Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Multiscale imaging of plant development by light-sheet fluorescence microscopy

Nature Plants volume 4, pages 639–650 (2018)Cite this article

Subjects

Abstract

Light-sheet fluorescence microscopy (LSFM) methods collectively represent the major breakthrough in developmental bio-imaging of living multicellular organisms. They are becoming a mainstream approach through the development of both commercial and custom-made LSFM platforms that are adjusted to diverse biological applications. Based on high-speed acquisition rates under conditions of low light exposure and minimal photo-damage of the biological sample, these methods provide ideal means for long-term and in-depth data acquisition during organ imaging at single-cell resolution. The introduction of LSFM methods into biology extended our understanding of pattern formation and developmental progress of multicellular organisms from embryogenesis to adult body. Moreover, LSFM imaging allowed the dynamic visualization of biological processes under almost natural conditions. Here, we review the most important, recent biological applications of LSFM methods in developmental studies of established and emerging plant model species, together with up-to-date methods of data editing and evaluation for modelling of complex biological processes. Recent applications in animal models push LSFM into the forefront of current bio-imaging approaches. Since LSFM is now the single most effective method for fast imaging of multicellular organisms, allowing quantitative analyses of their long-term development, its broader use in plant developmental biology will likely bring new insights.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Flexible long-term developmental imaging of plants (such as A. thaliana and M. sativa) using LSFM.
Fig. 2: Imaging of subcellular compartments and physiological cellular processes by LSFM.
Fig. 3: LSFM from multiple angles improves radial imaging.

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

References

  1. Gualda, E., Moreno, N., Tomancak, P. & Martins, G. G. Going “open” with Mesoscopy: a new dimension on multi-view imaging. Protoplasma 251, 363–372 (2014).

    Article  PubMed  Google Scholar 

  2. Reynaud, I. E., Peychl, J., Huisken, J. & Tomancak, P. Guide to light-sheet microscopy for adventurous biologists. Nat. Methods 12, 30–34 (2015).

    Article  PubMed  CAS  Google Scholar 

  3. Stelzer, E. H. K. Light-sheet fluorescence microscopy for quantitative biology. Nat. Methods 12, 23–26 (2015).

    Article  PubMed  CAS  Google Scholar 

  4. Weber, M. & Huisken, J. Light sheet microscopy for real-time developmental biology. Curr. Opin. Genet. Dev. 21, 566–572 (2011).

    Article  PubMed  CAS  Google Scholar 

  5. Huisken, J., Swoger, J., Del Bene, F., Wittbrodt, J. & Stelzer, E. H. K. Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007–1009 (2004).

    Article  PubMed  CAS  Google Scholar 

  6. Keller, P. J., Schmidt, A. D., Wittbrodt, J. & Stelzer, E. H. K. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322, 1065–1069 (2008).

    Article  PubMed  CAS  Google Scholar 

  7. Berthet, B. & Maizel, A. Light sheet microscopy and live imaging of plants. J. Microsc. 263, 158–164 (2016).

    Article  PubMed  CAS  Google Scholar 

  8. Power, R. M. & Huisken, J. A guide to light-sheet fluorescence microscopy for multiscale imaging. Nat. Methods 14, 360–373 (2017).

    Article  PubMed  CAS  Google Scholar 

  9. Zagato, E. et al. Technical implementations of light sheet microscopy. Microsc. Res. Tech. https://doi.org/10.1002/jemt.22981 (2018).

    Article  Google Scholar 

  10. Girkin, J. M. & Carvalho, M. T. The light-sheet microscopy revolution. J. Opt. 20, 053002 (2018).

    Article  Google Scholar 

  11. Keller, P. J. & Stelzer, E. H. K. Quantitative in vivo imaging of entire embryos with Digital Scanned Laser Light Sheet Fluorescence Microscopy. Curr. Opin. Neurobiol. 18, 624–632 (2008).

    Article  PubMed  CAS  Google Scholar 

  12. Icha, J., Weber, M., Waters, J. C. & Norden, C. Phototoxicity in live fluorescence microscopy, and how to avoid it. Bioessays 39, 1700003 (2017).

    Article  Google Scholar 

  13. Laissue, P. P., Alghamdi, R. A., Tomancak, P., Reynaud, I. E. & Shroff, H. Assessing phototoxicity in live fluorescence imaging. Nat Methods 14, 657–661 (2017).

    Article  PubMed  CAS  Google Scholar 

  14. Capua, Y. & Eshed, Y. Coordination of auxin-triggered leaf initiation by tomato LEAFLESS. Proc. Natl Acad. Sci. USA 114, 3246–3251 (2017).

    Article  PubMed  CAS  Google Scholar 

  15. von Wangenheim, D. et al. Rules and self-organizing properties of post-embryonic plant organ cell division patterns. Curr. Biol. 26, 1–11 (2016).

    Article  CAS  Google Scholar 

  16. Maizel, A., von Wangenheim, D., Federici, F., Haseloff, J. & Stelzer, E. H. K. High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J. 68, 377–385 (2011).

    Article  PubMed  CAS  Google Scholar 

  17. Komis, G. et al. Dynamics and organization of cortical microtubules as revealed by superresolution structured illumination microscopy. Plant Physiol. 165, 129–148 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Rieckher, M. et al. A customized light sheet microscope to measure spatio-temporal protein dynamics in small model organisms. PLoS ONE 10, e0127869 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Maioli, V. et al. Time-lapse 3D measurements of a glucose biosensor in multicellular spheroids by light sheet fluorescence microscopy in commercial 96-well plates. Sci. Rep. 6, 37777 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Candeo, A., Doccula, F. G., Valentini, G., Bassi, A. & Costa, A. Light sheet fluorescence microscopy quantifies calcium oscillations in root hairs of Arabidopsis thaliana. Plant Cell Physiol. 58, 1161–1172 (2017).

    Article  PubMed  CAS  Google Scholar 

  21. Capoulade, J., Wachsmuth, M., Hufnagel, L. & Knop, M. Quantitative fluorescence imaging of protein diffusion and interaction in living cells. Nat. Biotechnol. 29, 835–839 (2011).

    Article  PubMed  CAS  Google Scholar 

  22. De Luis Balaguer, M. A. et al. Multi-sample Arabidopsis growth and imaging chamber (MAGIC) for long term imaging in the ZEISS Lightsheet Z.1. Dev. Biol. 419, 19–25 (2016).

    Article  PubMed  CAS  Google Scholar 

  23. Liu, L. et al. High-throughput imaging of zebrafish embryos using a linear-CCD-based flow imaging system. Biomed. Opt. Express 8, 5651–5662 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Berson, T. et al. Trans-Golgi network localized small GTPase RabA1d is involved in cell plate formation and oscillatory root hair growth. BMC Plant Biol. 14, 252 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Yamashita, N. et al. Three-dimensional tracking of plus-tips by lattice light-sheet microscopy permits the quantification of microtubule growth trajectories within the mitotic apparatus. J. Biomed. Opt. 20, 101206 (2015).

    Article  PubMed  Google Scholar 

  26. Aguet, F. et al. Membrane dynamics of dividing cells imaged by lattice light-sheet microscopy. Mol. Biol. Cell 27, 3418–3435 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Gustavsson, A. K., Petrov, P. N., Lee, M. Y., Shechtman, Y. & Moerner, W. E. 3D single-molecule super-resolution microscopy with a tilted light sheet. Nat. Commun. 9, 123 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Keller, P. J. et al. Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nat. Methods 7, 637–642 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Krzic, U., Gunther, S., Saunders, T. E., Streichan, S. J. & Hufnagel, L. Multiview light-sheet microscope for rapid in toto imaging. Nat. Methods 9, 730–733 (2012).

    Article  PubMed  CAS  Google Scholar 

  30. Tomer, R., Khairy, K., Amat, F. & Keller, P. J. Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nat. Methods 9, 755–763 (2012).

    Article  PubMed  CAS  Google Scholar 

  31. Chhetri, R. K., Amat, F., Wan, Y., Höckendorf, B., Lemon, W. C. & Keller, P. J. Whole-animal functional and developmental imaging with isotropic spatial resolution. Nat. Methods 12, 1171–1178 (2015).

    Article  PubMed  CAS  Google Scholar 

  32. Ejsmont, R. K., Sarov, M., Winkler, S., Lipinski, K. A. & Tomancak, P. A toolkit for high-throughput, cross-species gene engineering in Drosophila. Nat. Methods 6, 435–437 (2009).

    Article  PubMed  CAS  Google Scholar 

  33. Sarov, M. et al. A genome-wide resource for the analysis of protein localisation in Drosophila. eLife 5, e12068 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Schmied, C., Stamataki, E. & Tomancak, P. Open-source solutions for SPIMage processing. Methods Cell Biol. 123, 505–529 (2014).

    Article  PubMed  Google Scholar 

  35. Schmied, C. & Tomancak, P. Sample preparation and mounting of Drosophila embryos for multiview light sheet microscopy. Methods Mol. Biol. 1478, 189–202 (2016).

    Article  PubMed  CAS  Google Scholar 

  36. Pitrone, P. G. et al. OpenSPIM: an open-access light-sheet microscopy platform. Nat. Methods 10, 598–599 (2013).

    Article  PubMed  CAS  Google Scholar 

  37. Gualda, E. J. et al. OpenSpinMicroscopy: an open-source integrated microscopy platform. Nat. Methods 10, 599–600 (2013).

    Article  PubMed  CAS  Google Scholar 

  38. Lemon, W. C. et al. Whole-central nervous system functional imaging in larval Drosophila. Nat. Commun. 6, 7924 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Chen, B. C. et al. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346, 1257998 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Mir, M. et al. Dense Bicoid hubs accentuate binding along the morphogen gradient. Genes Dev. 31, 1784–1794 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Gao, L. et al. Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens. Cell 151, 1370–1385 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Amat, F. et al. Efficient processing and analysis of large-scale light-sheet microscopy data. Nat. Protoc. 10, 1679–1696 (2015).

    Article  PubMed  CAS  Google Scholar 

  43. Lye, C. M. et al. Mechanical coupling between endoderm invagination and axis extension in Drosophila. PLoS Biol. 13, e1002292 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Streichan, S. J., Lefebvre, M. F., Noll, N., Wieschaus, E. F. & Shraiman, B. I. Quantification of myosin distribution predicts global morphogenetic flow in the fly embryo. Preprint at https://arxiv.org/abs/1701.07100 (2017).

  45. Strobl, F. & Stelzer, E. H. K. Non-invasive long-term fluorescence live imaging of Tribolium castaneum embryos. Development 141, 2331–2338 (2014).

    Article  PubMed  CAS  Google Scholar 

  46. Strobl, F., Schmitz, A. & Stelzer, E. H. K. Live imaging of Tribolium castaneum embryonic development using light-sheet-based fluorescence microscopy. Nat. Protoc. 10, 1486–1507 (2015).

    Article  PubMed  CAS  Google Scholar 

  47. Hilbrant, M., Horn, T., Koelzer, S. & Panfilio, K. A. The beetle amnion and serosa functionally interact as apposed epithelia. eLife 5, e13834 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Girstmair, J. et al. Light-sheet microscopy for everyone? experience of building an OpenSPIM to study flatworm development. BMC Dev. Biol. 16, 22 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wolff, C. et al. Multi-view light-sheet imaging and tracking with the MaMuT software reveals the cell lineage of a direct developing arthropod limb. eLife 7, e34410 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Wu, Y. et al. Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 108, 17708–17713 (2011).

    Article  PubMed  Google Scholar 

  51. Wu, Y. et al. Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy. Nat. Biotechnol. 31, 1032–1038 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Kumar, A. et al. Dual-view plane illumination microscopy for rapid and spatially isotropic imaging. Nat. Protoc. 9, 2555–2573 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Rieckher, M. et al. A customized light sheet microscope to measure spatio-temporal protein dynamics in small model organisms. PLoS ONE 10, e0127869 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Kaufmann, A., Mickoleit, M., Weber, M. & Huisken, J. Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope. Development 139, 3242–3247 (2012).

    Article  PubMed  CAS  Google Scholar 

  55. Schmid, B. et al. High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics. Nat. Commun. 4, 2207 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Jahr, W., Schmid, B., Schmied, C., Fahrbach, F. & Huisken, J. Hyperspectral light sheet microscopy. Nat. Commun. 6, 7990 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Bassi, A., Schmid, B. & Huisken, J. Optical tomography complements light sheet microscopy for in toto imaging of zebrafish development. Development 142, 1016–1020 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Lenard, A. et al. Endothelial cell self-fusion during vascular pruning. PLoS Biol. 13, e1002126 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Park, O. K. et al. 3D light-sheet fluorescence microscopy of cranial neurons and vasculature during sebrafish embryogenesis. Mol. Cells 38, 975–981 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Alvers, A. L., Ryan, S., Scherz, P. J., Huisken, J. & Bagnat, M. Single continuous lumen formation in the zebrafish gut is mediated by smoothened-dependent tissue remodeling. Development 141, 1110–1119 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Icha, J. et al. Using light sheet fluorescence microscopy to image zebrafish eye development. J. Vis. Exp. 110, e53966 (2016).

    Google Scholar 

  62. Beerman, R. W. et al. Direct in vivo manipulation and imaging of calcium transients in neutrophils identify a critical role for leading-edge calcium flux. Cell Rep. 13, 2107–2117 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Tomer, R. et al. SPED light sheet microscopy: fast mapping of biological system structure and function. Cell 163, 1796–1806 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Quirin, S. et al. Calcium imaging of neural circuits with extended depth-of-field light-sheet microscopy. Opt. Lett. 41, 855–858 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Arnaout, R. et al. Zebrafish model for human long QT syndrome. Proc. Natl Acad Sci. USA 104, 11316–11321 (2007).

    Article  PubMed  CAS  Google Scholar 

  66. Mickoleit, M. et al. High-resolution reconstruction of the beating zebrafish heart. Nat. Methods 11, 919–922 (2014).

    Article  PubMed  CAS  Google Scholar 

  67. Arrenberg, A. B., Stainier, D. Y., Baier, H. & Huisken, J. Optogenetic control of cardiac function. Science 330, 971–974 (2010).

    Article  PubMed  CAS  Google Scholar 

  68. Panier, T. et al. Fast functional imaging of multiple brain regions in intact zebrafish larvae using selective plane illumination microscopy. Front. Neural Circuits 7, 65 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ahrens, M. B., Orger, M. B., Robson, D. N., Li, J. M. & Keller, P. J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10, 413–420 (2013).

    Article  PubMed  CAS  Google Scholar 

  70. Xiao, Y. et al. High-resolution live imaging reveals axon-glia interactions during peripheral nerve injury and repair in zebrafish. Dis. Model. Mech. 8, 553–564 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Icha, J., Kunath, C., Rocha-Martins, M. & Norden, C. Independent modes of ganglion cell translocation ensure correct lamination of the zebrafish retina. J. Cell Biol. 215, 259–275 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Sidhaye, J. & Norden, C. Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis. eLife 6, e22689 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Ichikawa, T. et al. Live imaging of whole mouse embryos during gastrulation: migration analyses of epiblast and mesodermal cells. PLoS ONE 8, e64506 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Ichikawa, T. et al. Live imaging and quantitative analysis of gastrulation in mouse embryos using light-sheet microscopy and 3D tracking tools. Nat. Protoc. 9, 575–585 (2014).

    Article  PubMed  CAS  Google Scholar 

  75. Bouchard, M. B. et al. Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms. Nat. Photonics 9, 113–119 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Strnad, P. et al. Inverted light-sheet microscope for imaging mouse pre-implantation development. Nat. Methods 13, 139–142 (2016).

    Article  PubMed  CAS  Google Scholar 

  77. Ovečka, M. et al. Preparation of plants for developmental and cellular imaging by light-sheet microscopy. Nat. Protoc. 10, 1234–1247 (2015).

    Article  PubMed  CAS  Google Scholar 

  78. von Wangenheim, D., Hauschild, R. & Friml, J. Light sheet fluorescence microscopy of plant roots growing on the surface of a gel. J. Vis. Exp. 119, e55044 (2017).

    Google Scholar 

  79. Rosquete, M. R. et al. An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr. Biol. 23, 817–822 (2013).

    Article  PubMed  CAS  Google Scholar 

  80. Lucas, M. et al. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proc. Natl Acad. Sci. USA 110, 5229–5234 (2013).

    Article  PubMed  Google Scholar 

  81. Vermeer, J. E. et al. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343, 178–183 (2014).

    Article  PubMed  CAS  Google Scholar 

  82. Sena, G., Frentz, Z., Birnbaum, K. D. & Leibler, S. Quantitation of cellular dynamics in growing Arabidopsis roots with light sheet microscopy. PLoS ONE 6, e21303 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Novák, D., Kuchařová, A., Ovečka, M., Komis, G. & Šamaj, J. Developmental nuclear localization and quantification of GFP-tagged EB1c in Arabidopsis root using light-sheet microscopy. Front. Plant Sci. 6, 1187 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Vyplelová, P., Ovečka, M. & Šamaj, J. Alfalfa root growth rate correlates with progression of microtubules during mitosis and cytokinesis as revealed by environmental light-sheet microscopy. Front. Plant Sci. 8, 1870 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Meinert, T., Tietz, O., Palme, K. J. & Rohrbach, A. Separation of ballistic and diffusive fluorescence photons in confocal light-sheet microscopy of Arabidopsis roots. Sci. Rep. 6, 30378 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Silverberg, J. L. et al. 3D imaging and mechanical modeling of helical buckling in Medicago truncatula plant roots. Proc. Natl Acad. Sci. USA 109, 16794–16799 (2012).

    Article  PubMed  Google Scholar 

  87. Slattery, R. A., Grennan, A. K., Sivaguru, M., Sozzani, R. & Ort, D. R. Light sheet microscopy reveals more gradual light attenuation in light-green versus dark-green soybean leaves. J. Exp. Bot. 67, 4697–4709 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Lichtenberg, M., Trampe, E. C. K., Vogelmann, T. C. & Kühl, M. Light Sheet Microscopy Imaging of Light Absorption and Photosynthesis Distribution in Plant Tissue. Plant Physiol. 175, 721–733 (2017).

    PubMed  CAS  PubMed Central  Google Scholar 

  89. von Wangenheim, D. Long-term observation of Arabidopsis thaliana root growth under close-to-natural conditions using light sheet-based fluorescence microscopy. PhD thesis, Johann Wolfgang Goethe-Universität (2015).

  90. von Wangenheim, D. et al. Live imaging of Arabidopsis development. Methods Mol. Biol. 1062, 539–550 (2014).

    Article  Google Scholar 

  91. Baesso, P., Randall, R. S. & Sena, G. Light sheet fluorescence microscopy optimized for long-term imaging of Arabidopsis root development. Methods Mol. Biol. 1761, 145–163 (2018).

    Article  PubMed  Google Scholar 

  92. Costa, A., Candeo, A., Fieramonti, L., Valentini, G. & Bassi, A. Calcium dynamics in root cells of Arabidopsis thaliana visualized with selective plane illumination microscopy. PLoS ONE 8, e75646 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. De Col, V. et al. ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology. eLife 6, e26770 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  94. Smékalová, V. et al. Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation. New Phytol. 203, 1175–1193 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Royer, L. A. et al. ClearVolume: open-source live 3D visualization for light-sheet microscopy. Nat. Methods 12, 480–481 (2015).

    Article  PubMed  CAS  Google Scholar 

  96. von Wangenheim, D. et al. Live tracking of moving samples in confocal microscopy for vertically grown roots. eLife 6, e26792 (2017).

    Article  Google Scholar 

  97. Swoger, J., Verveer, P., Greger, K., Huisken, J. & Stelzer, E. H. K. Multi-view image fusion improves resolution in three-dimensional microscopy. Opt. Express 15, 8029–8042 (2007).

    Article  PubMed  Google Scholar 

  98. Preibisch, S., Saalfeld, S., Schindelin, J. & Tomancak, P. Software for bead-based registration of selective plane illumination microscopy data. Nat. Methods 7, 418–419 (2010).

    Article  PubMed  CAS  Google Scholar 

  99. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Article  PubMed  CAS  Google Scholar 

  100. Preibisch, S. et al. Efficient Bayesian-based multiview deconvolution. Nat. Methods 11, 645–648 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Janes, G. et al. Cellular patterning of Arabidopsis roots under low phosphate conditions. Front. Plant Sci. 9, 735 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Barbier de Reuille, P. et al. MorphoGraphX: A platform for quantifying morphogenesis in 4D. eLife 4, e05864 (2015).

    Article  PubMed Central  CAS  Google Scholar 

  103. Heemskerk, I. & Streichan, S. J. Tissue cartography: compressing bio-image data by dimensional reduction. Nat. Methods 12, 1139–1142 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Schmied, C., Steinbach, P., Pietzsch, T., Preibisch, S. & Tomancak, P. An automated workflow for parallel processing of large multiview SPIM recordings. Bioinformatics 32, 1112–1114 (2016).

    Article  PubMed  CAS  Google Scholar 

  105. Pietzsch, T., Saalfeld, S., Preibisch, S. & Tomancak, P. BigDataViewer: visualization and processing for large image data sets. Nat. Methods 12, 481–483 (2015).

    Article  PubMed  CAS  Google Scholar 

  106. Jug, F., Pietzsch, T., Preibisch, S. & Tomancak, P. Bioimage Informatics in the context of Drosophila research. Methods 68, 60–73 (2014).

    Article  PubMed  CAS  Google Scholar 

  107. Planchon, T. A. et al. Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination. Nat. Methods 8, 417–423 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. de Medeiros, G. et al. Confocal multiview light-sheet microscopy. Nat. Commun. 6, 8881 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Hu, Y. S., Zimmerley, M., Li, Y., Watters, R. & Cang, H. Single-molecule super-resolution light-sheet microscopy. Chem. Phys. Chem. 15, 577–586 (2014).

    Article  PubMed  CAS  Google Scholar 

  110. Hoyer, P. et al. Breaking the diffraction limit of light-sheet fluorescence microscopy by RESOLFT. Proc. Natl Acad. Sci. USA 113, 3442–3446 (2016).

    Article  PubMed  CAS  Google Scholar 

  111. Legant, W. R. et al. High-density three-dimensional localization microscopy across large volumes. Nat. Methods 13, 359–365 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Liu, T. L. et al. Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms. Science 360, eaaq1392 (2018).

    Article  PubMed  CAS  Google Scholar 

  113. Komis, G. et al. Superresolution live imaging of plant cells using structured illumination microscopy. Nat. Protoc. 10, 1248–1263 (2015).

    Article  PubMed  CAS  Google Scholar 

  114. Komis, G., Novák, D., Ovečka, M., Šamajová, O. & Šamaj, J. Advances in imaging plant cell dynamics. Plant Physiol. 176, 80–93 (2018).

    Article  PubMed  CAS  Google Scholar 

  115. Royer, L. A. et al. Adaptive light-sheet microscopy for long-term, high-resolution imaging in living organisms. Nat. Biotechnol. 34, 1267–1278 (2016).

    Article  PubMed  CAS  Google Scholar 

  116. Novák, D. et al. Gene expression pattern and protein localization of Arabidopsis phospholipase D alpha 1 revealed by advanced light-sheet and super-resolution microscopy. Frontiers Plant Sci. 9, 371 (2018).

    Article  Google Scholar 

  117. O’Callaghan, F. E., Braga, R. A., Neilson, R., MacFarlane, S. A. & Dupuy, L. X. New live-screening of plant-nematode interactions in the rhizosphere. Sci. Rep. 8, 1440 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Müllenbroich, M. C. et al. Comprehensive optical and data management infrastructure for high-throughput light-sheet microscopy of whole mouse brains. Neurophotonics 2, 041404 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Pampaloni, F., Richa, R., Ansari, N. & Stelzer, E. H. K. Live spheroid formation recorded with light sheet-based fluorescence microscopy. Methods Mol. Biol. 1251, 43–57 (2015).

    Article  PubMed  CAS  Google Scholar 

  120. Costantini, I. et al. A versatile clearing agent for multi-modal brain imaging. Sci. Rep. 5, 9808 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Fu, Q., Martin, B. L., Matus, D. Q. & Gao, L. Imaging multicellular specimens with real-time optimized tiling light-sheet selective plane illumination microscopy. Nat. Commun. 7, 11088 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported from ERDF project ‘Plants as a tool for sustainable global development’ (CZ.02.1.01/0.0/0.0/16_019/0000827). D.v.W. was funded through the BBSRC grants BB/N018575/1 and BB/M001806/1. P.T. was supported by European Regional Development Fund in the IT4Innovations national supercomputing center - path to exascale project, project number CZ.02.1.01/0.0/0.0/16_013/0001791 within the Operational Programme Research, Development and Education.

Author information

Author notes

  1. These authors contributed equally to this work: Miroslav Ovečka, Daniel von Wangenheim, Pavel Tomančák.

Authors and Affiliations

  1. Centre of the Region Haná for Biotechnological and Agricultural Research, Palacký University Olomouc, Olomouc, Czech Republic

    Miroslav Ovečka, Olga Šamajová, George Komis & Jozef Šamaj

  2. Plant Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, UK

    Daniel von Wangenheim

  3. Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany

    Pavel Tomančák

Authors
  1. Miroslav Ovečka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel von Wangenheim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pavel Tomančák
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Olga Šamajová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. George Komis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jozef Šamaj
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.O. and D.W. prepared figures. All authors contributed to the writing of this article.

Corresponding author

Correspondence to Jozef Šamaj.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Video legends

Reporting Summary

Supplementary Video 1

Time-lapse imaging of Arabidopsis seed germination, early seedling growth and lateral root formation.

Supplementary Video 2

Growth of the primary root of Medicago sativa.

Supplementary Video 3

Adventitious root emergence from Oryza sativa stem nodes.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ovečka, M., von Wangenheim, D., Tomančák, P. et al. Multiscale imaging of plant development by light-sheet fluorescence microscopy. Nature Plants 4, 639–650 (2018). https://doi.org/10.1038/s41477-018-0238-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0238-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing