Single-molecule detection and tracking in plants

Protoplasma

Volumn 251, Issue 2, 2014, Pages 277-291

  Langhans, Markus ^a   Meckel, Tobias ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Diffraction limit; Diffusion; Fluorescent proteins; Point spread function; Single molecule detection; Single molecule localization; Single molecule tracking

Indexed keywords

ANIMALIA; ARABIDOPSIS THALIANA;

ARABIDOPSIS; CHEMISTRY; CYTOLOGY; FLUORESCENCE MICROSCOPY; NANOTECHNOLOGY; PLANT STRUCTURES; PROCEDURES; ULTRASTRUCTURE;

ARABIDOPSIS; MICROSCOPY, FLUORESCENCE; NANOTECHNOLOGY; PLANT STRUCTURES;

EID: 84894266773     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-013-0601-0     Document Type: Review

References (110)

1. Abraham AV, Ram S, Chao J et al (2009) Quantitative study of single molecule location estimation techniques. Opt Express 17: 23352-23373.
2. Alcor D, Gouzer G, Triller A (2009) Single-particle tracking methods for the study of membrane receptors dynamics. Eur J Neurosci 30: 987-997. doi: 10. 1111/j. 1460-9568. 2009. 06927. x.
3. Arimura S, Yamamoto J, Aida GP et al (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci U S A 101: 7805-7808. doi: 10. 1073/pnas. 0401077101.
4. Axelrod D, Burghardt TP, Thompson NL (1984) Total internal reflection fluorescence. Ann Rev Biophys Bioeng 247-268.
5. Beck M, Zhou J, Faulkner C et al (2012) Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24: 4205-4219. doi: 10. 1105/tpc. 112. 100263.
6. Bender J, Benfey P, Bergmann D et al (2008) 2020 vision for biology: the role of plants in addressing grand challenges in biology. Mol Plant 1: 561-563. doi: 10. 1093/mp/ssn040.
7. Betzig E, Patterson GH, Sougrat R et al (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642-1645. doi: 10. 1126/science. 1127344.
8. Bolte S, Talbot C, Boutte Y et al (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214: 159-173.
9. Brown SC, Bolte S, Gaudin M et al (2010) Exploring plant endomembrane dynamics using the photoconvertible protein Kaede. Plant J 63: 696-711. doi: 10. 1111/j. 1365-313X. 2010. 04272. x.
10. Cheezum MK, Walker WF, Guilford WH (2001) Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys J 81: 2378-2388. doi: 10. 1016/S0006-3495(01)75884-5.
11. Durisic N, Godin AG, Wever CM et al (2012) Stoichiometry of the human glycine receptor revealed by direct subunit counting. J Neurosci 32: 12915-12920.
12. Fan L, Hao H, Xue Y et al (2013) Dynamic analysis of Arabidopsis AP2 σ subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 140: 3826-3837. doi: 10. 1242/dev. 095711.
13. Friml J, Benková E, Mayer U et al (2003) Automated whole mount localisation techniques for plant seedlings. Plant J 34: 115-124.
14. Gautier A, Juillerat A, Heinis C et al (2008) An engineered protein tag for multiprotein labeling in living cells. Chem Biol 15: 128-136. doi: 10. 1016/j. chembiol. 2008. 01. 007.
15. Haga T, Takahashi S, Sonehara T et al (2011) Dual-view imaging system using a wide-range dichroic mirror for simultaneous four-color single-molecule detection. Anal Chem 83: 6948-6955.
16. Hanson MR, Köhler RH (2001) GFP imaging: methodology and application to investigate cellular compartmentation in plants. J Exp Bot 52: 529-539.
17. Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci U S A 94: 2122-2127.
18. Hink M (2002) Fluorescence fluctuation spectroscopy applied to living plant cells.
19. Hink M a, Shah K, Russinova E et al (2008) Fluorescence fluctuation analysis of Arabidopsis thaliana somatic embryogenesis receptor-like kinase and brassinosteroid insensitive 1 receptor oligomerization. Biophys J 94: 1052-1062. doi: 10. 1529/biophysj. 107. 112003.
20. Huang Q, Huang Z, Meng G et al (2013) Plasmonic nanorod arrays for enhancement of single-molecule detection. Chem Commun (Camb) 49: 11743-11745.
21. Huisken J, Swoger J, Del Bene F et al (2004) Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305: 1007-1009. doi: 10. 1126/science. 1100035.
22. Isacoff EYUM (2007) Subunit counting in membrane-bound proteins. Bioscience 4: 319-321. doi: 10. 1038/NMETH1024. Subunit.
23. Jaqaman K, Loerke D, Mettlen M (2008) Robust single-particle tracking in live-cell time-lapse sequences. Nat 5: 695-702. doi: 10. 1038/NMETH. 1237.
24. Johnsson N, Johnsson K (2007) Review 2: 31-38.
25. Jorand R, Le Corre G, Andilla J et al (2012) Deep and clear optical imaging of thick inhomogeneous samples. PLoS One 7: e35795. doi: 10. 1371/journal. pone. 0035795.
26. Kiemer L, Cesareni G (2007) Comparative interactomics: comparing apples and pears? Trends Biotechnol 25: 448-454.
27. Kleine-Vehn J, Wabnik K, Martinière A et al (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 7: 540. doi: 10. 1038/msb. 2011. 72.
28. Konopka C a, Bednarek SY (2008) Variable-angle epifluorescence microscopy: A new way to look at protein dynamics in the plant cell cortex. Plant J 53: 186-196. doi: 10. 1111/j. 1365-313X. 2007. 03306. x.
29. Kwaaitaal M, Schor M, Hink MA et al (2011) Fluorescence correlation spectroscopy and fluorescence recovery after photobleaching to study receptor kinase mobility in planta. Methods Mol Biol 779: 225-242. doi: 10. 1007/978-1-61779-264-9.
30. Lang C, Schulze J, Mendel R-R, Hänsch R (2006) HaloTag: A new versatile reporter gene system in plant cells. J Exp Bot 57: 2985-2992. doi: 10. 1093/jxb/erl065.
31. Langhans M, Ratajczak R, Lützelschwab M et al (2001) Immunolocalization of plasma-membrane H+-ATPase and tonoplast-type pyrophosphatase in the plasma membrane of the sieve element-companion cell complex in the stem of Ricinus communis L. Planta 213: 11-19.
32. Larkin J, Cook P (2012) Maximum precision closed-form solution for localizing diffraction-limited spots in noisy images. Opt Express 20: 18478-18493.
33. Lee J, Miyanaga Y, Ueda M, Hohng S (2012) Video-rate confocal microscopy for single-molecule imaging in live cells and superresolution fluorescence imaging. Biophys J 103: 1691-1697. doi: 10. 1016/j. bpj. 2012. 09. 014.
34. Li X, Wang X, Yang Y, et al. (2011) Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 1-19. doi: 10. 1105/tpc. 111. 091454.
35. Löfblom J, Feldwisch J, Tolmachev V et al (2010) Affibody molecules: engineered proteins for therapeutic, diagnostic and biotechnological applications. FEBS Lett 584: 2670-2680. doi: 10. 1016/j. febslet. 2010. 04. 014.
36. Lommerse PHM, Blab G a, Cognet L et al (2004) Single-molecule imaging of the H-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane. Biophys J 86: 609-616. doi: 10. 1016/S0006-3495(04)74139-9.
37. Los GV, Darzins A, Zimprich C et al (2005) HaloTag interchangeable labeling technology for cell imaging, protein capture and immobilization. Promega Notes 89: 2-6.
38. Maizel A, von Wangenheim D, Federici F et al (2011) High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68: 377-385.
39. Mann DGJ, Abercrombie LL, Rudis MR et al (2012) Very bright orange fluorescent plants: endoplasmic reticulum targeting of orange fluorescent proteins as visual reporters in transgenic plants. BMC Biotechnol 12: 17. doi: 10. 1186/1472-6750-12-17.
40. Mappes T, Jahr N, Csaki A et al (2012) The invention of immersion ultramicroscopy in 1912-the birth of nanotechnology? Angew Chem Int Ed Engl 51: 11208-11212. doi: 10. 1002/anie. 201204688.
41. Martinière A, Lavagi I, Nageswaran G et al (2012) Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci U S A. doi: 10. 1073/pnas. 1202040109.
42. Mathur J, Radhamony R, Sinclair AM et al (2010) mEosFP-based green-to-red photoconvertible subcellular probes for plants. Plant Physiol 154: 1573-1587. doi: 10. 1104/pp. 110. 165431.
43. Meckel T, Hurst AC, Thiel G, Homann U (2004) Endocytosis against high turgor: Intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged K+-channel KAT1.
44. Meckel T, Semrau S, Schaaf MJM, Schmidt T (2011) Robust assessment of protein complex formation in vivo via single-molecule intensity distributions of autofluorescent proteins. J Biomed Opt 16: 076016. doi: 10. 1117/1. 3600002.
45. Meijering E, Dzyubachyk O, Smal I (2012) Methods for cell and particle tracking. Methods Enzymol 504: 183-200. doi: 10. 1016/B978-0-12-391857-4. 00009-4.
46. Merzlyak EM, Goedhart J, Shcherbo D et al (2007) Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods 4: 555-557. doi: 10. 1038/nmeth1062.
47. Millwood RJ, Halfhill MD, Harkins D et al (2003) Instrumentation and methodology for quantifying GFP fluorescence in intact plant organs. Biotechniques 34: 638-643.
48. Monici M (2005) Cell and tissue autofluorescence research and diagnostic applications. Biotechnol Annu Rev 11: 227-256.
49. Mortensen KI, Churchman LS, Spudich JA, Flyvbjerg H (2010) Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat Methods 7: 377-381.
50. Mutch S a, Fujimoto BS, Kuyper CL et al (2007) Deconvolving single-molecule intensity distributions for quantitative microscopy measurements. Biophys J 92: 2926-2943. doi: 10. 1529/biophysj. 106. 101428.
51. Muyldermans S (2013) Nanobodies: natural single-domain antibodies. Annu Rev Biochem 82: 775-797. doi: 10. 1146/annurev-biochem-063011-092449.
52. Napier RM, Fowke LC, Hawes C et al (1992) Immunological evidence that plants use both HDEL and KDEL for targeting proteins to the endoplasmic reticulum. J Cell Sci 102: 261-271, Pt 2.
53. Nie S, Chiu DT, Zare RN (1994) Probing individual molecules with confocal fluorescence microscopy. Science 266: 1018-1021.
54. Nienhaus K, Nienhaus UG (2013) Fluorescent proteins for live-cell imaging with super-resolution. Chem Soc Rev 20-24. doi: 10. 1039/c3cs60171d.
55. Nishimura H, Ritchie K, Kasai RS et al (2013) Biocompatible fluorescent silicon nanocrystals for single-molecule tracking and fluorescence imaging. J Cell Biol 202: 967-983. doi: 10. 1083/jcb. 201301053.
56. Ober RJ, Ram S, Ward ES (2004) Localization accuracy in single-molecule microscopy. Biophys J 86: 1185-1200. doi: 10. 1016/S0006-3495(04)74193-4.
57. Orrit M, Bernard J (1990) Single pentacene molecules detected by fluorescence excitation in a p-terphenyl crystal. Phys Rev Lett 65: 2716-2719.
58. Orrit M, Bernard J, Personov RI (1993) High-resolution spectroscopy of organic molecules in solids: from fluorescence line narrowing and hole burning to single molecule spectroscopy. J Phys Chem 97: 10256-10268. doi: 10. 1021/j100142a003.
59. Pinaud F, Clarke S, Sittner A, Dahan M (2010) Probing cellular events, one quantum dot at a time. Nat Methods 7: 275-285. doi: 10. 1038/nmeth. 1444.
60. Planchon TA, Gao L, Milkie DE et al (2011) Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination. Nat Methods. doi: 10. 1038/NMETH. 1586.
61. Quan T, Zhu H, Liu X et al (2011) High-density localization of active molecules using Structured Sparse Model and Bayesian Information Criterion. Opt Express 19: 16963-16974.
62. Ravindran S, Kim S, Martin R et al (2005) Quantum dots as bio-labels for the localization of a small plant adhesion protein. Nanotechnology 16: 1-4.
63. Reiner A, Arant R, Isacoff EY (2012) Assembly stoichiometry of the GluK2/GluK5 kainate receptor complex. Cell Rep 1: 234-240. doi: 10. 1016/j. celrep. 2012. 01. 003. Assembly.
64. Renz M, Daniels BR, Vámosi G et al (2012) Plasticity of the asialoglycoprotein receptor deciphered by ensemble FRET imaging and single-molecule counting PALM imaging. Proc Natl Acad Sci U S A 109: E2989-E2997. doi: 10. 1073/pnas. 1211753109.
65. Ritter JG, Veith R, Siebrasse J-P, Kubitscheck U (2008) High-contrast single-particle tracking by selective focal plane illumination microscopy. Opt Express 16: 7142-7152.
66. Ritter JG, Veith R, Veenendaal A et al (2010) Light sheet microscopy for single molecule tracking in living tissue. PLoS One 5: e11639. doi: 10. 1371/journal. pone. 0011639.
67. Rivière D, Leroy C, Guyon E, Hulin JP (1987) An optical study of thin interfacial liquid films using total reflection of light. Exp Fluids 5: 349-354.
68. Rolfe DJ, McLachlan CI, Hirsch M et al (2011) Automated multidimensional single molecule fluorescence microscopy feature detection and tracking. Eur Biophys J 40: 1167-1186. doi: 10. 1007/s00249-011-0747-7.
69. Rouwendal GJ, Mendes O, Wolbert EJ, Douwe de Boer A (1997) Enhanced expression in tobacco of the gene encoding green fluorescent protein by modification of its codon usage. Plant Mol Biol 33: 989-999.
70. Runions J, Brach T, Kühner S, Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57: 43-50. doi: 10. 1093/jxb/eri289.
71. Sakaue-Sawano A, Kurokawa H, Morimura T et al (2008) Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132: 487-498. doi: 10. 1016/j. cell. 2007. 12. 033.
72. Sako Y, Minoghchi S, Yanagida T (2000) Single-molecule imaging of EGFR signalling on the surface of living cells. Nat Cell Biol 2: 168-172.
73. Satiat-Jeunemaitre B, Boevink P, Hawes C (1999) Membrane trafficking in higher plant cells: GFP and antibodies, partners for probing the secretory pathway. Biochimie 81: 597-605.
74. Sauer M, Friml J (2010) Immunolocalization of proteins in plants. Methods Mol Biol 655: 253-263.
75. Savage RS, Oliver S (2007) Bayesian methods of astronomical source extraction. Astrophys J 661: 1339-1346. doi: 10. 1086/515393.
76. Schaaf MJM, Koopmans WJ a, Meckel T et al (2009) Single-molecule microscopy reveals membrane microdomain organization of cells in a living vertebrate. Biophys J 97: 1206-1214. doi: 10. 1016/j. bpj. 2009. 05. 044.
77. Schenkel M, Sinclair AM, Johnstone D et al (2008) Visualizing the actin cytoskeleton in living plant cells using a photo-convertible mEos:: FABD-mTn fluorescent fusion protein. Plant Methods 4: 21. doi: 10. 1186/1746-4811-4-21.
78. 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. doi: 10. 1186/1471-2229-12-123.
79. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: An open-source platform for biological-image analysis. Nat Methods 9: 676-682. doi: 10. 1038/nmeth. 2019.
80. Schnell U, Dijk F, Sjollema K, Giepmans B (2012) Immunolabeling artifacts and the need for live-cell imaging. Nat Methods. doi: 10. 1038/NMETH. 1855.
81. Schoen I, Ries J, Klotzsch E et al (2011) Binding-activated localization microscopy of DNA structures. Nano Lett 11: 4008-4011. doi: 10. 1021/nl2025954.
82. Schütz GJ, Schindler H, Schmidt T (1997) Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophys J 73: 1073-1080. doi: 10. 1016/S0006-3495(97)78139-6.
83. Semrau S, Schmidt T (2007) Particle image correlation spectroscopy (PICS): retrieving nanometer-scale correlations from high-density single-molecule position data. Biophys J 92: 613-621. doi: 10. 1529/biophysj. 106. 092577.
84. Shaner NC, Campbell RE, Steinbach PA et al (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572. doi: 10. 1038/nbt1037.
85. Shaner NC, Lin MZ, Mckeown MR et al (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5: 545-551. doi: 10. 1038/NMETH. 1209.
86. Sharonov A, Hochstrasser RM (2006) Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc Natl Acad Sci U S A 103: 18911-18916. doi: 10. 1073/pnas. 0609643104.
87. Shaw SL, Ehrhardt DW (2013) Smaller, faster, brighter: Advances in optical imaging of living plant cells. Annu Rev Plant Biol. doi: 10. 1146/annurev-arplant-042110-103843.
88. Shcherbo D, Murphy CS, Ermakova GV et al (2009) Far-red fluorescent tags for protein imaging in living tissues. Biochem J 418: 567-574. doi: 10. 1042/BJ20081949.
89. Shemiakina II, Ermakova GV, Cranfill PJ et al (2012) A monomeric red fluorescent protein with low cytotoxicity. Nat Commun 3: 1204.
90. Siebrasse JP, Kaminski T, Kubitscheck U (2012) Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc Natl Acad Sci U S A 109: 9426-9431. doi: 10. 1073/pnas. 1201781109.
91. Siedentopf H, Zsigmondy R (1902) Uber Sichtbarmachung und Größenbestimmung ultramikoskopischer Teilchen, mit besonderer Anwendung auf Goldrubingläser. Ann Phys 315: 1-39.
92. Sparkes I, Brandizzi F (2012) Fluorescent protein-based technologies: shedding new light on the plant endomembrane system. Plant J 70: 96-107.
93. Stewart CN (2006) Go with the glow: fluorescent proteins to light transgenic organisms. Trends Biotechnol 24: 155-162. doi: 10. 1016/j. tibtech. 2006. 02. 002.
94. Tokunaga M, Imamoto N, Sakata-sogawa K (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 5: 159-161. doi: 10. 1038/NMETH. 1171.
95. Tsutsui H, Karasawa S, Okamura Y, Miyawaki A (2008) Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 5: 683-685. doi: 10. 1038/NMETH. 1235.
96. Urh M, Rosenberg M (2012) HaloTag, a platform technology for protein analysis. Curr Chem Genom 6: 72-78. doi: 10. 2174/1875397301206010072.
97. Vizcay-Barrena G, Webb SED, Martin-Fernandez ML, Wilson Za (2011) Subcellular and single-molecule imaging of plant fluorescent proteins using total internal reflection fluorescence microscopy (TIRFM). J Exp Bot 1-10. doi: 10. 1093/jxb/err212.
98. Vogelmann T (1993) Plant tissue optics. Annu Rev Plant Physiol Plant Mol Biol 44: 231-251. doi: 10. 1146/annurev. arplant. 44. 1. 231.
99. VOIE AH, BURNS DH, SPELMAN FA (1993) Orthogonal-plane fluorescence optical sectioning: three-dimensional imaging of macroscopic biological specimens. J Microsc 170: 229-236.
100. Wan Y, Ash WM, Fan L et al (2011) Variable-angle total internal reflection fluorescence microscopy of intact cells of Arabidopsis thaliana. Plant Methods 7: 27.
101. Wang Y, Quan T, Zeng S, Huang Z (2012) PALMER: A method capable of parallel localization of multiple emitters for high-density localization microscopy. 20: 16039-16049. doi: 10. 1038/nmeth. 1978. S.
102. Wang Q, Zhao Y, Luo W et al (2013) Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization. Proc Natl Acad Sci U S A 110: 13204-13209.
103. Watanabe W, Shimada T, Matsunaga S et al (2007) Single-organelle tracking by two-photon conversion. Opt Express 15: 2490. doi: 10. 1364/OE. 15. 002490.
104. Weil T, Vosch T, Hofkens J et al (2010) The rylene colorant family-tailored nanoemitters for photonics research and applications. Angew Chem Int Ed Engl 49: 9068-9093. doi: 10. 1002/anie. 200902532.
105. Wieser S, Schütz GJ (2008) Tracking single molecules in the live cell plasma membrane-Do's and Don't's. Methods 46: 131-140. doi: 10. 1016/j. ymeth. 2008. 06. 010.
106. Wöll D, Kölbl C, Stempfle B, Karrenbauer A (2013) A novel method for automatic single molecule tracking of blinking molecules at low intensities. Phys Chem Chem Phys 15: 6196-6205. doi: 10. 1039/c3cp44693j.
107. Woolley JT (1975) Refractive index of soybean leaf cell walls. Plant Physiol 55: 172-174.
108. Xu X, Meckel T, Brzostowski J a et al (2010) Coupling mechanism of a GPCR and a heterotrimeric G protein during chemoattractant gradient sensing in Dictyostelium. Sci Signal 3: ra71. doi: 10. 1126/scisignal. 2000980.
109. Yoon JW, Bruckbauer A, Fitzgerald WJ, Klenerman D (2008) Bayesian inference for improved single molecule fluorescence tracking. Biophys J 94: 4932-4947. doi: 10. 1529/biophysj. 107. 116285.
110. Yoshida K, Ohnishi M, Fukao Y et al (2013) Studies on vacuolar membrane microdomains isolated from Arabidopsis suspension-cultured cells: local distribution of vacuolar membrane proteins. Plant Cell Physiol 54: 1571-1584. doi: 10. 1093/pcp/pct107.