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Title: Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy

Abstract

The performance of the photosynthesis machinery in plants, including light harvesting, electron transport, and protein repair is controlled by structural changes of the thylakoid membrane system inside the chloroplasts. In particular, the structure of the stacked grana area of thylakoid membranes is highly dynamic, changing in response to different environmental cues such as light intensity. For example, the aqueous thylakoid lumen enclosed by thylakoid membranes in grana has been documented to swell in the presence of light. However, light-induced alteration of the stromal gap in the stacked grana (partition gap) and of the unstacked stroma lamellae have not been well characterized. Light-induced changes of the entire thylakoid membrane system including the lumen in both stacked and unstacked domains as well as the partition gap are presented here, and the functional implications are discussed. This structural analysis was made possible by development of a robust semi-automated image analysis method combined with optimized plant tissue fixation techniques for transmission electron microscopy generating quantitative structural results for the analysis of thylakoid ultrastructure.

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1];  [2]; ORCiD logo [1]
  1. Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry
  2. Washington State Univ., Pullman, WA (United States). Franceschi Microscopy and Imaging Center
Publication Date:
Research Org.:
Washington State Univ., Pullman, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); USDA
OSTI Identifier:
1735366
Alternate Identifier(s):
OSTI ID: 1735373
Grant/Contract Number:  
SC0017160; 1005351; 0119; MCB-1158571; MCB-1953570
Resource Type:
Accepted Manuscript
Journal Name:
Plant Direct
Additional Journal Information:
Journal Volume: 4; Journal Issue: 11; Journal ID: ISSN 2475-4455
Publisher:
Wiley and American Society of Plant Biologists and Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis thaliana; high‐pressure freezing; photosynthesis; stromal gap; thylakoid lumen; thylakoid membrane; transmission electron microscopy

Citation Formats

Li, Meng, Mukhopadhyay, Roma, Svoboda, Václav, Oung, Hui Olivia, Mullendore, Daniel L., and Kirchhoff, Helmut. Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy. United States: N. p., 2020. Web. https://doi.org/10.1002/pld3.280.
Li, Meng, Mukhopadhyay, Roma, Svoboda, Václav, Oung, Hui Olivia, Mullendore, Daniel L., & Kirchhoff, Helmut. Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy. United States. https://doi.org/10.1002/pld3.280
Li, Meng, Mukhopadhyay, Roma, Svoboda, Václav, Oung, Hui Olivia, Mullendore, Daniel L., and Kirchhoff, Helmut. Thu . "Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy". United States. https://doi.org/10.1002/pld3.280. https://www.osti.gov/servlets/purl/1735366.
@article{osti_1735366,
title = {Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy},
author = {Li, Meng and Mukhopadhyay, Roma and Svoboda, Václav and Oung, Hui Olivia and Mullendore, Daniel L. and Kirchhoff, Helmut},
abstractNote = {The performance of the photosynthesis machinery in plants, including light harvesting, electron transport, and protein repair is controlled by structural changes of the thylakoid membrane system inside the chloroplasts. In particular, the structure of the stacked grana area of thylakoid membranes is highly dynamic, changing in response to different environmental cues such as light intensity. For example, the aqueous thylakoid lumen enclosed by thylakoid membranes in grana has been documented to swell in the presence of light. However, light-induced alteration of the stromal gap in the stacked grana (partition gap) and of the unstacked stroma lamellae have not been well characterized. Light-induced changes of the entire thylakoid membrane system including the lumen in both stacked and unstacked domains as well as the partition gap are presented here, and the functional implications are discussed. This structural analysis was made possible by development of a robust semi-automated image analysis method combined with optimized plant tissue fixation techniques for transmission electron microscopy generating quantitative structural results for the analysis of thylakoid ultrastructure.},
doi = {10.1002/pld3.280},
journal = {Plant Direct},
number = 11,
volume = 4,
place = {United States},
year = {2020},
month = {11}
}

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Works referenced in this record:

The major thylakoid protein kinases STN7 and STN8 revisited: effects of altered STN8 levels and regulatory specificities of the STN kinases
journal, January 2013


A chemical mechanism for tissue staining by osmium tetroxide-ferrocyanide mixtures.
journal, July 1979

  • White, D. L.; Mazurkiewicz, J. E.; Barrnett, R. J.
  • Journal of Histochemistry & Cytochemistry, Vol. 27, Issue 7
  • DOI: 10.1177/27.7.89155

Dynamic control of protein diffusion within the granal thylakoid lumen
journal, November 2011

  • Kirchhoff, H.; Hall, C.; Wood, M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 50
  • DOI: 10.1073/pnas.1104141109

Transversal and Lateral Exciton Energy Transfer in Grana Thylakoids of Spinach
journal, November 2004

  • Kirchhoff, Helmut; Borinski, Mauricio; Lenhert, Steven
  • Biochemistry, Vol. 43, Issue 45
  • DOI: 10.1021/bi048473w

Fundamental helical geometry consolidates the plant photosynthetic membrane
journal, October 2019

  • Bussi, Yuval; Shimoni, Eyal; Weiner, Allon
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 44
  • DOI: 10.1073/pnas.1905994116

Arabidopsis CURVATURE THYLAKOID1 Proteins Modify Thylakoid Architecture by Inducing Membrane Curvature
journal, July 2013


Architectural switch in plant photosynthetic membranes induced by light stress
journal, November 2012

  • Herbstova, M.; Tietz, S.; Kinzel, C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 49
  • DOI: 10.1073/pnas.1214265109

Pea PSII-LHCII supercomplexes form pairs by making connections across the stromal gap
journal, August 2017


Mobility of photosynthetic proteins
journal, August 2013


Compartmentalization of the protein repair machinery in photosynthetic membranes
journal, October 2014

  • Puthiyaveetil, S.; Tsabari, O.; Lowry, T.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
  • DOI: 10.1073/pnas.1413739111

Three-Dimensional Architecture of Grana and Stroma Thylakoids of Higher Plants as Determined by Electron Tomography
journal, January 2011


ImageJ2: ImageJ for the next generation of scientific image data
journal, November 2017

  • Rueden, Curtis T.; Schindelin, Johannes; Hiner, Mark C.
  • BMC Bioinformatics, Vol. 18, Issue 1
  • DOI: 10.1186/s12859-017-1934-z

Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer
journal, January 2018

  • Wood, William H. J.; MacGregor-Chatwin, Craig; Barnett, Samuel F. H.
  • Nature Plants, Vol. 4, Issue 2
  • DOI: 10.1038/s41477-017-0092-7

Structure of the Cytochrome b6f Complex of Oxygenic Photosynthesis: Tuning the Cavity
journal, November 2003


Ions channels/transporters and chloroplast regulation
journal, July 2015


Dynamic Thylakoid Stacking Is Regulated by LHCII Phosphorylation but Not Its interaction with PSI
journal, June 2019

  • Wood, William H. J.; Barnett, Samuel F. H.; Flannery, Sarah
  • Plant Physiology, Vol. 180, Issue 4
  • DOI: 10.1104/pp.19.00503

A quantitative model of the domain structure of the photosynthetic membrane
journal, August 2001


Phloem Ultrastructure and Pressure Flow: Sieve-Element-Occlusion-Related Agglomerations Do Not Affect Translocation
journal, December 2011

  • Froelich, Daniel R.; Mullendore, Daniel L.; Jensen, Kåre H.
  • The Plant Cell, Vol. 23, Issue 12
  • DOI: 10.1105/tpc.111.093179

Supramolecular organization of thylakoid membrane proteins in green plants
journal, January 2005

  • Dekker, Jan P.; Boekema, Egbert J.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
  • DOI: 10.1016/j.bbabio.2004.09.009

Chloroplast ultrastructure in plants
journal, March 2019


Routing of thylakoid lumen proteins by the chloroplast twin arginine transport pathway
journal, August 2018

  • New, Christopher Paul; Ma, Qianqian; Dabney-Smith, Carole
  • Photosynthesis Research, Vol. 138, Issue 3
  • DOI: 10.1007/s11120-018-0567-z

Three-Dimensional Organization of Higher-Plant Chloroplast Thylakoid Membranes Revealed by Electron Tomography
journal, July 2005


Crystal structure analyses of reduced (CuI) poplar plastocyanin at six pH values
journal, November 1986


Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips ofNicotiana andArabidopsis
journal, February 1990

  • Kiss, J. Z.; Giddings, Th. H.; Staehelin, L. A.
  • Protoplasma, Vol. 157, Issue 1-3
  • DOI: 10.1007/BF01322639

The structural and functional domains of plant thylakoid membranes
journal, November 2018

  • Koochak, Haniyeh; Puthiyaveetil, Sujith; Mullendore, Daniel L.
  • The Plant Journal, Vol. 97, Issue 3
  • DOI: 10.1111/tpj.14127

The Mechanism of Nonphotochemical Quenching: The End of the Ongoing Debate
journal, October 2019


Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis
journal, May 2014

  • Kunz, H. -H.; Gierth, M.; Herdean, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
  • DOI: 10.1073/pnas.1323899111

Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing
journal, June 1999

  • Bourett, Timothy M.; Czymmek, Kirk J.; Howard, Richard J.
  • Planta, Vol. 208, Issue 4
  • DOI: 10.1007/s004250050584

A voltage-dependent chloride channel fine-tunes photosynthesis in plants
journal, May 2016

  • Herdean, Andrei; Teardo, Enrico; Nilsson, Anders K.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11654

Sublocalization of Cytochrome b6f Complexes in Photosynthetic Membranes
journal, July 2017


Is There Excitation Energy Transfer between Different Layers of Stacked Photosystem-II-Containing Thylakoid Membranes?
journal, March 2016

  • Farooq, Shazia; Chmeliov, Jevgenij; Trinkunas, Gediminas
  • The Journal of Physical Chemistry Letters, Vol. 7, Issue 7
  • DOI: 10.1021/acs.jpclett.6b00474

Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively
journal, July 2007

  • Marmagne, A.; Vinauger-Douard, M.; Monachello, D.
  • Journal of Experimental Botany, Vol. 58, Issue 12
  • DOI: 10.1093/jxb/erm187

Changes in thylakoid membrane thickness associated with the reorganization of photosystem II light harvesting complexes during photoprotective energy dissipation
journal, September 2011

  • Johnson, Matthew P.; Brain, Anthony P. R.; Ruban, Alexander V.
  • Plant Signaling & Behavior, Vol. 6, Issue 9
  • DOI: 10.4161/psb.6.9.16503

Function and evolution of grana
journal, November 2005


Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue
journal, January 2005

  • Chow, Wah Soon; Kim, Eun-Ha; Horton, Peter
  • Photochemical & Photobiological Sciences, Vol. 4, Issue 12
  • DOI: 10.1039/b507310n

Surface charge dynamics in photosynthetic membranes and the structural consequences
journal, March 2017

  • Puthiyaveetil, Sujith; van Oort, Bart; Kirchhoff, Helmut
  • Nature Plants, Vol. 3, Issue 4
  • DOI: 10.1038/nplants.2017.20

How paired PSII–LHCII supercomplexes mediate the stacking of plant thylakoid membranes unveiled by structural mass-spectrometry
journal, March 2020


Thylakoid Membrane Remodeling during State Transitions in Arabidopsis
journal, April 2008

  • Chuartzman, Silvia G.; Nevo, Reinat; Shimoni, Eyal
  • The Plant Cell, Vol. 20, Issue 4
  • DOI: 10.1105/tpc.107.055830

The Arabidopsis Thylakoid Chloride Channel AtCLCe Functions in Chloride Homeostasis and Regulation of Photosynthetic Electron Transport
journal, February 2016


Hypothesis: Are grana necessary for regulation of light harvesting?
journal, January 1999

  • Horton, Peter
  • Functional Plant Biology, Vol. 26, Issue 7
  • DOI: 10.1071/PP99095

Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts
journal, April 2014

  • Kirchhoff, Helmut
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1640
  • DOI: 10.1098/rstb.2013.0225

New Insights in Thylakoid Membrane Organization
journal, September 2005

  • Pfeiffer, Stephan; Krupinska, Karin
  • Plant and Cell Physiology, Vol. 46, Issue 9
  • DOI: 10.1093/pcp/pci156

Interaction between the lumenal sides of the thylakoid membrane
journal, November 1982


Architectural switches in plant thylakoid membranes
journal, May 2013


Phosphorylation of Photosystem II Controls Functional Macroscopic Folding of Photosynthetic Membranes in Arabidopsis
journal, December 2009

  • Fristedt, Rikard; Willig, Adrian; Granath, Pontus
  • The Plant Cell, Vol. 21, Issue 12
  • DOI: 10.1105/tpc.109.069435

Structure-Function of the Cytochrome b 6 f Complex
journal, November 2008


Fine‐tuned regulation of the K + /H + antiporter KEA 3 is required to optimize photosynthesis during induction
journal, February 2017

  • Wang, Caijuan; Yamamoto, Hiroshi; Narumiya, Fumika
  • The Plant Journal, Vol. 89, Issue 3
  • DOI: 10.1111/tpj.13405

The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering
journal, September 2014

  • Ünnep, R.; Zsiros, O.; Solymosi, K.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 9
  • DOI: 10.1016/j.bbabio.2014.01.017

Differential Mobility of Pigment-Protein Complexes in Granal and Agranal Thylakoid Membranes of C 3 and C 4 Plants
journal, November 2012

  • Kirchhoff, Helmut; Sharpe, Richard M.; Herbstova, Miroslava
  • Plant Physiology, Vol. 161, Issue 1
  • DOI: 10.1104/pp.112.207548

Grana-Localized Proteins, RIQ1 and RIQ2, Affect the Organization of Light-Harvesting Complex II and Grana Stacking in Arabidopsis
journal, September 2016

  • Yokoyama, Ryo; Yamamoto, Hiroshi; Kondo, Maki
  • The Plant Cell, Vol. 28, Issue 9
  • DOI: 10.1105/tpc.16.00296

Microwave-assisted rapid plant sample preparation for transmission electron microscopy
journal, February 2009


The Three-Dimensional Network of the Thylakoid Membranes in Plants: Quasihelical Model of the Granum-Stroma Assembly
journal, October 2008

  • Mustárdy, László; Buttle, Karolyn; Steinbach, Gábor
  • The Plant Cell, Vol. 20, Issue 10
  • DOI: 10.1105/tpc.108.059147

Towards elucidation of dynamic structural changes of plant thylakoid architecture
journal, December 2012

  • Anderson, Jan M.; Horton, Peter; Kim, Eun-Ha
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1608
  • DOI: 10.1098/rstb.2012.0373

Diffusion of molecules and macromolecules in thylakoid membranes
journal, April 2014


Cryo-EM structure of the spinach cytochrome b6 f complex at 3.6 Å resolution
journal, November 2019


Arrangement of Photosystem II and ATP Synthase in Chloroplast Membranes of Spinach and Pea
journal, April 2010

  • Daum, Bertram; Nicastro, Daniela; Austin, Jotham
  • The Plant Cell, Vol. 22, Issue 4
  • DOI: 10.1105/tpc.109.071431

Functional domain size in aggregates of light-harvesting complex II and thylakoid membranes
journal, September 2011

  • Lambrev, Petar H.; Schmitt, Franz-Josef; Kussin, Sabine
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 9
  • DOI: 10.1016/j.bbabio.2011.05.003

OPM: Orientations of Proteins in Membranes database
journal, January 2006


Composition, phosphorylation and dynamic organization of photosynthetic protein complexes in plant thylakoid membrane
journal, January 2020

  • Rantala, Marjaana; Rantala, Sanna; Aro, Eva-Mari
  • Photochemical & Photobiological Sciences, Vol. 19, Issue 5
  • DOI: 10.1039/D0PP00025F

Charting the native architecture of Chlamydomonas thylakoid membranes with single-molecule precision
journal, April 2020

  • Wietrzynski, Wojciech; Schaffer, Miroslava; Tegunov, Dimitry
  • eLife, Vol. 9
  • DOI: 10.7554/eLife.53740

Ultrastructural modeling of small angle scattering from photosynthetic membranes
journal, December 2019


Advances in ultrarapid freezing for the preservation of cellular ultrastructure
journal, January 1986

  • Gilkey, John C.; Staehelin, L. Andrew
  • Journal of Electron Microscopy Technique, Vol. 3, Issue 2, p. 177-210
  • DOI: 10.1002/jemt.1060030206

An atypical haem in the cytochrome b6f complex
journal, November 2003

  • Stroebel, David; Choquet, Yves; Popot, Jean-Luc
  • Nature, Vol. 426, Issue 6965
  • DOI: 10.1038/nature02155