Advertisement

Technical Review: Microscopy and Image Processing Tools to Analyze Plant Chromatin: Practical Considerations

Protocol
First Online:
Part of the Methods in Molecular Biology book series (MIMB, volume 1675)

Abstract

In situ nucleus and chromatin analyses rely on microscopy imaging that benefits from versatile, efficient fluorescent probes and proteins for static or live imaging. Yet the broad choice in imaging instruments offered to the user poses orientation problems. Which imaging instrument should be used for which purpose? What are the main caveats and what are the considerations to best exploit each instrument’s ability to obtain informative and high-quality images? How to infer quantitative information on chromatin or nuclear organization from microscopy images? In this review, we present an overview of common, fluorescence-based microscopy systems and discuss recently developed super-resolution microscopy systems, which are able to bridge the resolution gap between common fluorescence microscopy and electron microscopy. We briefly present their basic principles and discuss their possible applications in the field, while providing experience-based recommendations to guide the user toward best-possible imaging. In addition to raw data acquisition methods, we discuss commercial and noncommercial processing tools required for optimal image presentation and signal evaluation in two and three dimensions.

Key words

Plant chromatin Widefield microscopy Confocal microscopy Light sheet microscopy Super-resolution microscopy Electron microscopy Resolution Image processing Image segmentation Deconvolution Signal quantification 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

CB is funded by the Swiss National Science Foundation (SNSF), the University of Zürich and SystemsX.ch. CB acknowledges the expert assistance and training provided by the Microscopy Facility of the University of Zürich particularly in TEM, LSM and SRM imaging (ZMB, Prof. Urs Ziegler, Jana Doehner, Dominik Haenni, Moritz Kirschmann, Andreas Kaech), Mariamawit Ashenafi for the 3D image file used in Fig. 3c3. We thank Jörg Fuchs for flow sorting of nuclei, Martina Kühne and Andrea Kunze for slide preparation, Andreas Houben, Gerhard Wanner and Klaus Weisshart for critical reading of the manuscript, Marian Bemer for critical reading and suggestions.

References

  1. 1.
    Olins DE, Olins AL (2003) Chromatin history: a view from the bridge. Nat Rev Mol Cell Biol 4:809–814PubMedCrossRefGoogle Scholar
  2. 2.
    Hergeth SP, Schneider R (2015) The H1 linker histones: multifunctional proteins beyond the nucleosomal core particle. EMBO Rep 16(11):1439–1453PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Schneider R, Grosschedl R (2007) Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev 21(23):3027–3043PubMedCrossRefGoogle Scholar
  4. 4.
    van Driel R, Fransz P (2004) Nuclear architecture and genome functioning in plants and animals: what can we learn from both? Exp Cell Res 296(1):86–90PubMedCrossRefGoogle Scholar
  5. 5.
    Deal RB, Henikoff S (2011) The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat Protoc 6(1):56–68PubMedCrossRefGoogle Scholar
  6. 6.
    Moreno-Romero J, Santos-Gonzalez J, Hennig L, Kohler C (2017) Applying the INTACT method to purify endosperm nuclei and to generate parental-specific epigenome profiles. Nat Protoc 12(2):238–254PubMedCrossRefGoogle Scholar
  7. 7.
    Kawakatsu T, Stuart T, Valdes M, Breakfield N, Schmitz RJ, Nery JR, Urich MA, Han X, Lister R, Benfey PN, Ecker JR (2016) Unique cell-type-specific patterns of DNA methylation in the root meristem. Nat Plants 2(5):16058PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Morao AK, Caillieux E, Colot V, Roudier F (2017) Cell type-specific profiling of chromatin modifications and associated proteins. In: Plant chromatin dynamics, Methods in Molecular Biology. Springer, New York, NYGoogle Scholar
  9. 9.
    Gonzalez-Sandoval A, Gasser SM (2016) On TADs and LADs: spatial control over gene expression. Trends Genet 32(8):485–495PubMedCrossRefGoogle Scholar
  10. 10.
    North AJ (2006) Seeing is believing? A beginners’ guide to practical pitfalls in image acquisition. J Cell Biol 172(1):9–18PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Lambert TJ, Waters JC (2017) Navigating challenges in the application of superresolution microscopy. J Cell Biol 216(1):53–63PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Shaw SL (2006) Imaging the live plant cell. Plant J 45(4):573–598PubMedCrossRefGoogle Scholar
  13. 13.
    Shaw SL, Ehrhardt DW (2013) Smaller, faster, brighter: advances in optical imaging of living plant cells. Annu Rev Plant Biol 64:351–375PubMedCrossRefGoogle Scholar
  14. 14.
    Probst A (2017) A compendium of methods to analyse the spatial organization of plant chromatin. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_23 Google Scholar
  15. 15.
    Mao YS, Zhang B, Spector DL (2011) Biogenesis and function of nuclear bodies. Trends Genet 27(8):295–306PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Meier I (2009) Functional organization of the plant nucleus. In: Meier I (ed) Functional organization of the plant nucleus. Springer, Berlin, pp 1–8. doi: 10.1007/978-3-540-71058-5_1 CrossRefGoogle Scholar
  17. 17.
    Cheng P-C (2010) Interaction of light with botanical specimens. In: Pawley JB (ed) Handbook for biological confocal microscopy, 3rd edn. Springer, New York, NY, pp 414–441Google Scholar
  18. 18.
    Ohad N, Yalovsky S (2010) Utilizing bimolecular fluorescence complementation (BiFC) to assay protein-protein interaction in plants. Methods Mol Biol 655:347–358PubMedCrossRefGoogle Scholar
  19. 19.
    Horstman A, Tonaco IA, Boutilier K, Immink RG (2014) A cautionary note on the use of split-YFP/BiFC in plant protein-protein interaction studies. Int J Mol Sci 15(6):9628–9643PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Bu Z, Yu Y, Li Z, Liu Y, Jiang W, Huang Y, Dong AW (2014) Regulation of arabidopsis flowering by the histone mark readers MRG1/2 via interaction with CONSTANS to modulate FT expression. PLoS Genet 10(9):e1004617PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Song ZT, Sun L, Lu SJ, Tian Y, Ding Y, Liu JX (2015) Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants. Proc Natl Acad Sci U S A 112(9):2900–2905PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Perrella G, Carr C, Asensi-Fabado MA, Donald NA, Paldi K, Hannah MA, Amtmann A (2016) The histone deacetylase complex 1 protein of arabidopsis has the capacity to interact with multiple proteins including histone 3-binding proteins and histone 1 variants. Plant Physiol 171(1):62–70PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Gadella TW Jr, van der Krogt GN, Bisseling T (1999) GFP-based FRET microscopy in living plant cells. Trends Plant Sci 4(7):287–291PubMedCrossRefGoogle Scholar
  24. 24.
    Benvenuto G, Formiggini F, Laflamme P, Malakhov M, Bowler C (2002) The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr Biol 12(17):1529–1534PubMedCrossRefGoogle Scholar
  25. 25.
    Hasegawa J, Sakamoto Y, Nakagami S, Aida M, Sawa S, Matsunaga S (2016) Three-dimensional imaging of plant organs using a simple and rapid transparency technique. Plant Cell Physiol 57(3):462–472PubMedCrossRefGoogle Scholar
  26. 26.
    Kurihara D, Mizuta Y, Sato Y, Higashiyama T (2015) ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142(23):4168–4179PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Warner CA, Biedrzycki ML, Jacobs SS, Wisser RJ, Caplan JL, Sherrier DJ (2014) An optical clearing technique for plant tissues allowing deep imaging and compatible with fluorescence microscopy. Plant Physiol 166(4):1684–1687PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Musielak TJ, Schenkel L, Kolb M, Henschen A, Bayer M (2015) A simple and versatile cell wall staining protocol to study plant reproduction. Plant Reprod 28(3-4):161–169PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Musielak TJ, Slane D, Liebig C, Bayer M (2016) A versatile optical clearing protocol for deep tissue imaging of fluorescent proteins in Arabidopsis thaliana. PLoS One 11(8):e0161107PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    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(4):1018–1025PubMedCrossRefGoogle Scholar
  31. 31.
    Littlejohn GR, Mansfield JC, Christmas JT, Witterick E, Fricker MD, Grant MR, Smirnoff N, Everson RM, Moger J, Love J (2014) An update: improvements in imaging perfluorocarbon-mounted plant leaves with implications for studies of plant pathology, physiology, development and cell biology. Front Plant Sci 5:140PubMedPubMedCentralGoogle Scholar
  32. 32.
    Nagaki K, Yamaji N, Murata M (2017) ePro-ClearSee: a simple immunohistochemical method that does not require sectioning of plant samples. Sci Rep 7:42203PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    She W, Grimanelli D, Baroux C (2014) An efficient method for quantitative, single-cell analysis of chromatin modification and nuclear organization in whole-mount ovules in Arabidopsis. J Vis Exp (88):e51530Google Scholar
  34. 34.
    Escobar-Guzman R, Rodriguez-Leal D, Vielle-Calzada JP, Ronceret A (2015) Whole-mount immunolocalization to study female meiosis in Arabidopsis. Nat Protoc 10(10):1535–1542PubMedCrossRefGoogle Scholar
  35. 35.
    Pillot M, Baroux C, Vazquez MA, Autran D, Leblanc O, Vielle-Calzada JP, Grossniklaus U, Grimanelli D (2010) Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22(2):307–320PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    She W, Grimanelli D, Rutowicz K, Whitehead MW, Puzio M, Kotlinski M, Jerzmanowski A, Baroux C (2013) Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140(19):4008–4019PubMedCrossRefGoogle Scholar
  37. 37.
    Costa S, Shaw P (2006) Chromatin organization and cell fate switch respond to positional information in Arabidopsis. Nature 439(7075):493–496PubMedCrossRefGoogle Scholar
  38. 38.
    Gernand D, Rutten T, Varshney A, Rubtsova M, Prodanovic S, Bruss C, Kumlehn J, Matzk F, Houben A (2005) Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation. Plant Cell 17(9):2431–2438PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Wegel E, Vallejos RH, Christou P, Stoger E, Shaw P (2005) Large-scale chromatin decondensation induced in a developmentally activated transgene locus. J Cell Sci 118(Pt 5):1021–1031PubMedCrossRefGoogle Scholar
  40. 40.
    Braszewska-Zalewska AJ, Wolny EA, Smialek L, Hasterok R (2013) Tissue-specific epigenetic modifications in root apical meristem cells of Hordeum vulgare. PLoS One 8(7):e69204PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Wolny E, Braszewska-Zalewska A, Kroczek D, Hasterok R (2015) In situ analysis of epigenetic modifications in the chromatin of Brachypodium distachyon embryos. Plant Signal Behav 10(5):e1011948PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Bourdon M, Coriton O, Pirrello J, Cheniclet C, Brown SC, Poujol C, Chevalier C, Renaudin JP, Frangne N (2011) In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH). Plant J 66(6):1089–1099PubMedCrossRefGoogle Scholar
  43. 43.
    Garcia-Aguilar M, Michaud C, Leblanc O, Grimanelli D (2010) Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22(10):3249–3267PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Bey TD, Koini M, Fransz P (2017) Fluorescence in situ hybridization (FISH) and immunolabeling on 3D preserved nuclei. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_27 Google Scholar
  45. 45.
    Ashenafi M, Baroux C (2017) Automated 3D gene position analysis using a customized Imaris plugin: XTFISHInsideNucleus. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_32 Google Scholar
  46. 46.
    She W, Baroux C, Grossniklaus U (2017) Cell-type specific chromatin analysis in whole-mount plant tissues by immunostaining. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_25 Google Scholar
  47. 47.
    Marques-Bueno MM, Morao AK, Cayrel A, Platre MP, Barberon M, Caillieux E, Colot V, Jaillais Y, Roudier F, Vert G (2016) A versatile multisite gateway-compatible promoter and transgenic line collection for cell type-specific functional genomics in Arabidopsis. Plant J 85(2):320–333PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Poulet A, Arganda-Carreras I, Legland D, Probst AV, Andrey P, Tatout C (2015) NucleusJ: an ImageJ plugin for quantifying 3D images of interphase nuclei. Bioinformatics 31(7):1144–1146PubMedCrossRefGoogle Scholar
  49. 49.
    Andrey P, Kieu K, Kress C, Lehmann G, Tirichine L, Liu Z, Biot E, Adenot PG, Hue-Beauvais C, Houba-Herin N, Duranthon V, Devinoy E, Beaujean N, Gaudin V, Maurin Y, Debey P (2010) Statistical analysis of 3D images detects regular spatial distributions of centromeres and chromocenters in animal and plant nuclei. PLoS Comput Biol 6(7):e1000853PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Desset S, Poulet A, Tatout C (2017) Quantitative 3D analysis of nuclear morphology and heterochromatin organization from whole mount plant tissue using NucleusJ. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_33 Google Scholar
  51. 51.
    Arpon J, Gaudin V, Andrey P (2017) A method for testing random spatial model on nuclear object distributions. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_29 Google Scholar
  52. 52.
    Fang Y, Spector DL (2005) Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell 16(12):5710–5718PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    de Nooijer S, Wellink J, Mulder B, Bisseling T (2009) Non-specific interactions are sufficient to explain the position of heterochromatic chromocenters and nucleoli in interphase nuclei. Nucleic Acids Res 37(11):3558–3568PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Murphy SP, Gumber HK, Mao Y, Bass HW (2014) A dynamic meiotic SUN belt includes the zygotene-stage telomere bouquet and is disrupted in chromosome segregation mutants of maize (Zea mays L.) Front Plant Sci 5:314PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Kato N, Lam E (2003) Chromatin of endoreduplicated pavement cells has greater range of movement than that of diploid guard cells in Arabidopsis thaliana. J Cell Sci 116(Pt 11):2195–2201PubMedCrossRefGoogle Scholar
  56. 56.
    Lindhout BI, Meckel T, van der Zaal BJ (2010) Zinc finger-mediated live cell imaging in Arabidopsis roots. Methods Mol Biol 649:383–398PubMedCrossRefGoogle Scholar
  57. 57.
    Aki SS, Umeda M (2016) Cytrap marker systems for in vivo visualization of cell cycle progression in Arabidopsis. In: Caillaud M-C (ed) Plant cell division: methods and protocols. Springer, New York, NY, pp 51–57. doi: 10.1007/978-1-4939-3142-2_4 CrossRefGoogle Scholar
  58. 58.
    Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17(12):1032–1037PubMedCrossRefGoogle Scholar
  59. 59.
    Ingouff M, Selles B, Michaud C, Vu TM, Berger F, Schorn AJ, Autran D, Van Durme M, Nowack MK, Martienssen RA, Grimanelli D (2017) Live-cell analysis of DNA methylation during sexual reproduction in Arabidopsis reveals context and sex-specific dynamics controlled by noncanonical RdDM. Genes Dev 31(1):72–83PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Rosa S (2017) Measuring dynamics of histone proteins by photobleaching in Arabidopsis roots. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_26 Google Scholar
  61. 61.
    Padilla-Parra S, Auduge N, Coppey-Moisan M, Tramier M (2008) Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells. Biophys J 95(6):2976–2988PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Molitor AM, Bu Z, Yu Y, Shen WH (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10(1):e1004091PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D, Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H, Raffaele S, Berthome R, Coute Y, Parker JE, Deslandes L (2015) A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161(5):1074–1088PubMedCrossRefGoogle Scholar
  64. 64.
    Ramirez-Garces D, Camborde L, Pel MJ, Jauneau A, Martinez Y, Neant I, Leclerc C, Moreau M, Dumas B, Gaulin E (2016) CRN13 candidate effectors from plant and animal eukaryotic pathogens are DNA-binding proteins which trigger host DNA damage response. New Phytol 210(2):602–617PubMedCrossRefGoogle Scholar
  65. 65.
    Tonaco IA, Borst JW, de Vries SC, Angenent GC, Immink RG (2006) In vivo imaging of MADS-box transcription factor interactions. J Exp Bot 57(1):33–42PubMedCrossRefGoogle Scholar
  66. 66.
    Lleres D, James J, Swift S, Norman DG, Lamond AI (2009) Quantitative analysis of chromatin compaction in living cells using FLIM-FRET. J Cell Biol 187(4):481–496PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Lleres D, Bailly AP, Perrin A, Norman DG, Xirodimas DP, Feil R (2017) Quantitative FLIM-FRET microscopy to monitor nanoscale chromatin compaction in vivo reveals structural roles of condensin complexes. Cell Rep 18(7):1791–1803PubMedCrossRefGoogle Scholar
  68. 68.
    Lorenz M (2009) Visualizing protein-RNA interactions inside cells by fluorescence resonance energy transfer. RNA 15(1):97–103PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Cremazy FG, Manders EM, Bastiaens PI, Kramer G, Hager GL, van Munster EB, Verschure PJ, Gadella TJ Jr, van Driel R (2005) Imaging in situ protein-DNA interactions in the cell nucleus using FRET-FLIM. Exp Cell Res 309(2):390–396PubMedCrossRefGoogle Scholar
  70. 70.
    Stelzer EH (2015) Light-sheet fluorescence microscopy for quantitative biology. Nat Methods 12(1):23–26PubMedCrossRefGoogle Scholar
  71. 71.
    von Wangenheim D, Daum G, Lohmann JU, Stelzer EK, Maizel A (2014) Live imaging of Arabidopsis development. Methods Mol Biol 1062:539–550CrossRefGoogle Scholar
  72. 72.
    Ovecka M, Vaskebova L, Komis G, Luptovciak I, Smertenko A, Samaj J (2015) Preparation of plants for developmental and cellular imaging by light-sheet microscopy. Nat Protoc 10(8):1234–1247PubMedCrossRefGoogle Scholar
  73. 73.
    de Luis Balaguer MA, Ramos-Pezzotti M, Rahhal MB, Melvin CE, Johannes E, Horn TJ, Sozzani R (2016) Multi-sample Arabidopsis growth and imaging chamber (MAGIC) for long term imaging in the ZEISS Lightsheet Z.1. Dev Biol 419(1):19–25PubMedCrossRefGoogle Scholar
  74. 74.
    Meinert T, Tietz O, Palme KJ, Rohrbach A (2016) Separation of ballistic and diffusive fluorescence photons in confocal Light-Sheet Microscopy of Arabidopsis roots. Sci Rep 6:30378PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Royer LA, Lemon WC, Chhetri RK, Wan Y, Coleman M, Myers EW, Keller PJ (2016) Adaptive light-sheet microscopy for long-term, high-resolution imaging in living organisms. Nat Biotechnol 34(12):1267–1278PubMedCrossRefGoogle Scholar
  76. 76.
    Gualda E, Moreno N, Tomancak P, Martins GG (2014) Going “open” with mesoscopy: a new dimension on multi-view imaging. Protoplasma 251(2):363–372PubMedCrossRefGoogle Scholar
  77. 77.
    Sena G, Frentz Z, Birnbaum KD, Leibler S (2011) Quantitation of cellular dynamics in growing Arabidopsis roots with light sheet microscopy. PLoS One 6(6):e21303PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Novak D, Kucharova A, Ovecka M, Komis G, Samaj J (2015) Developmental nuclear localization and quantification of GFP-tagged EB1c in Arabidopsis root using light-sheet microscopy. Front Plant Sci 6:1187PubMedGoogle Scholar
  79. 79.
    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(2):377–385PubMedCrossRefGoogle Scholar
  80. 80.
    Berson T, von Wangenheim D, Takac T, Samajova O, Rosero A, Ovecka M, Komis G, Stelzer EH, Samaj J (2014) Trans-Golgi network localized small GTPase RabA1d is involved in cell plate formation and oscillatory root hair growth. BMC Plant Biol 14:252PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Preibisch S, Saalfeld S, Schindelin J, Tomancak P (2010) Software for bead-based registration of selective plane illumination microscopy data. Nat Methods 7(6):418–419PubMedCrossRefGoogle Scholar
  82. 82.
    Rego EH, Shao L, Macklin JJ, Winoto L, Johansson GA, Kamps-Hughes N, Davidson MW, Gustafsson MG (2012) Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution. Proc Natl Acad Sci U S A 109(3):E135–E143PubMedCrossRefGoogle Scholar
  83. 83.
    Schermelleh L, Heintzmann R, Leonhardt H (2010) A guide to super-resolution fluorescence microscopy. J Cell Biol 190(2):165–175PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Ball G, Parton RM, Hamilton RS, Davis I (2012) A cell biologist’s guide to high resolution imaging. Methods Enzymol 504:29–55PubMedCrossRefGoogle Scholar
  85. 85.
    Agrawal U, Reilly DT, Schroeder CM (2013) Zooming in on biological processes with fluorescence nanoscopy. Curr Opin Biotechnol 24(4):646–653PubMedCrossRefGoogle Scholar
  86. 86.
    Allen JR, Ross ST, Davidson MW (2014) Structured illumination microscopy for superresolution. ChemPhysChem 15(4):566–576PubMedCrossRefGoogle Scholar
  87. 87.
    Komis G, Samajova O, Ovecka M, Samaj J (2015) Super-resolution microscopy in plant cell imaging. Trends Plant Sci 20(12):834–843PubMedCrossRefGoogle Scholar
  88. 88.
    Nienhaus K, Nienhaus GU (2016) Where do we stand with super-resolution optical microscopy? J Mol Biol 428(2 Pt A):308–322PubMedCrossRefGoogle Scholar
  89. 89.
    Coltharp C, Xiao J (2012) Superresolution microscopy for microbiology. Cell Microbiol 14(12):1808–1818PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Dame RT, Tark-Dame M (2016) Bacterial chromatin: converging views at different scales. Curr Opin Cell Biol 40:60–65PubMedCrossRefGoogle Scholar
  91. 91.
    Fornasiero EF, Opazo F (2015) Super-resolution imaging for cell biologists: concepts, applications, current challenges and developments. Bioessays 37(4):436–451PubMedCrossRefGoogle Scholar
  92. 92.
    Schubert V (2017) Super-resolution microscopy - applications in plant cell research. Front Plant Sci 8:531PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Markaki Y, Smeets D, Fiedler S, Schmid VJ, Schermelleh L, Cremer T, Cremer M (2012) The potential of 3D-FISH and super-resolution structured illumination microscopy for studies of 3D nuclear architecture. Bioessays 34(5):412–426PubMedCrossRefGoogle Scholar
  94. 94.
    Markaki Y, Gunkel M, Schermelleh L, Beichmanis S, Neumann J, Heidemann M, Leonhardt H, Eick D, Cremer C, Cremer T (2010) Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Cold Spring Harb Symp Quant Biol 75:475–492PubMedCrossRefGoogle Scholar
  95. 95.
    Schubert V (2014) RNA polymerase II forms transcription networks in rye and Arabidopsis nuclei and its amount increases with endopolyploidy. Cytogenet Genome Res 143(1-3):69–77PubMedCrossRefGoogle Scholar
  96. 96.
    Schubert V, Lermontova I, Schubert I (2013) The Arabidopsis CAP-D proteins are required for correct chromatin organisation, growth and fertility. Chromosoma 122(6):517–533PubMedCrossRefGoogle Scholar
  97. 97.
    Ma W, Gabriel TS, Martis MM, Gursinsky T, Schubert V, Vrana J, Dolezel J, Grundlach H, Altschmied L, Scholz U, Himmelbach A, Behrens SE, Banaei-Moghaddam AM, Houben A (2016) Rye B chromosomes encode a functional Argonaute-like protein with in vitro slicer activities similar to its A chromosome paralog. New Phytol 213(2):916–928PubMedCrossRefGoogle Scholar
  98. 98.
    Zakrzewski F, Schubert V, Viehoever P, Minoche AE, Dohm JC, Himmelbauer H, Weisshaar B, Schmidt T (2014) The CHH motif in sugar beet satellite DNA: a modulator for cytosine methylation. Plant J 78(6):937–950PubMedCrossRefGoogle Scholar
  99. 99.
    Ishii T, Karimi-Ashtiyani R, Banaei-Moghaddam AM, Schubert V, Fuchs J, Houben A (2015) The differential loading of two barley CENH3 variants into distinct centromeric substructures is cell type- and development-specific. Chromosome Res 23(2):277–284PubMedCrossRefGoogle Scholar
  100. 100.
    Demidov D, Schubert V, Kumke K, Weiss O, Karimi-Ashtiyani R, Buttlar J, Heckmann S, Wanner G, Dong Q, Han F, Houben A (2014) Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenet Genome Res 143(1-3):150–156PubMedCrossRefGoogle Scholar
  101. 101.
    Neumann P, Schubert V, Fukova I, Manning JE, Houben A, Macas J (2016) Epigenetic histone marks of extended meta-polycentric centromeres of Lathyrus and Pisum chromosomes. Front Plant Sci 7:234PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Weisshart K, Fuchs J, Schubert V (2016) Structured illumination microscopy (SIM) and photoactivated localization microscopy (PALM) to analyze the abundance and distribution of RNA polymerase II molecules in flow-sorted Arabidopsis nuclei. Bio Protocol 6(3): e1725. http://wwwbio-protocolorg/e1725Google Scholar
  103. 103.
    Heckmann S, Macas J, Kumke K, Fuchs J, Schubert V, Ma L, Novak P, Neumann P, Taudien S, Platzer M, Houben A (2013) The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J 73(4):555–565PubMedCrossRefGoogle Scholar
  104. 104.
    Marques A, Ribeiro T, Neumann P, Macas J, Novak P, Schubert V, Pellino M, Fuchs J, Ma W, Kuhlmann M, Brandt R, Vanzela AL, Beseda T, Simkova H, Pedrosa-Harand A, Houben A (2015) Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. Proc Natl Acad Sci USA 112(44):13633–13638PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Ribeiro SA, Vagnarelli P, Dong Y, Hori T, McEwen BF, Fukagawa T, Flors C, Earnshaw WC (2010) A super-resolution map of the vertebrate kinetochore. Proc Natl Acad Sci USA 107(23):10484–10489PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Dürr J, Lolas IB, Sorensen BB, Schubert V, Houben A, Melzer M, Deutzmann R, Grasser M, Grasser KD (2014) The transcript elongation factor SPT4/SPT5 is involved in auxin-related gene expression in Arabidopsis. Nucleic Acids Res 42(7):4332–4347PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Antosz W, Pfab A, Ehrnsberger H, Holzinger H, Köllen K, Mortensen S, Bruckmann A, Schubert T, Längst G, Griesenbeck J, Schubert V, Grasser M, Grasser K (2017) Composition of the Arabidopsis RNA polymerase II transcript elongation complex reveals interplay of elongation and mRNA processing factors. Plant Cell 29(4):854–870PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Marques A, Schubert V, Houben A, Pedrosa-Harand A (2016) Restructuring of holocentric centromeres during meiosis in the plant Rhynchospora pubera. Genetics 204(2):555–568PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Schubert V, Ruban A, Houben A (2016) Chromatin ring formation at plant centromeres. Front Plant Sci 7:28PubMedPubMedCentralGoogle Scholar
  110. 110.
    Schubert V, Zelkowski M, Klemme S, Houben A (2016) Similar sister chromatid arrangement in mono- and holocentric plant chromosomes. Cytogenet Genome Res 149(3):218–225PubMedCrossRefGoogle Scholar
  111. 111.
    Ball G, Demmerle J, Kaufmann R, Davis I, Dobbie IM, Schermelleh L (2015) SIMcheck: a toolbox for successful super-resolution structured illumination microscopy. Sci Rep 5:15915PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Schubert V, Weisshart K (2015) Abundance and distribution of RNA polymerase II in Arabidopsis interphase nuclei. J Exp Bot 66(6):1687–1698PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X (2011) Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat Methods 8(12):1027–1036PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Fernandez-Suarez M, Ting AY (2008) Fluorescent probes for super-resolution imaging in living cells. Nat Rev Mol Cell Biol 9(12):929–943PubMedCrossRefGoogle Scholar
  115. 115.
    Hedde PN, Nienhaus GU (2014) Super-resolution localization microscopy with photoactivatable fluorescent marker proteins. Protoplasma 251(2):349–362PubMedCrossRefGoogle Scholar
  116. 116.
    Olivier N, Keller D, Gonczy P, Manley S (2013) Resolution doubling in 3D-STORM imaging through improved buffers. PLoS One 8(7):e69004PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Flors C (2013) Super-resolution fluorescence imaging of directly labelled DNA: from microscopy standards to living cells. J Microsc 251(1):1–4PubMedCrossRefGoogle Scholar
  118. 118.
    Flors C, Earnshaw WC (2011) Super-resolution fluorescence microscopy as a tool to study the nanoscale organization of chromosomes. Curr Opin Chem Biol 15(6):838–844PubMedCrossRefGoogle Scholar
  119. 119.
    Hamel V, Guichard P, Fournier M, Guiet R, Fluckiger I, Seitz A, Gonczy P (2014) Correlative multicolor 3D SIM and STORM microscopy. Biomed Opt Express 5(10):3326–3336PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Wurm CA, Kolmakov K, Göttfert F, Ta H, Bossi M, Schill H, Berning S, Jakobs S, Donnert G, Belov VN, Hell SW (2012) Novel red fluorophores with superior performance in STED microscopy. Optical Nanosc 1(1):7CrossRefGoogle Scholar
  121. 121.
    Wanner G, Schroeder-Reiter E (2008) Scanning electron microscopy of chromosomes. Methods Cell Biol 88:451PubMedCrossRefGoogle Scholar
  122. 122.
    Schubert I, Dolezel J, Houben A, Scherthan H, Wanner G (1993) Refined examination of plant metaphase chromosome structure at different levels made feasible by new isolation methods. Chromosoma 102(2):96–101CrossRefGoogle Scholar
  123. 123.
    Wanner G, Formanek H, Martin R, Herrmann RG (1991) High-resolution scanning electron-microscopy of plant chromosomes. Chromosoma 100(2):103–109CrossRefGoogle Scholar
  124. 124.
    Martin R, Busch W, Herrmann RG, Wanner G (1994) Efficient preparation of plant chromosomes for high-resolution scanning electron microscopy. Chromosome Res 2(5):411–415PubMedCrossRefGoogle Scholar
  125. 125.
    Iwano M, Che FS, Takayama S, Fukui K, Isogai A (2003) Three-dimensional architecture of ribosomal DNA within barley nucleoli revealed with electron microscopy. Scanning 25(5):257–263PubMedCrossRefGoogle Scholar
  126. 126.
    Jander G, Wendt H (1960) Lehrbuch der analytischen und präparativen anorganischen Chemie. Hirzel Verlag, LeipzigGoogle Scholar
  127. 127.
    Wanner G, Formanek H (1995) Imaging of DNA in human and plant chromosomes by high-resolution scanning electron microscopy. Chromosome Res 3(6):368–374PubMedCrossRefGoogle Scholar
  128. 128.
    Wanner G, Formanek H (2000) A new chromosome model. J Struct Biol 132(2):147–161PubMedCrossRefGoogle Scholar
  129. 129.
    Schroeder-Reiter E, Houben A, Wanner G (2003) Immunogold labeling of chromosomes for scanning electron microscopy: a closer look at phosphorylated histone H3 in mitotic metaphase chromosomes of Hordeum vulgare. Chromosome Res 11(6):585–596PubMedCrossRefGoogle Scholar
  130. 130.
    Schroeder-Reiter E, Perez-Willard F, Zeile U, Wanner G (2009) Focused ion beam (FIB) combined with high resolution scanning electron microscopy: a promising tool for 3D analysis of chromosome architecture. J Struct Biol 165(2):97–106PubMedCrossRefGoogle Scholar
  131. 131.
    Houben A, Schroeder-Reiter E, Nagaki K, Nasuda S, Wanner G, Murata M, Endo TR (2007) CENH3 interacts with the centromeric retrotransposon cereba and GC-rich satellites and locates to centromeric substructures in barley. Chromosoma 116(3):275–283PubMedCrossRefGoogle Scholar
  132. 132.
    Schroeder-Reiter E, Houben A, Grau J, Wanner G (2006) Characterization of a peg-like terminal NOR structure with light microscopy and high-resolution scanning electron microscopy. Chromosoma 115(1):50–59PubMedCrossRefGoogle Scholar
  133. 133.
    Schroeder-Reiter E, Sanei M, Houben A, Wanner G (2012) Current SEM techniques for de- and re-construction of centromeres to determine 3D CENH3 distribution in barley mitotic chromosomes. J Microsc 246(1):96–106PubMedCrossRefGoogle Scholar
  134. 134.
    Neumann P, Navratilova A, Schroeder-Reiter E, Koblizkova A, Steinbauerova V, Chocholova E, Novak P, Wanner G, Macas J (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet 8(6):e1002777PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Wanner G, Schroeder-Reiter E, Formanek H (2005) 3D analysis of chromosome architecture: advantages and limitations with SEM. Cytogenet Genome Res 109(1-3):70–78PubMedCrossRefGoogle Scholar
  136. 136.
    Zoller JF, Herrmann RG, Wanner G (2004) Chromosome condensation in mitosis and meiosis of rye (Secale cereale L.) Cytogenet Genome Res 105(1):134–144PubMedCrossRefGoogle Scholar
  137. 137.
    Zoller JF, Hohmann U, Herrmann RG, Wanner G (2004) Ultrastructural analysis of chromatin in meiosis I + II of rye (Secale cereale L.) Cytogenet Genome Res 105(1):145–156PubMedCrossRefGoogle Scholar
  138. 138.
    Heckmann S, Schroeder-Reiter E, Kumke K, Ma L, Nagaki K, Murata M, Wanner G, Houben A (2011) Holocentric chromosomes of Luzula elegans are characterized by a longitudinal centromere groove, chromosome bending, and a terminal nucleolus organizer region. Cytogenet Genome Res 134(3):220–228PubMedCrossRefGoogle Scholar
  139. 139.
    Schroeder-Reiter E, Wanner G (2009) Chromosome centromeres: structural and analytical investigations with high resolution scanning electron microscopy in combination with focused ion beam milling. Cytogenet Genome Res 124(3-4):239–250PubMedCrossRefGoogle Scholar
  140. 140.
    Dwiranti A, Lin L, Mochizuki E, Kuwabata S, Takaoka A, Uchiyama S, Fukui K (2012) Chromosome observation by scanning electron microscopy using ionic liquid. Microsc Res Tech 75(8):1113–1118PubMedCrossRefGoogle Scholar
  141. 141.
    Hamano T, Dwiranti A, Kaneyoshi K, Fukuda S, Kometani R, Nakao M, Takata H, Uchiyama S, Ohmido N, Fukui K (2014) Chromosome interior observation by focused ion beam/scanning electron microscopy (FIB/SEM) using ionic liquid technique. Microsc Microanal 20(5):1340–1347PubMedCrossRefGoogle Scholar
  142. 142.
    Houben A, Demidov D, Rutten T, Scheidtmann KH (2005) Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells. Cytogenet Genome Res 109(1-3):148–155PubMedCrossRefGoogle Scholar
  143. 143.
    Cherkezyan L, Stypula-Cyrus Y, Subramanian H, White C, Dela Cruz M, Wali RK, Goldberg MJ, Bianchi LK, Roy HK, Backman V (2014) Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study. BMC Cancer 14:189PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Fabrice TN, Cherkezeyan L, Ringli C, Baroux C (2017) Transmission electron microscopy imaging to analyse chromatin density distribution at the nanoscale level. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols, Methods in molecular biology. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_34 Google Scholar
  145. 145.
    Meijering E, Carpenter AE, Peng H, Hamprecht FA, Olivo-Marin JC (2016) Imagining the future of bioimage analysis. Nat Biotechnol 34(12):1250–1255PubMedCrossRefGoogle Scholar
  146. 146.
    Haider SA, Cameron A, Siva P, Lui D, Shafiee MJ, Boroomand A, Haider N, Wong A (2016) Fluorescence microscopy image noise reduction using a stochastically-connected random field model. Sci Rep 6:20640PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Pavlova P, Tessadori F, de Jong HJ, Fransz P (2010) Immunocytological analysis of chromatin in isolated nuclei. Methods Mol Biol 655:413–432PubMedCrossRefGoogle Scholar
  148. 148.
    Fransz P, ten Hoopen R, Tessadori F (2006) Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14(1):71–82PubMedCrossRefGoogle Scholar
  149. 149.
    van Zanten M, Tessadori F, Peeters AJ, Fransz P (2012) Shedding light on large-scale chromatin reorganization in Arabidopsis thaliana. Mol Plant 5(3):583–590PubMedCrossRefGoogle Scholar
  150. 150.
    Fransz PF, de Jong JH (2002) Chromatin dynamics in plants. Curr Opin Plant Biol 5(6):560–567PubMedCrossRefGoogle Scholar
  151. 151.
    Almassalha LM, Tiwari A, Ruhoff PT, Stypula-Cyrus Y, Cherkezyan L, Matsuda H, Dela Cruz MA, Chandler JE, White C, Maneval C, Subramanian H, Szleifer I, Roy HK, Backman V (2017) The global relationship between chromatin physical topology, fractal structure, and gene expression. Sci Rep 7:41061PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Ricci MA, Manzo C, Garcia-Parajo MF, Lakadamyali M, Cosma MP (2015) Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160(6):1145–1158PubMedCrossRefGoogle Scholar
  153. 153.
    Chytilova E, Macas J, Sliwinska E, Rafelski SM, Lambert GM, Galbraith DW (2000) Nuclear dynamics in Arabidopsis thaliana. Mol Biol Cell 11(8):2733–2741PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Higa T, Suetsugu N, Wada M (2014) Plant nuclear photorelocation movement. J Exp Bot 65(11):2873–2881PubMedCrossRefGoogle Scholar
  155. 155.
    Qiu M, Yang G (2013) Drift correction for fluorescence live cell imaging through correlated motion identification. In: 10th Intern Symp Biomed Imaging, 7–11 April 2013. pp 452–455. doi:10.1109/ISBI.2013.6556509Google Scholar
  156. 156.
    Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682PubMedCrossRefGoogle Scholar
  157. 157.
    Van Bruaene N, Joss G, Thas O, Van Oostveldt P (2003) Four-dimensional imaging and computer-assisted track analysis of nuclear migration in root hairs of Arabidopsis thaliana. J Microsc 211(Pt 2):167–178PubMedCrossRefGoogle Scholar
  158. 158.
    Uchida S (2013) Image processing and recognition for biological images. Dev Growth Differ 55(4):523–549PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Poulet A, Duc C, Voisin M, Desset S, Tutois S, Vanrobays E, Benoit M, Evans DE, Probst AV, Tatout C (2017) The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants. J Cell Sci 130(3):590–601PubMedCrossRefGoogle Scholar
  160. 160.
  161. 161.
    Faure E, Savy T, Rizzi B, Melani C, Stasova O, Fabreges D, Spir R, Hammons M, Cunderlik R, Recher G, Lombardot B, Duloquin L, Colin I, Kollar J, Desnoulez S, Affaticati P, Maury B, Boyreau A, Nief JY, Calvat P, Vernier P, Frain M, Lutfalla G, Kergosien Y, Suret P, Remesikova M, Doursat R, Sarti A, Mikula K, Peyrieras N, Bourgine P (2016) A workflow to process 3D+time microscopy images of developing organisms and reconstruct their cell lineage. Nat Commun 7:8674PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Amat F, Lemon W, Mossing DP, McDole K, Wan Y, Branson K, Myers EW, Keller PJ (2014) Fast, accurate reconstruction of cell lineages from large-scale fluorescence microscopy data. Nat Methods 11(9):951–958PubMedCrossRefGoogle Scholar
  163. 163.
    Fernandez R, Das P, Mirabet V, Moscardi E, Traas J, Verdeil JL, Malandain G, Godin C (2010) Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution. Nat Methods 7(7):547–553PubMedCrossRefGoogle Scholar
  164. 164.
    Bassel GW, Smith RS (2016) Quantifying morphogenesis in plants in 4D. Curr Opin Plant Biol 29:87–94PubMedCrossRefGoogle Scholar
  165. 165.
    Chalut KJ, Ekpenyong AE, Clegg WL, Melhuish IC, Guck J (2012) Quantifying cellular differentiation by physical phenotype using digital holographic microscopy. Integrat Biol 4(3):280–284CrossRefGoogle Scholar
  166. 166.
    Kus A, Dudek M, Kemper B, Kujawinska M, Vollmer A (2014) Tomographic phase microscopy of living three-dimensional cell cultures. J Biomed Opt 19(4):046009PubMedCrossRefGoogle Scholar
  167. 167.
    Cherkezyan L, Zhang D, Subramanian H, Taflove A, Backman V (2016) Reconstruction of explicit structural properties at the nanoscale via spectroscopic microscopy. J Biomed Opt 21(2):025007–025007PubMedCentralCrossRefGoogle Scholar
  168. 168.
    Shachar S, Voss TC, Pegoraro G, Sciascia N, Misteli T (2015) Identification of gene positioning factors using high-throughput imaging mapping. Cell 162(4):911–923PubMedPubMedCentralCrossRefGoogle Scholar
  169. 169.
    Lindhout BI, Fransz P, Tessadori F, Meckel T, Hooykaas PJ, van der Zaal BJ (2007) Live cell imaging of repetitive DNA sequences via GFP-tagged polydactyl zinc finger proteins. Nucleic Acids Res 35(16):e107PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Fujimoto S, Sugano SS, Kuwata K, Osakabe K, Matsunaga S (2016) Visualization of specific repetitive genomic sequences with fluorescent TALEs in Arabidopsis thaliana. J Exp Bot 67(21):6101–6110PubMedPubMedCentralCrossRefGoogle Scholar
  171. 171.
    Ma H, Naseri A, Reyes-Gutierrez P, Wolfe SA, Zhang S, Pederson T (2015) Multicolor CRISPR labeling of chromosomal loci in human cells. Proc Natl Acad Sci USA 112(10):3002–3007PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Dreissig S, Schiml S, Schindele P, Weiss O, Rutten T, Schubert V, Gladilin E, Mette M, Puchta H, Houben A (2017) Live cell CRISPR-imaging in plants reveals dynamic telomere movements. Plant J. doi: 10.1111/tpj.13601
  173. 173.
    Pawley JB (2013) Handbook of biological confocal microscopy. Springer, New York, NYGoogle Scholar
  174. 174.
    Wilson T, Tan JB (1993) Three dimensional image reconstruction in conventional and confocal microscopy. Bioimaging 1(3):176–184CrossRefGoogle Scholar
  175. 175.
    Tokunaga M, Imamoto N, Sakata-Sogawa K (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 5(2):159–161PubMedCrossRefGoogle Scholar
  176. 176.
    Beier HT, Ibey BL (2014) Experimental comparison of the high-speed imaging performance of an EM-CCD and sCMOS camera in a dynamic live-cell imaging test case. PLoS One 9(1):e84614PubMedPubMedCentralCrossRefGoogle Scholar
  177. 177.
    Zemach A, Li Y, Wayburn B, Ben-Meir H, Kiss V, Avivi Y, Kalchenko V, Jacobsen SE, Grafi G (2005) DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17(5):1549–1558PubMedPubMedCentralCrossRefGoogle Scholar
  178. 178.
    Libault M, Tessadori F, Germann S, Snijder B, Fransz P, Gaudin V (2005) The Arabidopsis LHP1 protein is a component of euchromatin. Planta 222(5):910–925PubMedCrossRefGoogle Scholar
  179. 179.
    Koroleva OA, Calder G, Pendle AF, Kim SH, Lewandowska D, Simpson CG, Jones IM, Brown JW, Shaw PJ (2009) Dynamic behavior of Arabidopsis eIF4A-III, putative core protein of exon junction complex: fast relocation to nucleolus and splicing speckles under hypoxia. Plant Cell 21(5):1592–1606PubMedPubMedCentralCrossRefGoogle Scholar
  180. 180.
    Yu X, Sayegh R, Maymon M, Warpeha K, Klejnot J, Yang H, Huang J, Lee J, Kaufman L, Lin C (2009) Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation. Plant Cell 21(1):118–130PubMedPubMedCentralCrossRefGoogle Scholar
  181. 181.
    Dittmer TA, Stacey NJ, Sugimoto-Shirasu K, Richards EJ (2007) LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. Plant Cell 19(9):2793–2803PubMedPubMedCentralCrossRefGoogle Scholar
  182. 182.
    Guggisberg A, Baroux C, Grossniklaus U, Conti E (2008) Genomic origin and organization of the allopolyploid Primula egaliksensis investigated by in situ hybridization. Ann Bot 101(7):919–927PubMedPubMedCentralCrossRefGoogle Scholar
  183. 183.
    Wanner G, Schroeder-Reiter E, Ma W, Houben A, Schubert V (2015) The ultrastructure of mono- and holocentric plant centromeres: an immunological investigation by structured illumination microscopy and scanning electron microscopy. Chromosoma 124(4):503–517PubMedCrossRefGoogle Scholar
  184. 184.
    Baroux C, Pecinka A, Fuchs J, Schubert I, Grossniklaus U (2007) The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19(6):1782–1794PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Käthner R, Zölffel M (2016) Light microscopy - technology and application. Süddeutscher Verlag onpact GmbH, MunichGoogle Scholar
  186. 186.
    Becker W, Su B, Holub O, Weisshart K (2011) FLIM and FCS detection in laser-scanning microscopes: increased efficiency by GaAsP hybrid detectors. Microsc Res Tech 74(9):804–811PubMedGoogle Scholar
  187. 187.
    Feijo JA, Moreno N (2004) Imaging plant cells by two-photon excitation. Protoplasma 223(1):1–32PubMedCrossRefGoogle Scholar
  188. 188.
    Benninger RK, Piston DW (2013) Two-photon excitation microscopy for the study of living cells and tissues. Curr Protoc Cell Biol. Chapter 4:Unit 4 11 11–24Google Scholar
  189. 189.
    Weber M, Huisken J (2011) Light sheet microscopy for real-time developmental biology. Curr Opin Genet Dev 21(5):566–572PubMedCrossRefGoogle Scholar
  190. 190.
    Power RM, Huisken J (2017) A guide to light-sheet fluorescence microscopy for multiscale imaging. Nat Methods 14(4):360–373PubMedCrossRefGoogle Scholar
  191. 191.
    Abbe E (1873) Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Arch Mikrosk Anat 9(1):413–468CrossRefGoogle Scholar
  192. 192.
    Rayleigh L (1896) On the theory of optical images, with special reference to the microscope. Philos Mag 42:167–195CrossRefGoogle Scholar
  193. 193.
    Van Noorden R (2014) Insider view of cells scoops Nobel. Nature 514(7522):286PubMedCrossRefGoogle Scholar
  194. 194.
    Erni R, Rossell MD, Kisielowski C, Dahmen U (2009) Atomic-resolution imaging with a sub-50-pm electron probe. Phys Rev Lett 102(9):096101PubMedCrossRefGoogle Scholar
  195. 195.
    Lobet G, Draye X, Perilleux C (2013) An online database for plant image analysis software tools. Plant Methods 9(1):38PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675PubMedPubMedCentralCrossRefGoogle Scholar
  197. 197.
    Wan Y, Otsuna H, Chien C-B, Hansen C (2012) FluoRender: an application of 2D image space methods for 3D and 4D confocal microscopy data visualization in neurobiology research. IEEE Pacific Visualization Symposium [proceedings], pp 201–208Google Scholar
  198. 198.
    Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7(10):R100PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2018

Authors and Affiliations

  1. 1.Department of Plant and Microbial Biology, Zürich-Basel Plant Science CenterUniversity of ZürichZürichSwitzerland
  2. 2.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) GaterslebenSeelandGermany

Personalised recommendations

Cite protocol