orange fluorescent proteins as visual reporters in transgenic plants. BMC Biotechnol. 12:17
88. MarkwardtML, Kremers GJ, KraftCA, RayK,Cranfill PJ, et al. 2011. An improved cerulean fluorescent protein with enhanced brightness and reduced reversible photoswitching. PLoS ONE 6:e17896
89. Martiniere A, Li X, Runions J, Lin J, Maurel C, Luu DT. 2012. Salt stress triggers enhanced cycling of Arabidopsis root plasma-membrane aquaporins. Plant Signal. Behav. 7:529-32
90. Marvin JS, Schreiter ER, Echevarria IM, Looger LL. 2011. A genetically encoded, high-signal-to-noise maltose sensor. Proteins 79:3025-36
91. Mathur J, Radhamony R, Sinclair AM, Donoso A, Dunn N, et al. 2010. mEosFP-based green-to-red photoconvertible subcellular probes for plants. Plant Physiol. 154:1573-87
92. Meng F, Sachs F. 2011. Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor. J. Cell Sci. 124:261-69
93. Merzlyak EM, Goedhart J, Shcherbo D, Bulina ME, Shcheglov AS, et al. 2007. Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 4:555-57
94. MiesenbockG,De Angelis DA, Rothman JE. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-95
95. 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
96. Mravec J, Petrasek J, Li N, Boeren S, Karlova R, et al. 2011. Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr. Biol. 21:1055-60
97. Murray JM. 2007. Practical aspects of quantitative confocal microscopy. Methods Cell Biol. 81:467-78
98. Murray JM, Appleton PL, Swedlow JR,Waters JC. 2007. Evaluating performance in three-dimensional fluorescence microscopy. J. Microsc. 228:390-405
99. 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
100. 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
101. Nakai J, Ohkura M, Imoto K. 2001. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19:137-41
102. Nakamura M, Ehrhardt DW, Hashimoto T. 2010. Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 12:1064-70
103. Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, et al. 2010. ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc. Natl. Acad. Sci. USA 107:21890-95
104. Nausch LW, Ledoux J, Bonev AD, Nelson MT, DostmannWR. 2008. Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc. Natl. Acad. Sci. USA 105:365-70
105. Nohe A, Petersen NO. 2007. Image correlation spectroscopy. Sci. STKE 2007:pl7
106. Okumoto S, Jones A, FrommerWB. 2012. Quantitative imaging with fluorescent biosensors. Annu. Rev. Plant Biol. 63:663-706
107. Okumoto S, Takanaga H, FrommerWB. 2008. Quantitative imaging for discovery and assembly of the metabo-regulome. New Phytol. 180:271-95
108. Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, et al. 2003. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. USA 100:2987-91
109. Ozawa T, Kaihara A, Sato M, Tachihara K, Umezawa Y. 2001. Split luciferase as an optical probe for detecting protein-protein interactions in mammalian cells based on protein splicing. Anal. Chem. 73:2516-21
110. Padilla-Parra S, Auduge N, Lalucque H, Mevel JC, Coppey-Moisan M, TramierM. 2009. Quantitative comparison of different fluorescent protein couples for fast FRET-FLIM acquisition. Biophys. J. 97:2368-76
111. Paige JS, Nguyen-Duc T, Song W, Jaffrey SR. 2012. Fluorescence imaging of cellular metabolites with RNA. Science 335:1194
112. Paige JS, Wu KY, Jaffrey SR. 2011. RNA mimics of green fluorescent protein. Science 333:642-46
113. Patterson GH, Lippincott-Schwartz J. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-77
114. Paulmurugan R,Gambhir SS. 2003. Monitoring protein-protein interactions using split synthetic renilla luciferase protein-fragment-assisted complementation. Anal. Chem. 75:1584-89
115. Qi YP, Tsuda K, Nguyen LV,Wang X, Lin JS, et al. 2011. Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J. Biol. Chem. 286:31297-307
116. Rankin BR,Moneron G,WurmCA,Nelson JC, Walter A, et al. 2011. Nanoscopy in a livingmulticellular organism expressing GFP. Biophys. J. 100:L63-65
117. Rast MI, Simon R. 2012. Arabidopsis JAGGED LATERAL ORGANS acts with ASYMMETRIC LEAVES2 to coordinate KNOX and PIN expression in shoot and root meristems. Plant Cell 24:2917-33
118. Reddy ASN, Day IS, Gohring J, Barta A. 2012. Localization and dynamics of nuclear speckles in plants. Plant Physiol. 158:67-77
119. Reynaud EG, Krzic U, Greger K, Stelzer EH. 2008. Light sheet-based fluorescence microscopy: more dimensions, more photons, and less photodamage. HFSP J. 2:266-75
120. Roppolo D, DeRybel B, Tendon VD, Pfister A, Alassimone J, et al. 2011. A novel protein family mediates Casparian strip formation in the endodermis. Nature 473:380-83
121. Runions J, Brach T, Kuhner S,Hawes C. 2006. Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J. Exp. Bot. 57:43-50
122. Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, et al. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216-29
123. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3:793-95
124. SawchukMG, Head P, Donner TJ, Scarpella E. 2007. Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytol. 176:560-71
125. Schenkel M, Sinclair AM, Johnstone D, Bewley JD, Mathur J. 2008. Visualizing the actin cytoskeleton in living plant cells using a photo-convertible mEos::FABD-mTn fluorescent fusion protein. PlantMethods 4:21
126. Schiller M, Massalski C, Kurth T, Steinebrunner I. 2012. The Arabidopsis apyrase AtAPY1 is localized in the Golgi instead of the extracellular space. BMC Plant Biol. 12:123
127. Sena G, Frentz Z, Birnbaum KD, Leibler S. 2011. Quantitation of cellular dynamics in growing Arabidopsis roots with light sheet microscopy. PLoS ONE 6:e21303
128. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22:1567-72
129. Shaner NC, Patterson GH, Davidson MW. 2007. Advances in fluorescent protein technology. J. Cell Sci. 120:4247-60
130. Shaner NC, Steinbach PA, Tsien RY. 2005. A guide to choosing fluorescent proteins. Nat. Methods 2:905-9
131. Shao L, Kner P, Rego EH, Gustafsson MG. 2011. Superresolution 3D microscopy of live whole cells using structured illumination. Nat. Methods 8:1044-46
132. Sinclair AM, Trobacher CP, Mathur N, Greenwood JS, Mathur J. 2009. Peroxule extension over ERdefined paths constitutes a rapid subcellular response to hydroxyl stress. Plant J. 59:231-42
133. Slayter EM, Slayter HS. 1992. Light and Electron Microscopy. Cambridge, UK: Cambridge Univ. Press
134. Sosinsky GE, Gaietta GM, Hand G, Deerinck TJ, Han A, et al. 2003. Tetracysteine genetic tags complexed with biarsenical ligands as a tool for investigating gap junction structure and dynamics. Cell Commun. Adhes. 10:181-86
135. Spring KR. 2007. Cameras for digital microscopy. Methods Cell Biol. 81:171-86
136. Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L. 2009. Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184:269-80
137. Steinebrunner I, Landschreiber M, Krause-Buchholz U, Teichmann J, Rodel G. 2011. HCC1, the Arabidopsis homologue of the yeast mitochondrial copper chaperone SCO1, is essential for embryonic development. J. Exp. Bot. 62:319-30
138. Stelzer EHK. 1998. Contrast, resolution, pixelation, dynamic range and signal-to-noise ratio: fundamental limits to resolution in fluorescence light microscopy. J. Microsc. Oxf. 189:15-24
139. Stoltenburg R, Reinemann C, Strehlitz B. 2007. SELEX - a (r)evolutionary method to generate highaffinity nucleic acid ligands. Biomol. Eng. 24:381-403
140. Sun X, Zhang A, Baker B, Sun L, Howard A, et al. 2011. Development of SNAP-tag fluorogenic probes for wash-free fluorescence imaging. ChemBioChem 12:2217-26
141. Swanson SJ, Choi WG, Chanoca A, Gilroy S. 2011. In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. Annu. Rev. Plant Biol. 62:273-97
142. Tabuchi S, Ito J, AdachiT, IshidaH,Hata Y, et al. 2010. Display of bothN-and C-terminal target fusion proteins on the Aspergillus oryzae cell surface using a chitin-binding module. Appl. Microbiol. Biotechnol. 87:1783-89
143. TantamaM, Hung YP, Yellen G. 2011. Imaging intracellular pH in live cells with a genetically encoded red fluorescent protein sensor. J. Am. Chem. Soc. 133:10034-37
144. Thompson NL, Lieto AM, Allen NW. 2002. Recent advances in fluorescence correlation spectroscopy. Curr. Opin. Struct. Biol. 12:634-41
145. Thompson RE, Larson DR, Webb WW. 2002. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82:2775-83
146. Umemoto Y, Araki T. 2010. Cell wall regeneration in Bangia atropurpurea (Rhodophyta) protoplasts observed using a mannan-specific carbohydrate-binding module. Mar. Biotechnol. 12:24-31
147. Urano D, Phan N, Jones JC, Yang J, Huang J, et al. 2012. Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nat. Cell Biol. 14:1079-88
148. Vaziri A, Tang J, Shroff H, Shank CV. 2008. Multilayer three-dimensional super resolution imaging of thick biological samples. Proc. Natl. Acad. Sci. USA 105:20221-26
149. Vogelmann TC. 1993. Plant-tissue optics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:231-51
150. Wallace IS, Anderson CT. 2012. Small molecule probes for plant cell wall polysaccharide imaging. Front. Plant Sci. 3:89
151. Wilt BA, Burns LD, Wei Ho ET, Ghosh KK, Mukamel EA, Schnitzer MJ. 2009. Advances in light microscopy for neuroscience. Annu. Rev. Neurosci. 32:435-506
152. Wu B, Piatkevich KD, Lionnet T, Singer RH, Verkhusha VV. 2011. Modern fluorescent proteins and imaging technologies to study gene expression, nuclear localization, and dynamics. Curr. Opin. Cell Biol. 23:310-17
153. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, et al. 2009. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461:104-8
154. Xie Q, Soutto M, Xu X, Zhang Y, Johnson CH. 2011. Bioluminescence resonance energy transfer (BRET) imaging in plant seedlings and mammalian cells. Methods Mol. Biol. 680:3-28
155. Xu X, Soutto M, Xie Q, Servick S, Subramanian C, et al. 2007. Imaging protein interactions with bioluminescence resonance energy transfer (BRET) in plant and mammalian cells and tissues. Proc. Natl. Acad. Sci. USA 104:10264-69
156. Xu Y, Piston DW, Johnson CH. 1999. A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc. Natl. Acad. Sci. USA 96:151-56
157. Zemeckis R, Gale B. 1985. Back to the Future. Directed by R Zemeckis. Universal City, CA: Universal Pictures
158. Zhou R, Kozlov AG, Roy R, Zhang J, Korolev S, et al. 2011. SSB functions as a sliding platform that migrates on DNA via reptation. Cell 146:222-32
159. Zhu L, Zhang W, Elnatan D, Huang B. 2012. Faster STORM using compressed sensing. Nat. Methods 9:721-23
160. Zou J, Hofer AM, Lurtz MM, Gadda G, Ellis AL, et al. 2007. Developing sensors for real-time measurement of high Ca2+ concentrations. Biochemistry 46:12275-88