1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 69, 2018
  5. Article

Annual Review of Plant Biology

Volume 69, 2018

Exploring the Spatiotemporal Organization of Membrane Proteins in Living Plant Cells

Abstract

Plasma membrane proteins have important roles in transport and signal transduction. Deciphering the spatiotemporal organization of these proteins provides crucial information for elucidating the links between the behaviors of different molecules. However, monitoring membrane proteins without disrupting their membrane environment remains difficult. Over the past decade, many studies have developed single-molecule techniques, opening avenues for probing the stoichiometry and interactions of membrane proteins in their native environment by providing nanometer-scale spatial information and nanosecond-scale temporal information. In this review, we assess recent progress in the development of labeling and imaging technology for membrane protein analysis. We focus in particular on several single-molecule techniques for quantifying the dynamics and assembly of membrane proteins. Finally, we provide examples of how these new techniques are advancing our understanding of the complex biological functions of membrane proteins.

Keyword(s): assembly stoichiometry, cytoskeleton, membrane microdomain, membrane proteins, protein interaction, single-molecule techniques
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042817-040233
2018-04-29
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/arplant/69/1/annurev-arplant-042817-040233.html?itemId=/content/journals/10.1146/annurev-arplant-042817-040233&mimeType=html&fmt=ahah

Literature Cited

  1. Aggarwal V, Ha T. 1.  2014. Single-molecule pull-down (SiMPull) for new-age biochemistry. Bioessays 36:1109–19 [Google Scholar]
  2. Aker J, Hesselink R, Engel R, Karlova R, Borst JW. 2.  et al. 2007. In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A complex using Förster resonance energy transfer-fluorescence lifetime imaging microscopy and fluorescence correlation spectroscopy. Plant Physiol 145:339–50 [Google Scholar]
  3. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S. 3.  et al. 2012. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. PNAS 109:303–8 [Google Scholar]
  4. Bujalowski PJ, Sherman M, Oberhauser AF. 4.  2013. Single-molecule methods. Molecular Biophysics for the Life Sciences NM Allewell, LO Narhi, I Rayment 257–88 New York: Springer [Google Scholar]
  5. Arant RJ, Ulbrich MH. 5.  2014. Deciphering the subunit composition of multimeric proteins by counting photobleaching steps. Chemphyschem 15:600–5 [Google Scholar]
  6. Bacia K, Kim SA, Schwille P. 6.  2006. Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 3:83–89 [Google Scholar]
  7. Barbieri E, Di Fiore PP, Sigismund S. 7.  2016. Endocytic control of signaling at the plasma membrane. Curr. Opin. Cell Biol. 39:21–27 [Google Scholar]
  8. Bayle V, Arrighi JF, Creff A, Nespoulous C, Vialaret J. 8.  et al. 2011. Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23:1523–35 [Google Scholar]
  9. Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S. 9.  2012. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24:4205–19 [Google Scholar]
  10. Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G. 10.  et al. 2016. Novel aquaporin regulatory mechanisms revealed by interactomics. Mol. Cell Proteom. 15:3473–87 [Google Scholar]
  11. Ben Khaled S, Postma J, Robatzek S. 11.  2015. A moving view: subcellular trafficking processes in pattern recognition receptor-triggered plant immunity. Annu. Rev. Phytopathol. 53:379–402 [Google Scholar]
  12. Berg RH, Beachy RN. 12.  2008. Fluorescent protein applications in plants. Methods Cell Biol 85:153–77 [Google Scholar]
  13. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R. 13.  2005. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. PNAS 102:3135–40 [Google Scholar]
  14. Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser MT, Persson S. 14.  2012. POM-POM2/CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24:163–77 [Google Scholar]
  15. Bücherl C, Aker J, de Vries S, Borst JW. 15.  2010. Probing protein-protein interactions with FRET-FLIM. Methods Mol. Biol. 655:389–99 [Google Scholar]
  16. Bücherl CA, Bader A, Westphal AH, Laptenok SP, Borst JW. 16.  2014. FRET-FLIM applications in plant systems. Protoplasma 251:383–94 [Google Scholar]
  17. Bücherl CA, Jarsch IK, Schudoma C, Segonzac C, Mbengue M. 17.  et al. 2017. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6:e25114 [Google Scholar]
  18. Bücherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH. 18.  et al. 2013. Visualization of BRI1 and BAK1 (SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol 162:1911–25 [Google Scholar]
  19. Candelli A, Holthausen JT, Depken M, Brouwer I, Franker MA. 19.  et al. 2014. Visualization and quantification of nascent RAD51 filament formation at single-monomer resolution. PNAS 111:15090–95 [Google Scholar]
  20. Cardinale M.20.  2014. Scanning a microhabitat: plant-microbe interactions revealed by confocal laser microscopy. Front. Plant Sci. 5:94 [Google Scholar]
  21. Chan FT, Kaminski CF, Kaminski Schierle GS. 21.  2011. HomoFRET fluorescence anisotropy imaging as a tool to study molecular self-assembly in live cells. Chemphyschem 12:500–9 [Google Scholar]
  22. Chang H, Zhang M, Ji W, Chen J, Zhang Y. 22.  et al. 2012. A unique series of reversibly switchable fluorescent proteins with beneficial properties for various applications. PNAS 109:4455–60 [Google Scholar]
  23. Chen T, Wang X, von Wangenheim D, Zheng M, Šamaj J. 23.  et al. 2012. Probing and tracking organelles in living plant cells. Protoplasma 249:S157–67 [Google Scholar]
  24. Chen Y, Müller JD, So PT, Gratton E. 24.  1999. The photon counting histogram in fluorescence fluctuation spectroscopy. Biophys. J. 77:553–67 [Google Scholar]
  25. Clark NM, Hinde E, Winter CM, Fisher AP, Crosti G. 25.  et al. 2016. Tracking transcription factor mobility and interaction in Arabidopsis roots with fluorescence correlation spectroscopy. eLife 5:e14770Uses three scanning FCS methodologies to quantify protein mobility, oligomeric state, and association. [Google Scholar]
  26. Cognet L, Leduc C, Lounis B. 26.  2014. Advances in live-cell single-particle tracking and dynamic super-resolution imaging. Curr. Opin. Chem. Biol. 20:78–85 [Google Scholar]
  27. Couto D, Zipfel C. 27.  2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52 [Google Scholar]
  28. Das SK, Darshi M, Cheley S, Wallace MI, Bayley H. 28.  2007. Membrane protein stoichiometry determined from the step-wise photobleaching of dye-labelled subunits. Chembiochem 8:994–99 [Google Scholar]
  29. Demir F, Horntrich C, Blachutzik JO, Scherzer S, Reinders Y. 29.  et al. 2013. Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. PNAS 110:8296–301Demonstrates the existence of a functional signaling complex in plant membrane nanodomains. [Google Scholar]
  30. Dunn KW, Kamocka MM, McDonald JH. 30.  2011. A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. Cell Physiol. 300:C723–42 [Google Scholar]
  31. Dunne PD, Fernandes RA, McColl J, Yoon JW, James JR. 31.  et al. 2009. DySCo: quantitating associations of membrane proteins using two-color single-molecule tracking. Biophys. J. 97:L5–7 [Google Scholar]
  32. Eggeling C, Ringemann C, Medda R, Schwarzmann G, Sandhoff K. 32.  et al. 2009. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457:1159–62 [Google Scholar]
  33. Ehrhardt DW, Frommer WB. 33.  2012. New technologies for 21st century plant science. Plant Cell 24:374–94 [Google Scholar]
  34. Elangovan M, Day RN, Periasamy A. 34.  2002. Nanosecond fluorescence resonance energy transfer-fluorescence lifetime imaging microscopy to localize the protein interactions in a single living cell. J. Microsc. 205:3–14 [Google Scholar]
  35. Fan LS, Hao HQ, Xue YQ, Zhang L, Song K. 35.  et al. 2013. Dynamic analysis of Arabidopsis AP2 σ subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 140:3826–37 [Google Scholar]
  36. Fernández-Suárez M, Ting AY. 36.  2008. Fluorescent probes for super-resolution imaging in living cells. Nat. Rev. Mol. Cell Biol. 9:929–43 [Google Scholar]
  37. Fish KN.37.  2009. Total internal reflection fluorescence (TIRF) microscopy. Curr. Protoc. Cytom. 12: Unit12.18. doi: 10.1002/0471142956.cy1218s50
  38. Fontenot EB, Ditusa SF, Kato N, Olivier DM, Dale R. 38.  et al. 2015. Increased phosphate transport of Arabidopsis thaliana Pht1;1 by site-directed mutagenesis of tyrosine 312 may be attributed to the disruption of homomeric interactions. Plant Cell Environ 38:2012–22 [Google Scholar]
  39. Giepmans BN, Adams SR, Ellisman MH, Tsien RY. 39.  2006. The fluorescent toolbox for assessing protein location and function. Science 312:217–24 [Google Scholar]
  40. Godina AG, Costantino S, Lorenzo LE, Swift JL, Sergeev M. 40.  et al. 2011. Revealing protein oligomerization and densities in situ using spatial intensity distribution analysis. PNAS 108:7010–15 [Google Scholar]
  41. Gregorio GG, Masureel M, Hilqer D, Terry DS, Juette M. 41.  et al. 2017. Single-molecule analysis of ligand efficacy in β2AR-G-protein activation. Nature 547:68–73 [Google Scholar]
  42. Grennan AK.42.  2007. Lipid rafts in plants. Plant Physiol 143:1083–85 [Google Scholar]
  43. Groves JT, Kuriyan J. 43.  2010. Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17:659–65 [Google Scholar]
  44. Gust A, Zander A, Gietl A, Holzmeister P, Schulz S. 44.  et al. 2014. A starting point for fluorescence-based single-molecule measurements in biomolecular research. Molecules 19:15824–65 [Google Scholar]
  45. Haney CH, Long SR. 45.  2010. Plant flotillins are required for infection by nitrogen-fixing bacteria. PNAS 107:478–83 [Google Scholar]
  46. Hannich JT, Umebayashi K, Riezman H. 46.  2011. Distribution and functions of sterols and sphingolipids. CSH Perspect. Biol. 3:a004762 [Google Scholar]
  47. Hao HQ, Fan LS, Chen T, Li RL, Li XJ. 47.  et al. 2014. Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26:1729–45 [Google Scholar]
  48. Hassler K, Leutenegger M, Rigler P, Rao R, Rigler R. 48.  et al. 2005. Total internal reflection fluorescence correlation spectroscopy (TIR-FCS) with low background and high count-rate per molecule. Opt. Express 13:7415–23 [Google Scholar]
  49. He HT, Marguet D. 49.  2011. Detecting nanodomains in living cell membrane by fluorescence correlation spectroscopy. Annu. Rev. Phys. Chem. 62:417–36 [Google Scholar]
  50. Head BP, Patel HH, Insel PA. 50.  2014. Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim. Biophys. Acta 1838:532–45 [Google Scholar]
  51. Hedde PN, Nienhaus GU. 51.  2014. Super-resolution localization microscopy with photoactivatable fluorescent marker proteins. Protoplasma 251:349–62 [Google Scholar]
  52. Henty-Ridilla JL, Li J, Blanchoin L, Staiger CJ. 52.  2013. Actin dynamics in the cortical array of plant cells. Curr. Opin. Plant Biol. 16:678–87 [Google Scholar]
  53. Hink MA, Shah K, Russinova E, de Vries SC, Visser AJ. 53.  2008. Fluorescence fluctuation analysis of Arabidopsis thaliana somatic embryogenesis receptor-like kinase and brassinosteroid insensitive 1 receptor oligomerization. Biophys. J. 94:1052–62Analyzes the oligomerization state and mobility of plasma membrane proteins in plants by FCCS and PCH techniques. [Google Scholar]
  54. Hosy E, Martinière A, Choquet D, Maurel C, Luu DT. 54.  2015. Super-resolved and dynamic imaging of membrane proteins in plant cells reveal contrasting kinetic profiles and multiple confinement mechanisms. Mol. Plant 8:339–42 [Google Scholar]
  55. Husbands AY, Aggarwal V, Ha T, Timmermans MC. 55.  2016. In planta single-molecule pull-down reveals tetrameric stoichiometry of HD-ZIPIII:LITTLE ZIPPER complexes. Plant Cell 28:1783–94 [Google Scholar]
  56. Ishikawa-Ankerhold HC, Ankerhold R, Drummen GP. 56.  2012. Advanced fluorescence microscopy techniques—FRAP, FLIP, FLAP, FRET and FLIM. Molecules 17:4047–132 [Google Scholar]
  57. Jaqaman K, Grinstein S. 57.  2012. Regulation from within: the cytoskeleton in transmembrane signaling. Trends Cell Biol 22:515–26 [Google Scholar]
  58. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S. 58.  et al. 2008. Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5:695–702 [Google Scholar]
  59. Jarsch IK, Konrad SS, Stratil TF, Urbanus SL, Szymanski W. 59.  et al. 2014. Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698–711 [Google Scholar]
  60. Jarsch IK, Ott T. 60.  2011. Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol. Plant Microbe. Interact. 24:7–12 [Google Scholar]
  61. Ji W, Xu P, Li Z, Lu J, Liu L. 61.  et al. 2008. Functional stoichiometry of the unitary calcium-release-activated calcium channel. PNAS 105:13668–73 [Google Scholar]
  62. Kleine-Vehn J, Wabnik K, Martinière A, Łangowski Ł, Willig K. 62.  et al. 2011. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7:540 [Google Scholar]
  63. Komis G, Šamajová O, Ovečka M, Šamaj J. 63.  2015. Super-resolution microscopy in plant cell imaging. Trends Plant Sci 20:834–43Summarizes the basic principles of existing super-resolution methods and provides their applications to plants. [Google Scholar]
  64. Konopka CA, Backues SK, Bednarek SY. 64.  2008. Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20:1363–80 [Google Scholar]
  65. Konopka CA, Bednarek SY. 65.  2008. Variable-angle epifluorescence microscopy: a new way to look at protein dynamics in the plant cell cortex. Plant J 53:186–96 [Google Scholar]
  66. Konrad SS, Ott T. 66.  2015. Molecular principles of membrane microdomain targeting in plants. Trends Plant Sci 20:351–61Provides an overview of the different types of membrane microdomains and the targeting modes of membrane proteins at the plasma membrane. [Google Scholar]
  67. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK. 67.  2011. Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36:604–15 [Google Scholar]
  68. Kwon C, Neu C, Pajonk HS, Yun H, Lipka U. 68.  et al. 2008. Co-option of a default secretory pathway for plant immune responses. Nature 451:835–40 [Google Scholar]
  69. Kwon C, Yun HS. 69.  2014. Plant exocytic secretion of toxic compounds for defense. Toxicol. Res. 30:77–81 [Google Scholar]
  70. Landrum M, Smertenko A, Edwards R, Hussey PJ, Steel PG. 70.  2010. BODIPY probes to study peroxisome dynamics in vivo. Plant J 62:529–38 [Google Scholar]
  71. Langhans M, Meckel T. 71.  2014. Single-molecule detection and tracking in plants. Protoplasma 251:277–91Describes the main steps required to perform a single-molecule experiment from acquisition to analysis. [Google Scholar]
  72. Laude AJ, Prior IA. 72.  2004. Plasma membrane microdomains: organization, function and trafficking. Mol. Membr. Biol. 21:193–205 [Google Scholar]
  73. Leborgne-Castel N, Luu DT. 73.  2009. Regulation of endocytosis by external stimuli in plant cells. Plant Biosyst 143:630–35 [Google Scholar]
  74. Lefebvre B, Timmers T, Mbengue M, Moreau S, Hervé C. 74.  et al. 2010. A remorin protein interacts with symbiotic receptors and regulates bacterial infection. PNAS 107:2343–48 [Google Scholar]
  75. Lherminier J, Elmayan T, Fromentin J, Elaraqui KT, Vesa S. 75.  et al. 2009. NADPH oxidase-mediated reactive oxygen species production: subcellular localization and reassessment of its role in plant defense. Mol. Plant Microbe. Interact. 22:868–81 [Google Scholar]
  76. Li J, Tax FE. 76.  2013. Receptor‐like kinases: key regulators of plant development and defense. J. Integr. Plant Biol. 55:1184–87 [Google Scholar]
  77. Li RL, Liu P, Wan YL, Chen T, Wang QL. 77.  et al. 2012. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24:1–19 [Google Scholar]
  78. Li X, Luu DT, Maurel C, Lin J. 78.  2013. Probing plasma membrane dynamics at the single-molecule level. Trends Plant Sci 18:617–24 [Google Scholar]
  79. Li X, Wang X, Yang Y, Li R, He Q. 79.  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 [Google Scholar]
  80. Li X, Xing J, Qiu Z, He Q, Lin J. 80.  2016. Quantification of membrane protein dynamics and interactions in plant cells by fluorescence correlation spectroscopy. Mol. Plant 9:1229–39 [Google Scholar]
  81. Lillemeier BF, Pfeiffer JR, Surviladze Z, Wilson BS, Davis MM. 81.  2006. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. PNAS 103:18992–97 [Google Scholar]
  82. Lingwood D, Simons K. 82.  2010. Lipid rafts as a membrane organizing principle. Science 327:46–50 [Google Scholar]
  83. Liu Z, Lavis LD, Betzig E. 83.  2015. Imaging live-cell dynamics and structure at the single-molecule level. Mol. Cell 58:644–59 [Google Scholar]
  84. Liu Z, Schneider R, Kesten C, Zhang Y, Somssich M. 84.  et al. 2016. Cellulose-microtubule uncoupling proteins prevent lateral displacement of microtubules during cellulose synthesis in Arabidopsis. Dev. Cell 38:305–15 [Google Scholar]
  85. Lukyanov KA, Chudakov DM, Lukyanov S, Verkhusha VV. 85.  2005. Innovation: photoactivatable fluorescent proteins. Nat. Rev. Mol. Cell Biol. 6:885–91 [Google Scholar]
  86. Luo Y, Scholl S, Doering A, Zhang Y, Irani NG. 86.  et al. 2015. V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis. Nat. Plants 1:15094 [Google Scholar]
  87. Luschnig C, Vert G. 87.  2014. The dynamics of plant plasma membrane proteins: PINs and beyond. Development 141:2924–38 [Google Scholar]
  88. Luu DT, Martinière A, Sorieul M, Runions J, Maurel C. 88.  2012. Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J 69:894–905 [Google Scholar]
  89. Lv X, Jing Y, Wu H, Lin J. 89.  2017. Tracking tonoplast protein behaviors in intact vacuoles isolated from Arabidopsis leaves. Mol. Plant 10:349–52 [Google Scholar]
  90. Lv X, Jing Y, Xiao J, Zhang Y, Zhu Y. 90.  et al. 2017. Membrane microdomains and the cytoskeleton constrain AtHIR1 dynamics and facilitate the formation of an AtHIR1‐associated immune complex. Plant J 90:3–16 [Google Scholar]
  91. Ma X, Foo YH, Wohland T. 91.  2014. Fluorescence cross-correlation spectroscopy (FCCS) in living cells. Methods Mol. Biol. 1076:557–73 [Google Scholar]
  92. Malinsky J, Opekarova M, Grossmann G, Tanner W. 92.  2013. Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu. Rev. Plant Biol. 64:501–29 [Google Scholar]
  93. Martfeld AN, Rajaqopalan V, Greathouse DV, Koeppe RE. 93.  2015. Dynamic regulation of lipid-protein interactions. Biochim. Biophys. Acta 1848:1849–59 [Google Scholar]
  94. Martinière A, Gayral P, Hawes C, Runions J. 94.  2011. Building bridges: FORMIN1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J 66:354–65 [Google Scholar]
  95. Martinière A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L. 95.  et al. 2012. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. PNAS 109:12805–10 [Google Scholar]
  96. Martinière A, Runions J. 96.  2013. Protein diffusion in plant cell plasma membranes: the cell-wall corral. Front. Plant Sci. 4:515 [Google Scholar]
  97. McGuire H, Aurousseau MR, Bowie D, Blunck R. 97.  2012. Automating single subunit counting of membrane proteins in mammalian cells. J. Biol. Chem. 287:35912–21 [Google Scholar]
  98. Men S, Boutte Y, Ikeda Y, Li X, Palme K. 98.  et al. 2008. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 10:237–44 [Google Scholar]
  99. Miesenbock G, De Angelis DA, Rothman JE. 99.  1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192–95 [Google Scholar]
  100. Mirabella R, Franken C, van der Krogt GN, Bisseling T, Geurts R. 100.  2004. Use of the fluorescent timer DsRED-E5 as reporter to monitor dynamics of gene activity in plants. Plant Physiol 135:1879–87 [Google Scholar]
  101. Miyawaki A.101.  2011. Proteins on the move: insights gained from fluorescent protein technologies. Nat. Rev. Mol. Cell Biol. 12:656–68 [Google Scholar]
  102. Monaghan J, Zipfel C. 102.  2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349–57 [Google Scholar]
  103. Mongrand S, Stanislas T, Bayer EM, Lherminier J, Simon-Plas F. 103.  2010. Membrane rafts in plant cells. Trends Plant Sci 15:656–63 [Google Scholar]
  104. Mudumbi KC, Schirmer EC, Yang W. 104.  2016. Single-point single-molecule FRAP distinguishes inner and outer nuclear membrane protein distribution. Nat. Commun. 7:12562 [Google Scholar]
  105. Müller SM, Galliardt H, Schneider J, Barisas BG, Seidel T. 105.  2013. Quantification of Förster resonance energy transfer by monitoring sensitized emission in living plant cells. Front. Plant Sci. 4:413 [Google Scholar]
  106. Nechyporuk-Zloy V, Dieterich P, Oberleithner H, Stock C, Schwab A. 106.  2008. Dynamics of single potassium channel proteins in the plasma membrane of migrating cells. Am. J. Physiol. Cell Physiol. 294:C1096–102 [Google Scholar]
  107. Nishida N, Osawa M, Takeuchi K, Imai S, Stampoulis P. 107.  et al. 2014. Functional dynamics of cell surface membrane proteins. J. Magn. Reson. 24:186–96 [Google Scholar]
  108. Padilla-Parra S, Tramier M. 108.  2012. FRET microscopy in the living cell: different approaches, strengths and weaknesses. Bioessays 34:369–76 [Google Scholar]
  109. Paez Valencia J, Goodman K, Otegui MS. 109.  2016. Endocytosis and endosomal trafficking in plants. Annu. Rev. Plant Biol. 67:309–35 [Google Scholar]
  110. Paredez AR, Somerville CR, Ehrhardt DW. 110.  2006. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–95 [Google Scholar]
  111. Patterson GH, Lippincott-Schwartz J. 111.  2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873–77 [Google Scholar]
  112. Pi J, Jin H, Yang F, Chen ZW, Cai J. 112.  2014. In situ single molecule imaging of cell membranes: linking basic nanotechniques to cell biology, immunology and medicine. Nanoscale 6:12229–49 [Google Scholar]
  113. Pinaud F, Clarke S, Sittner A, Dahan M. 113.  2010. Probing cellular events, one quantum dot at a time. Nat. Methods 7:275–85 [Google Scholar]
  114. Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T. 114.  2008. Quantum dots versus organic dyes as fluorescent labels. Nat. Methods 5:763–75 [Google Scholar]
  115. Rieckher M.115.  2017. Light sheet microscopy to measure protein dynamics. J. Cell Physiol. 232:27–35 [Google Scholar]
  116. Ries J, Schwille P. 116.  2012. Fluorescence correlation spectroscopy. Bioessays 34:361–68 [Google Scholar]
  117. Ritter JG, Veith R, Veenendaal A, Siebrasse JP, Kubitscheck U. 117.  2010. Light sheet microscopy for single molecule tracking in living tissue. PLOS ONE 23:e11629 [Google Scholar]
  118. Robert S, Bichet A, Grandjean O, Kierzkowski D, Satiat-Jeunemaître B. 118.  et al. 2005. An Arabidopsis endo-1,4-beta-d-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell 17:3378–89 [Google Scholar]
  119. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH. 119.  et al. 2005. COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–63 [Google Scholar]
  120. Roy R, Hohng S, Ha T. 120.  2008. A practical guide to single-molecule FRET. Nat. Methods 5:507–16Describes the practical issues of TIR-based smFRET. [Google Scholar]
  121. Sampathkumar A, Gutierrez R, McFarlane HE, Bringmann M, Lindeboom J. 121.  et al. 2013. Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol 162:675–88 [Google Scholar]
  122. Sardar HS, Yang J, Showalter AM. 122.  2006. Molecular interactions of arabinogalactan proteins with cortical microtubules and F-actin in bright yellow-2 tobacco cultured cells. Plant Physiol 142:1469–79 [Google Scholar]
  123. Sasmal DK, Pulido LE, Kasal S, Huang J. 123.  2016. Single-molecule fluorescence resonance energy transfer in molecular biology. Nanoscale 48:19928–44 [Google Scholar]
  124. Schubert V.124.  2017. Super-resolution microscopy - applications in plant cell research. Front. Plant Sci. 8:531 [Google Scholar]
  125. Shaw SL, Ehrhardt DW. 125.  2013. Smaller, faster, brighter: advances in optical imaging of living plant cells. Annu. Rev. Plant Biol. 64:351–75Summarizes technological advances focused on the challenges and opportunities for imaging living plant cells. [Google Scholar]
  126. Simons K, Toomre D. 126.  2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31–39 [Google Scholar]
  127. Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A. 127.  2014. Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol 164:440–54 [Google Scholar]
  128. Song K, Xue Y, Wang X, Wan Y, Deng X, Lin J. 128.  2017. A modified GFP facilitates counting membrane protein subunits by step-wise photobleaching in Arabidopsis. J. Plant Physiol 213:129–33 [Google Scholar]
  129. Sorkin A, von Zastrow M. 129.  2009. Endocytosis and signaling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10:609–22 [Google Scholar]
  130. Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S. 130.  et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23:362–71 [Google Scholar]
  131. Stock K, Sailer R, Strauss WS, Lyttek M, Steiner R, Schneckenburger H. 131.  2003. Variable-angle total internal reflection fluorescence microscopy (VA-TIRFM): realization and application of a compact illumination device. J. Microsc. 211:19–29 [Google Scholar]
  132. Sustarsic M, Kapanidis AN. 132.  2015. Taking the ruler to the jungle: single-molecule FRET for understanding biomolecular structure and dynamics in live cells. Curr. Opin. Struct. Biol. 34:52–59 [Google Scholar]
  133. Sutter JU, Campanoni P, Tyrrell M, Blatt MR. 133.  2006. Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18:935–54 [Google Scholar]
  134. Swift JL, Godin AG, Doré K, Freland L, Bouchard N. 134.  et al. 2011. Quantification of receptor tyrosine kinase transactivation through direct dimerization and surface density measurements in single cells. PNAS 108:7016–21 [Google Scholar]
  135. Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K. 135.  et al. 2010. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. PNAS 107:5220–25 [Google Scholar]
  136. Ulbrich MH, Isacoff EY. 136.  2007. Subunit counting in membrane-bound proteins. Nat. Methods 4:319–21Describes a single-molecule technique for counting subunits of proteins in living cell membranes by analyzing the bleaching steps of fluorescent proteins. [Google Scholar]
  137. Vizcay-Barrena G, Webb SE, Martin-Fernandez ML, Wilson ZA. 137.  2011. Subcellular and single-molecule imaging of plant fluorescent proteins using total internal reflection fluorescence microscopy (TIRFM). J. Exp. Bot. 62:5419–28Demonstrates that TIRFM is a valuable tool for in vivo analysis and can be used for single-molecule analysis in plants. [Google Scholar]
  138. Wallrabe H, Periasamy A. 138.  2005. Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol. 16:19–27 [Google Scholar]
  139. Wan Y, III Ash WM, Fan L, Hao H, Kim MK, Lin J. 139.  2011. Variable-angle total internal reflection fluorescence microscopy of intact cells of Arabidopsis thaliana. Plant Methods 7:27 [Google Scholar]
  140. Wang H, Han S, Siao W, Song C, Xiang Y. 140.  et al. 2015. Arabidopsis synaptotagmin 2 participates in pollen germination and tube growth and is delivered to plasma membrane via conventional secretion. Mol. Plant 8:1737–50 [Google Scholar]
  141. Wang L, Li H, Lv X, Chen T, Li R. 141.  et al. 2015. Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol. Plant 8:1334–49 [Google Scholar]
  142. Wang QL, Chen B, Liu P, Zheng M, Wang Y. 142.  et al. 2009. Calmodulin binds to extracellular sites on the plasma membrane of plant cells and elicits a rise in intracellular calcium concentration. J. Biol. Chem. 284:12000–7 [Google Scholar]
  143. Wang QL, Zhao YY, Luo WX, Li RL, He QH. 143.  et al. 2013. Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization. PNAS 110:13204–9 [Google Scholar]
  144. Wang X, Li X, Deng X, Luu DT, Maurel C, Lin J. 144.  2015. Single-molecule fluorescence imaging to quantify membrane protein dynamics and oligomerization in living plant cells. Nat. Protoc. 10:2054–63 [Google Scholar]
  145. Xia T, Li N, Fang XH. 145.  2013. Single-molecule fluorescence imaging in living cells. Annu. Rev. Physiol. 64:459–80 [Google Scholar]
  146. Yu G, Tan Y, He X, Qin Y, Liang J. 146.  2014. CLAVATA3 dodecapeptide modified CdTe nanoparticles: a biocompatible quantum dot probe for in vivo labeling of plant stem cells. PLOS ONE 9:e89241 [Google Scholar]
  147. Yu J.147.  2016. Single-molecule studies in live cells. Annu. Rev. Phys. Chem. 67:565–85 [Google Scholar]
  148. Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F. 148.  2007. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. PNAS 104:12359–64 [Google Scholar]
  149. Zhang WH, Rengel Z, Kuo J. 149.  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 [Google Scholar]
  150. Zinchuk V, Wu Y, Grossenbacher-Zinchuk O. 150.  2013. Bridging the gap between qualitative and quantitative colocalization results in fluorescence microscopy studies. Sci. Rep. 3:1365 [Google Scholar]
  151. Zinchuk V, Wu Y, Grossenbacher-Zinchuk O, Stefani E. 151.  2011. Quantifying spatial correlations of fluorescent markers using enhanced background reduction with protein proximity index and correlation coefficient estimations. Nat. Protoc. 6:1554–67 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040233
Loading
Exploring the Spatiotemporal Organization of Membrane Proteins in Living Plant Cells
Annual Review of Plant Biology 69, 525 (2018); https://doi.org/10.1146/annurev-arplant-042817-040233
/content/journals/10.1146/annurev-arplant-042817-040233
/content/journals/10.1146/annurev-arplant-042817-040233
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error