Differential Polarization Imaging of Plant Cells. Mapping the Anisotropy of Cell Walls and Chloroplasts
Language English Country Switzerland Media electronic
Document type Journal Article, Review
Grant support
GINOP-2.3.3-15-2016-00003
Nemzetgazdasági Minisztérium
GINOP-2.3.3-15-2016-00030
Nemzetgazdasági Minisztérium
GINOP-2.1.7-15-2016-00713
Nemzetgazdasági Minisztérium
GINOP-2.3.2-15-2016-00001
Nemzetgazdasági Minisztérium
OTKA K 128679
Hungarian Scientific Research Fund
No 451-03-9/2021-14/200053
Science Fund of the Republic of Serbia
PubMed
34299279
PubMed Central
PMC8306740
DOI
10.3390/ijms22147661
PII: ijms22147661
Knihovny.cz E-resources
- Keywords
- DP-LSM, RCM, anisotropy, cell wall, chloroplast, circular dichroism, fluorescence-detected linear dichroism, micro-spectropolarimetry, molecular organization, polarized light,
- MeSH
- Anisotropy MeSH
- Cell Wall ultrastructure MeSH
- Chloroplasts ultrastructure MeSH
- Microscopy, Confocal methods MeSH
- Microscopy, Polarization methods MeSH
- Plant Cells ultrastructure MeSH
- Thylakoids ultrastructure MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
Modern light microscopy imaging techniques have substantially advanced our knowledge about the ultrastructure of plant cells and their organelles. Laser-scanning microscopy and digital light microscopy imaging techniques, in general-in addition to their high sensitivity, fast data acquisition, and great versatility of 2D-4D image analyses-also opened the technical possibilities to combine microscopy imaging with spectroscopic measurements. In this review, we focus our attention on differential polarization (DP) imaging techniques and on their applications on plant cell walls and chloroplasts, and show how these techniques provided unique and quantitative information on the anisotropic molecular organization of plant cell constituents: (i) We briefly describe how laser-scanning microscopes (LSMs) and the enhanced-resolution Re-scan Confocal Microscope (RCM of Confocal.nl Ltd. Amsterdam, Netherlands) can be equipped with DP attachments-making them capable of measuring different polarization spectroscopy parameters, parallel with the 'conventional' intensity imaging. (ii) We show examples of different faces of the strong anisotropic molecular organization of chloroplast thylakoid membranes. (iii) We illustrate the use of DP imaging of cell walls from a variety of wood samples and demonstrate the use of quantitative analysis. (iv) Finally, we outline the perspectives of further technical developments of micro-spectropolarimetry imaging and its use in plant cell studies.
Biofotonika Research and Development Ltd 6720 Szeged Hungary
Department of Physics Faculty of Science Ostrava University 709 00 Ostrava Czech Republic
See more in PubMed
Abbe E. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Arch. Für Mikrosk. Anat. 1873;9:413–418. doi: 10.1007/BF02956173. DOI
Airy G.B. On the diffraction of an object-glass with circular aperture. Trans. Cambridge Phil. Soc. 1835;5:283–291.
Webb R.H. Confocal optical microscopy. Rep. Prog. Phys. 1996;59:427–471. doi: 10.1088/0034-4885/59/3/003. DOI
Diaspro A.F.M., Sapuppo P. Confocal Microscopy. Leica Microsystems CMS GmbH; Mannheim, Germany: 2008.
De Luca G.M.R., Breedijk R.M.P., Brandt R.A.J., Zeelenberg C.H.C., de Jong B.E., Timmermans W., Azar L.N., Hoebe R.A., Stallinga S., Manders E.M.M. Re-scan confocal microscopy: Scanning twice for better resolution. Biomed. Opt. Express. 2013;4:2644–2656. doi: 10.1364/BOE.4.002644. PubMed DOI PMC
Huszka G., Gijs M.A.M. Super-resolution optical imaging: A comparison. Micro. Nano. Eng. 2019;2:7–28. doi: 10.1016/j.mne.2018.11.005. DOI
Datta R., Heaster T.M., Sharick J.T., Gillette A.A., Skala M.C. Fluorescence lifetime imaging microscopy: Fundamentals and advances in instrumentation, analysis, and applications. J. Biomed. Opt. 2020;25:071203. doi: 10.1117/1.JBO.25.7.071203. PubMed DOI PMC
Fish K.N. Total Internal Reflection Fluorescence. Curr. Protoc. Cytom. 2009;50:12–18. PubMed PMC
Gierlinger N., Schwanninger M. The potential of Raman microscopy and Raman imaging in plant research. Spectrosc. Int. J. 2007;21:69–89. doi: 10.1155/2007/498206. DOI
Steinbach G., Pawlak K., Pomozi I., Toth E.A., Molnar A., Matko J., Garab G. Mapping microscopic order in plant and mammalian cells and tissues: Novel differential polarization attachment for new generation confocal microscopes (DP-LSM) Methods Appl. Fluores. 2014;2:015005. doi: 10.1088/2050-6120/2/1/015005. PubMed DOI
Steinbach G., Pomozi I., Zsiros O., Menczel L., Garab G. Imaging anisotropy using differential polarization laser scanning confocal microscopy. Acta Histochem. 2009;111:317–326. doi: 10.1016/j.acthis.2008.11.021. PubMed DOI
Steinbach G., Nagy D., Sipka G., Manders E., Garab G., Zimanyi L. Fluorescence-detected linear dichroism imaging in a re-scan confocal microscope equipped with differential polarization attachment. Eur. Biophys. J. Biophy. 2019;48:457–463. doi: 10.1007/s00249-019-01365-4. PubMed DOI PMC
Kim M., Keller D., Bustamante C. Differential Polarization Imaging.1. Theory. Biophys. J. 1987;52:911–927. doi: 10.1016/S0006-3495(87)83285-X. PubMed DOI PMC
Kim M., Bustamante C. Differential Polarization Imaging.4. Images in Higher Born Approximations. Biophys. J. 1991;59:1171–1182. doi: 10.1016/S0006-3495(91)82333-5. PubMed DOI PMC
Mueller H. The foundation of optics. J. Opt. Soc. Am. 1948;38:661.
Tinoco I., Mickols W., Maestre M.F., Bustamante C. Absorption, Scattering, and Imaging of Biomolecular Structures with Polarized-Light. Annu. Rev. Biophys. Bio. 1987;16:319–349. doi: 10.1146/annurev.bb.16.060187.001535. PubMed DOI
Patty C.H.L., Luo D.A., Snik F., Ariese F., Buma W.J., ten Kate I.L., van Spanning R.J.M., Sparks W.B., Germer T.A., Garab G., et al. Imaging linear and circular polarization features in leaves with complete Mueller matrix polarimetry. Bba-Gen Subj. 2018;1862:1350–1363. doi: 10.1016/j.bbagen.2018.03.005. PubMed DOI PMC
Lakowicz J.R. Principles of Fluorescence Spectroscopy. Springer; New York, NY, USA: 2006.
Garab G. Linear and Circular Dichroism. Kluwer Academic Publishers; Amsterdam, The Netherlands: 1996.
Gombos I., Steinbach G., Pomozi I., Balogh A., Vamosi G., Gansen A., Laszlo G., Garab G., Matko J. Some new faces of membrane microdomains: A complex confocal fluorescence, differential polarization, and FCS imaging study on live immune cells. Cytom. Part A. 2008;73:220–229. doi: 10.1002/cyto.a.20516. PubMed DOI
Kuball H.G. CD and ACD spectroscopy on anisotropic samples: Chirality of oriented molecules and anisotropic phases—A critical analysis. Enantiomer. 2002;7:197–205. doi: 10.1080/10242430212880. PubMed DOI
Akhtar P., Lindorfer D., Lingvay M., Pawlak K., Zsiros O., Siligardi G., Javorfi T., Dorogi M., Ughy B., Garab G., et al. Anisotropic Circular Dichroism of Light-Harvesting Complex II in Oriented Lipid Bilayers: Theory Meets Experiment. J. Phys. Chem. B. 2019;123:1090–1098. doi: 10.1021/acs.jpcb.8b12474. PubMed DOI
Mickols W., Tinoco I., Katz J.E., Maestre M.F., Bustamante C. Imaging Differential Polarization Microscope with Electronic Readout. Rev. Sci. Instrum. 1985;56:2228–2236. doi: 10.1063/1.1138354. DOI
Finzi L., Bustamante C., Garab G., Juang C.B. Direct Observation of Large Chiral Domains in Chloroplast Thylakoid Membranes by Differential Polarization Microscopy. Proc. Natl. Acad. Sci. USA. 1989;86:8748–8752. doi: 10.1073/pnas.86.22.8748. PubMed DOI PMC
Gupta V.K., Kornfield J.A. Polarization Modulation Laser-Scanning Microscopy—A Powerful Tool to Image Molecular-Orientation and Order. Rev. Sci. Instrum. 1994;65:2823–2828. doi: 10.1063/1.1144622. DOI
Garab G., Pomozi I., Weiss G., Jörgens R. Method and Apparatus for Determining the Polarization Properties of Light Emitted, Reflected or Transmitted by a Material Using a Laser Scanning Microscope. No. 6,856,391. U.S. Patent. 2005 Feb 15;
Gorjanacz M., Torok I., Pomozi I., Garab G., Szlanka T., Kiss I., Mechler B.M. Domains of importin-alpha 2 required for ring canal assembly during Drosophila oogenesis. J. Struct. Biol. 2006;154:27–41. doi: 10.1016/j.jsb.2005.12.007. PubMed DOI
Kim M., Ulibarri L., Bustamante C. Differential Polarization Imaging.2. Symmetry Properties and Calculations. Biophys. J. 1987;52:929–946. doi: 10.1016/S0006-3495(87)83286-1. PubMed DOI PMC
Steinbach G., Besson F., Pomozi I., Garab G. Photonic Applications in Biosensing and Imaging. Volume 5969. International Society for Optics and Photonics; San Diego, CA, USA: 2005. Differential polarization laser scanning microscopy: Biological applications; pp. 566–575.
Lazar J., Bondar A., Timr S., Firestein S.J. Two-photon polarization microscopy reveals protein structure and function. Nat. Methods. 2011;8:684–690. doi: 10.1038/nmeth.1643. PubMed DOI
Wang X., Kress A., Brasselet S., Ferrand P. High frame-rate fluorescence confocal angle-resolved linear dichroism microscopy. Rev. Sci. Instrum. 2013;84:053708. doi: 10.1063/1.4807318. PubMed DOI
Hafi N., Grunwald M., van den Heuvel L.S., Aspelmeier T., Chen J.H., Zagrebelsky M., Schutte O.M., Steinem C., Korte M., Munk A., et al. Fluorescence nanoscopy by polarization modulation and polarization angle narrowing. Nat. Methods. 2014;11:579–584. doi: 10.1038/nmeth.2919. PubMed DOI
Mazumder N., Qiu J.J., Kao F.J., Diaspro A. Mueller matrix signature in advanced fluorescence microscopy imaging. J. Opt. UK. 2017;19:025301. doi: 10.1088/2040-8986/aa5114. DOI
Loison O., Weitkunat M., Kaya-Copur A., Alves C.N., Matzat T., Spletter M.L., Luschnig S., Brasselet S., Lenne P.F., Schnorrer F. Polarization-resolved microscopy reveals a muscle myosin motor-independent mechanism of molecular actin ordering during sarcomere maturation. Plos. Biol. 2018;16:e2004718. doi: 10.1371/journal.pbio.2004718. PubMed DOI PMC
Blankenship R.E. Molecular Mechanisms of Photosynthesis. Wiley-Blackwell; Oxford, UK: 2014.
Garab G., van Amerongen H. Linear dichroism and circular dichroism in photosynthesis research. Photosynth. Res. 2009;101:135–146. doi: 10.1007/s11120-009-9424-4. PubMed DOI PMC
Keller D., Bustamante C. Theory of the Interaction of Light with Large Inhomogeneous Molecular Aggregates.2. Psi-Type Circular-Dichroism. J. Chem. Phys. 1986;84:2972–2980. doi: 10.1063/1.450278. DOI
Mustardy L., Garab G. Granum revisited. A three-dimensional model—Where things fall into place. Trends Plant Sci. 2003;8:117–122. doi: 10.1016/S1360-1385(03)00015-3. PubMed DOI
Mustardy L., Buttle K., Steinbach G., Garab G. The Three-Dimensional Network of the Thylakoid Membranes in Plants: Quasihelical Model of the Granum-Stroma Assembly. Plant Cell. 2008;20:2552–2557. doi: 10.1105/tpc.108.059147. PubMed DOI PMC
Garab G., Galajda P., Pomozi I., Finzi L., Praznovszky T., Ormos P., van Amerongen H. Alignment of biological microparticles by a polarized laser beam. Eur. Biophys. J. Biophy. 2005;34:335–343. doi: 10.1007/s00249-004-0454-8. PubMed DOI
Verbelen J.P., Kerstens S. Polarization confocal microscopy and Congo Red fluorescence: A simple and rapid method to determine the mean cellulose fibril orientation in plants. J. Microsc. 2000;198:101–107. doi: 10.1046/j.1365-2818.2000.00691.x. PubMed DOI
Harris P.J. Primary and secondary plant cell walls: A comparative overview. N. Z. J. For. Sci. 2006;36:36–53.
Cosgrove D.J., Jarvis M.C. Comparative structure and biomechanics of plant primary and secondary cell walls. Front. Plant Sci. 2012;3:204. doi: 10.3389/fpls.2012.00204. PubMed DOI PMC
Timell T.E. Compression Wood in Gymnosperms. Springer; Heidelberg, Germany: 1986.
Donaldson L., Xu P. Microfibril orientation across the secondary cell wall of Radiata pine tracheids. Trees-Struct. Funct. 2005;19:644–653. doi: 10.1007/s00468-005-0428-1. DOI
Barnett J.R., Bonham V.A. Cellulose microfibril angle in the cell wall of wood fibres. Biol. Rev. 2004;79:461–472. doi: 10.1017/S1464793103006377. PubMed DOI
Schaffer J.B.H. Test Preparation for Microscopes. 20040180384. U.S. Patent. 2002 Dec 12;
Baskin T.I., Meekes H.T.H.M., Liang B.M., Sharp R.E. Regulation of growth anisotropy in well-watered and water-stressed maize roots. II. Role of cortical microtubules and cellulose microfibrils. Plant Physiol. 1999;119:681–692. doi: 10.1104/pp.119.2.681. PubMed DOI PMC
Steinbach G., Pomozi I., Zsiros O., Pay A., Horvath G.V., Garab G. Imaging fluorescence detected linear dichroism of plant cell walls in laser scanning confocal microscope. Cytom. Part A. 2008;73:202–208. doi: 10.1002/cyto.a.20517. PubMed DOI
Kerstens S., Verbelen J.P. Cellulose orientation in the outer epidermal wall of angiosperm roots: Implications for biosystematics. Ann. Bot. Lond. 2002;90:669–676. doi: 10.1093/aob/mcf237. PubMed DOI PMC
Djikanovic D., Devecerski A., Steinbach G., Simonovic J., Matovic B., Garab G., Kalauzi A., Radotic K. Comparison of macromolecular interactions in the cell walls of hardwood, softwood and maize by fluorescence and FTIR spectroscopy, differential polarization laser scanning microscopy and X-ray diffraction. Wood Sci. Technol. 2016;50:547–566. doi: 10.1007/s00226-015-0792-y. DOI
Radosavljevic J.S., Pristov J.B., Mitrovic A.L., Steinbach G., Mouille G., Tufegdzic S., Maksimovic V., Mutavdzic D., Janosevic D., Vukovic M., et al. Parenchyma cell wall structure in twining stem of Dioscorea balcanica. Cellulose. 2017;24:4653–4669. doi: 10.1007/s10570-017-1460-1. DOI
Savic A., Mitrovic A., Donaldson L., Radosavljevic J.S., Pristov J.B., Steinbach G., Garab G., Radotic K. Fluorescence-Detected Linear Dichroism of Wood Cell Walls in Juvenile Serbian Spruce: Estimation of Compression Wood Severity. Microsc. Microanal. 2016;22:361–367. doi: 10.1017/S143192761600009X. PubMed DOI
Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC
Chappaz-Gillot C., Marek P.L., Blaive B.J., Canard G., Burck J., Garab G., Hahn H., Javorfi T., Kelemen L., Krupke R., et al. Anisotropic Organization and Microscopic Manipulation of Self-Assembling Synthetic Porphyrin Microrods That Mimic Chlorosomes: Bacterial Light-Harvesting Systems. J. Am. Chem. Soc. 2012;134:944–954. doi: 10.1021/ja203838p. PubMed DOI
Garab G. Hierarchical organization and structural flexibility of thylakoid membranes. Biochim. Biophys. Acta (BBA) Bioenerg. 2014;1837:481–494. doi: 10.1016/j.bbabio.2013.12.003. PubMed DOI
Banas A.K., Aggarwal C., Labuz J., Sztatelman O., Gabrys H. Blue light signalling in chloroplast movements. J. Exp. Bot. 2012;63:1559–1574. doi: 10.1093/jxb/err429. PubMed DOI
Wada M. Chloroplast movement. Plant Sci. 2013;210:177–182. doi: 10.1016/j.plantsci.2013.05.016. PubMed DOI
Kost B., Chua N.H. The plant cytoskeleton: Vacuoles and cell walls make the difference. Cell. 2002;108:9–12. doi: 10.1016/S0092-8674(01)00634-1. PubMed DOI
Friese M.E.J., Nieminen T.A., Heckenberg N.R., Rubinsztein-Dunlop H. Optical alignment and spinning of laser-trapped microscopic particles. Nature. 1998;394:348–350. doi: 10.1038/28566. DOI
Steinbach G., Pomozi I., Janosa D.P., Makovitzky J., Garab G. Confocal Fluorescence Detected Linear Dichroism Imaging of Isolated Human Amyloid Fibrils. Role of Supercoiling. J. Fluoresc. 2011;21:983–989. doi: 10.1007/s10895-010-0684-3. PubMed DOI