Three-dimensional imaging of xylem at cell wall level through near field nano holotomography.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
25 02 2021
Historique:
received: 08 05 2020
accepted: 08 02 2021
entrez: 26 2 2021
pubmed: 27 2 2021
medline: 27 2 2021
Statut: epublish

Résumé

Detailed imaging of the three-dimensionally complex architecture of xylary plants is important for studying biological and mechanical functions of woody plants. Apart from common two-dimensional microscopy, X-ray micro-computed tomography has been established as a three-dimensional (3D) imaging method for studying the hydraulic function of wooden plants. However, this X-ray imaging method can barely reach the resolution needed to see the minute structures (e.g. pit membrane). To complement the xylem structure with 3D views at the nanoscale level, X-ray near-field nano-holotomography (NFH) was applied to analyze the wood species Pinus sylvestris and Fagus sylvatica. The demanded small specimens required focused ion beam (FIB) application. The FIB milling, however, influenced the image quality through gallium implantation on the cell-wall surfaces. The measurements indicated that NFH is appropriate for imaging wood at nanometric resolution. With a 26 nm voxel pitch, the structure of the cell-wall surface in Pinus sylvestris could be visualized in genuine detail. In wood of Fagus sylvatica, the structure of a pit pair, including the pit membrane, between two neighboring fibrous cells could be traced tomographically.

Identifiants

pubmed: 33633184
doi: 10.1038/s41598-021-83885-8
pii: 10.1038/s41598-021-83885-8
pmc: PMC7907381
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4574

Références

Brodersen, C. R. & Roddy, A. B. New frontiers in the three-dimensional visualization of plant structure and function. Am. J. Bot. 103, 184–188 (2016).
doi: 10.3732/ajb.1500532
Daniel, G. Chapter 15—Microscope techniques for understanding wood cell structure and biodegradation. In Secondary xylem biology (eds Kim, Y. S. et al.) 309–343 (Academic Press, 2016).
Schulte, P. J. Computational fluid dynamics models of conifer bordered pits show how pit structure affects flow. New Phytol. 193, 721–729 (2012).
doi: 10.1111/j.1469-8137.2011.03986.x
Kotowska, M. M., Thom, R., Zhang, Y., Schenk, H. J. & Jansen, S. Within-tree variability and sample storage effects of bordered pit membranes in xylem of Acer pseudoplatanus. Trees 34, 61–71 (2020).
doi: 10.1007/s00468-019-01897-4
Zhang, Y. et al. High porosity with tiny pore constrictions and unbending pathways characterize the 3D structure of intervessel pit membranes in angiosperm xylem. Plant Cell Environ. 43, 116–130 (2020).
doi: 10.1111/pce.13654
Van den Bulcke, J. et al. Potential of X-ray computed tomography for 3D anatomical analysis and microdensitometrical assessment in wood research with focus on wood modification. Int. Wood Prod. J. 4, 183–190 (2013).
doi: 10.1179/2042645313Y.0000000046
Koddenberg, T. Three-dimensional X-ray micro-computed tomography imaging for applications to the structural characterization of wood. (Sierke Verlag, 2019).
Brodersen, C. R. Visualizing wood anatomy in three dimensions with high-resolution X-ray micro-tomography (μCT)—A review. IAWA J. 34, 408–424 (2013).
doi: 10.1163/22941932-00000033
Van den Bulcke, J. et al. Advanced X-ray CT scanning can boost tree ring research for earth system sciences. Ann. Bot. 124, 837–847 (2019).
doi: 10.1093/aob/mcz126
Losso, A. et al. Insights from in vivo micro-CT analysis: Testing the hydraulic vulnerability segmentation in Acer pseudoplatanus and Fagus sylvatica seedlings. New Phytol. 221, 1831–1842 (2019).
doi: 10.1111/nph.15549
Pratt, R. B. & Jacobsen, A. L. Identifying which conduits are moving water in woody plants: A new HRCT-based method. Tree Physiol. 38, 1200–1212 (2018).
doi: 10.1093/treephys/tpy034
Brodersen, C. R., Knipfer, T. & McElrone, A. J. In vivo visualization of the final stages of xylem vessel refilling in grapevine Vitis vinifera stems. New Phytol. 217, 117–126 (2018).
doi: 10.1111/nph.14811
Choat, B., Brodersen, C. R. & McElrone, A. J. Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytol. 205, 1095–1105 (2015).
doi: 10.1111/nph.13110
Li, X. et al. Lack of vulnerability segmentation in four angiosperm tree species: Evidence from direct X-ray microtomography observation. Ann. For. Sci. 77, 37 (2020).
doi: 10.1007/s13595-020-00944-2
Carrer, M., von Arx, G., Castagneri, D. & Petit, G. Distilling allometric and environmental information from time series of conduit size: The standardization issue and its relationship to tree hydraulic architecture. Tree Physiol. 35, 27–33 (2015).
doi: 10.1093/treephys/tpu108
Pfautsch, S. Hydraulic anatomy and function of trees? Basics and critical developments. Curr. For. Rep. 2, 236–248 (2016).
Sperry, J. S., Meinzer, F. C. & McCULLOH, K. A. Safety and efficiency conflicts in hydraulic architecture: Scaling from tissues to trees. Plant Cell Environ. 31, 632–645 (2008).
doi: 10.1111/j.1365-3040.2007.01765.x
Li, S. et al. Investigating effects of bordered pit membrane morphology and properties on plant xylem hydraulic functions—A case study from 3D reconstruction and microflow modelling of pit membranes in angiosperm xylem. Plants 9, 231 (2020).
doi: 10.3390/plants9020231
Choat, B., Cobb, A. R. & Jansen, S. Structure and function of bordered pits: New discoveries and impacts on whole-plant hydraulic function. New Phytol. 177, 608–625 (2008).
doi: 10.1111/j.1469-8137.2007.02317.x
Kaack, L. et al. Function and three-dimensional structure of intervessel pit membranes in angiosperms: A review. IAWA J. 40, 673–702 (2019).
doi: 10.1163/22941932-40190259
Trtik, P. et al. 3D imaging of microstructure of spruce wood. J. Struct. Biol. 159, 46–55 (2007).
doi: 10.1016/j.jsb.2007.02.003
Koddenberg, T., Wentzel, M. & Militz, H. Volumetric estimate of bordered pits in Pinus sylvestris based on X-ray tomography and light microscopy imaging. Micron 124, 102704 (2019).
doi: 10.1016/j.micron.2019.102704
Jansen, S., Choat, B. & Pletsers, A. Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am. J. Bot. 96, 409–419 (2009).
doi: 10.3732/ajb.0800248
Krenkel, M. Cone-beam x-ray phase-contrast tomography for the observation of single cells in whole organs. Vol 17 (Göttingen University Press, 2015).
Xu, P., Donaldson, L. A., Gergely, Z. R. & Staehelin, L. A. Dual-axis electron tomography: A new approach for investigating the spatial organization of wood cellulose microfibrils. Wood Sci. Technol. 41, 101 (2006).
doi: 10.1007/s00226-006-0088-3
Gabor, D. Holography, 1948–1971. Proc. IEEE 60, 655–668 (1972).
doi: 10.1109/PROC.1972.8725
Spence, J. C. H., Weierstall, U. & Howells, M. Phase recovery and lensless imaging by iterative methods in optical, X-ray and electron diffraction. Philos. Trans. R. Soc. Lond. Ser. Math. Phys. Eng. Sci. 360, 875–895 (2002).
doi: 10.1098/rsta.2001.0972
Bartels, M. Cone-beam x-ray phase contrast tomography of biological samples. Vol. 13 (Göttingen University Press, 2013).
Cloetens, P. et al. Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation x rays. Appl. Phys. Lett. 75, 2912–2914 (1999).
doi: 10.1063/1.125225
Hagemann, J., Töpperwien, M. & Salditt, T. Phase retrieval for near-field X-ray imaging beyond linearisation or compact support. Appl. Phys. Lett. 113, 041109 (2018).
doi: 10.1063/1.5029927
Greving, I. et al. Full-field hard X-ray microscope designed for materials science applications. Microsc. Microanal. 24, 228–229 (2018).
doi: 10.1017/S143192761801348X
Flenner, S. et al. Hard X-ray nano-holotomography with a Fresnel zone plate. Opt. Express 28, 37514–37525 (2020).
doi: 10.1364/OE.406074
Gürsoy, D., De Carlo, F., Xiao, X. & Jacobsen, C. TomoPy: A framework for the analysis of synchrotron tomographic data. J. Synchrotron Radiat. 21, 1188–1193 (2014).
doi: 10.1107/S1600577514013939
Turner, L. D. et al. X-ray phase imaging: Demonstration of extended conditions with homogeneous objects. Opt. Express 12, 2960–2965 (2004).
doi: 10.1364/OPEX.12.002960
Starck, J.-L., Elad, M. & Donoho, D. L. Image decomposition via the combination of sparse representations and a variational approach. IEEE Trans. Image Process. 14, 1570–1582 (2005).
doi: 10.1109/TIP.2005.852206
Reme, P. A. & Helle, T. Assessment of transverse dimensions of wood tracheids using SEM and image analysis. Holz Roh Werkst. 60, 277–282 (2002).
doi: 10.1007/s00107-002-0310-4
Martín, J. A., Esteban, L. G., de Palacios, P. & Fernandez, F. G. Variation in wood anatomical traits of Pinus sylvestris L. between Spanish regions of provenance. Trees-Struct. Funct. 24, 1017–1028 (2010).
doi: 10.1007/s00468-010-0471-4
Li, S. et al. Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA J. 37, 152–171 (2016).
doi: 10.1163/22941932-20160128
Zhang, Y., Klepsch, M. & Jansen, S. Bordered pits in xylem of vesselless angiosperms and their possible misinterpretation as perforation plates. Plant Cell Environ. 40, 2133–2146 (2017).
doi: 10.1111/pce.13014
Baas, P. Terminology of imperforate tracheary elements - in defence of libriform fibres with minutely bordered pits. IAWA J. 7, 82–86 (1986).
doi: 10.1163/22941932-90000446
Barnett, J. R. Plasmodesmata and pit development in secondary xylem elements. Planta 155, 251–260 (1982).
doi: 10.1007/BF00392724
Tixier, A. et al. Modelling the mechanical behaviour of pit membranes in bordered pits with respect to cavitation resistance in angiosperms. Ann. Bot. 114, 325–334 (2014).
doi: 10.1093/aob/mcu109

Auteurs

Tim Koddenberg (T)

Wood Biology and Wood Products, Faculty of Forest Sciences and Forest Ecology, University of Goettingen, Büsgenweg 4, 37077, Göttingen, Germany.

Imke Greving (I)

Institute of Materials Physics, Helmholtz-Zentrum Geesthacht, Max Plank Straße1, 21502, Geesthacht, Germany.

Johannes Hagemann (J)

Deutsches Elektronen Synchrotron-DESY, Notkestrasse 85, 22607, Hamburg, Germany.

Silja Flenner (S)

Institute of Materials Physics, Helmholtz-Zentrum Geesthacht, Max Plank Straße1, 21502, Geesthacht, Germany.

Andreas Krause (A)

Thünen-Institute of Wood Research, Leuschnerstraße 91, Hamburg-Bergedorf, 21031, Hamburg, Germany.

Daniel Laipple (D)

Institute of Materials Physics, Helmholtz-Zentrum Geesthacht, Max Plank Straße1, 21502, Geesthacht, Germany.

Kim C Klein (KC)

Wood Biology and Wood Products, Faculty of Forest Sciences and Forest Ecology, University of Goettingen, Büsgenweg 4, 37077, Göttingen, Germany.

Uwe Schmitt (U)

Thünen-Institute of Wood Research, Leuschnerstraße 91, Hamburg-Bergedorf, 21031, Hamburg, Germany.

Max Schuster (M)

Erlangen Centre for Astroparticle Physics, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Erwin-Rommel-Strasse 1, 91058, Erlangen, Germany.

Andreas Wolf (A)

Erlangen Centre for Astroparticle Physics, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Erwin-Rommel-Strasse 1, 91058, Erlangen, Germany.

Maria Seifert (M)

Erlangen Centre for Astroparticle Physics, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Erwin-Rommel-Strasse 1, 91058, Erlangen, Germany.

Veronika Ludwig (V)

Erlangen Centre for Astroparticle Physics, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Erwin-Rommel-Strasse 1, 91058, Erlangen, Germany.

Stefan Funk (S)

Erlangen Centre for Astroparticle Physics, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Erwin-Rommel-Strasse 1, 91058, Erlangen, Germany.

Holger Militz (H)

Wood Biology and Wood Products, Faculty of Forest Sciences and Forest Ecology, University of Goettingen, Büsgenweg 4, 37077, Göttingen, Germany.

Martin Nopens (M)

Thünen-Institute of Wood Research, Leuschnerstraße 91, Hamburg-Bergedorf, 21031, Hamburg, Germany. martin.nopens@thuenen.de.

Classifications MeSH