Subdiffraction-resolution live-cell imaging for visualizing thylakoid membranes

Iwai, Masakazu; Roth, Melissa S.; Niyogi, Krishna K.

doi:10.1111/tpj.14021

Title: Subdiffraction-resolution live-cell imaging for visualizing thylakoid membranes

Journal Article · 30 July 2018 · The Plant Journal

DOI: https://doi.org/10.1111/tpj.14021 · OSTI ID:1560876

^[1]; Roth, Melissa S. ^[2]; Niyogi, Krishna K. ^[1]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Div.; Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology, Howard Hughes Medical Institute
Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology, Howard Hughes Medical Institute

Summary The chloroplast is the chlorophyll‐containing organelle that produces energy through photosynthesis. Within the chloroplast is an intricate network of thylakoid membranes containing photosynthetic membrane proteins that mediate electron transport and generate chemical energy. Historically, electron microscopy (EM) has been a powerful tool for visualizing the macromolecular structure and organization of thylakoid membranes. However, an understanding of thylakoid membrane dynamics remains elusive because EM requires fixation and sectioning. To improve our knowledge of thylakoid membrane dynamics we need to consider at least two issues: (i) the live‐cell imaging conditions needed to visualize active processes in vivo ; and (ii) the spatial resolution required to differentiate the characteristics of thylakoid membranes. Here, we utilize three‐dimensional structured illumination microscopy (3D‐ SIM ) to explore the optimal imaging conditions for investigating the dynamics of thylakoid membranes in living plant and algal cells. We show that 3D‐ SIM is capable of examining broad characteristics of thylakoid structures in chloroplasts of the vascular plant Arabidopsis thaliana and distinguishing the structural differences between wild‐type and mutant strains. Using 3D‐ SIM , we also visualize thylakoid organization in whole cells of the green alga Chlamydomonas reinhardtii . These data reveal that high light intensity changes thylakoid membrane structure in C. reinhardtii . Moreover, we observed the green alga Chromochloris zofingiensis and the moss Physcomitrella patens to show the applicability of 3D‐ SIM . This study demonstrates that 3D‐ SIM is a promising approach for studying the dynamics of thylakoid membranes in photoautotrophic organisms during photoacclimation processes.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE

Grant/Contract Number:: SC0018301; AC02-05CH11231

OSTI ID:: 1560876

Alternate ID(s):: OSTI ID: 1462279; OSTI ID: 1559159

Journal Information:: The Plant Journal, Vol. 96, Issue 1; Related Information: Figure S1. Optical sections of reconstructed three‐dimensional structured illumination microscopy images of the side view of the chloroplast isolated from wild‐type Arabidopsis thaliana leaves.Figure S2. Optical sections of reconstructed three‐dimensional structured illumination microscopy images of the side view of the chloroplast isolated from Arabidopsis thaliana stn7 stn8 mutant leaves.Figure S3. Optical sections of reconstructed three‐dimensional structured illumination microscopy images of the side view of the chloroplast isolated from Arabidopsis thaliana tap38 mutant leaves.Figure S4. Optical sections of reconstructed three‐dimensional structured illumination microscopy images of a wild‐type Chlamydomonas reinhardtii cell.Figure S5. Additional reconstructed three‐dimensional structured illumination microscopy images showing shrinkage of thylakoid membranes at the lobe region of Chlamydomonas reinhardtii chloroplasts under high‐light conditions for 1 day.; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 24 works

Citation information provided by
Web of Science

References (55)

Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases Bonardi, Vera; Pesaresi, Paolo; Becker, Thomas Nature, Vol. 437, Issue 7062 https://doi.org/10.1038/nature04016	journal	October 2005
Light-induced Dissociation of an Antenna Hetero-oligomer Is Needed for Non-photochemical Quenching Induction Betterle, Nico; Ballottari, Matteo; Zorzan, Simone Journal of Biological Chemistry, Vol. 284, Issue 22 https://doi.org/10.1074/jbc.M808625200	journal	March 2009
Visualizing structural dynamics of thylakoid membranes Iwai, Masakazu; Yokono, Makio; Nakano, Akihiko Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep03768	journal	January 2014
Effect of the energy supply on filamentous growth and development in Physcomitrella patens Thelander, M. Journal of Experimental Botany, Vol. 56, Issue 412 https://doi.org/10.1093/jxb/eri040	journal	January 2005
Dynamic control of protein diffusion within the granal thylakoid lumen Kirchhoff, H.; Hall, C.; Wood, M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 50 https://doi.org/10.1073/pnas.1104141109	journal	November 2011
Programmed Changes in Form during Moss Development. Schumaker, K. S.; Dietrich, M. A. The Plant Cell https://doi.org/10.1105/tpc.9.7.1099	journal	July 1997
Ultrafast superresolution fluorescence imaging with spinning disk confocal microscope optics Hayashi, Shinichi; Okada, Yasushi Molecular Biology of the Cell, Vol. 26, Issue 9 https://doi.org/10.1091/mbc.E14-08-1287	journal	May 2015
Arabidopsis CURVATURE THYLAKOID1 Proteins Modify Thylakoid Architecture by Inducing Membrane Curvature Armbruster, U.; Labs, M.; Pribil, M. The Plant Cell, Vol. 25, Issue 7 https://doi.org/10.1105/tpc.113.113118	journal	July 2013
Three-Dimensional Resolution Doubling in Wide-Field Fluorescence Microscopy by Structured Illumination Gustafsson, Mats G. L.; Shao, Lin; Carlton, Peter M. Biophysical Journal, Vol. 94, Issue 12 https://doi.org/10.1529/biophysj.107.120345	journal	June 2008
Role of Plastid Protein Phosphatase TAP38 in LHCII Dephosphorylation and Thylakoid Electron Flow Pribil, Mathias; Pesaresi, Paolo; Hertle, Alexander PLoS Biology, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pbio.1000288	journal	January 2010
Photo-oxidative Stress in a Xanthophyll-deficient Mutant of Chlamydomonas Baroli, Irene; Gutman, Benjamin L.; Ledford, Heidi K. Journal of Biological Chemistry, Vol. 279, Issue 8 https://doi.org/10.1074/jbc.M312919200	journal	December 2003
Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution Chen, Bi-Chang; Legant, Wesley R.; Wang, Kai Science, Vol. 346, Issue 6208 https://doi.org/10.1126/science.1257998	journal	October 2014
Three-Dimensional Architecture of Grana and Stroma Thylakoids of Higher Plants as Determined by Electron Tomography Austin, Jotham R.; Staehelin, L. Andrew Plant Physiology, Vol. 155, Issue 4 https://doi.org/10.1104/pp.110.170647	journal	January 2011
Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer Wood, William H. J.; MacGregor-Chatwin, Craig; Barnett, Samuel F. H. Nature Plants, Vol. 4, Issue 2 https://doi.org/10.1038/s41477-017-0092-7	journal	January 2018
Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography Engel, Benjamin D.; Schaffer, Miroslava; Kuhn Cuellar, Luis eLife, Vol. 4 https://doi.org/10.7554/eLife.04889	journal	January 2015
High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana Kouřil, Roman; Wientjes, Emilie; Bultema, Jelle B. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3 https://doi.org/10.1016/j.bbabio.2012.12.003	journal	March 2013
Photosystems and global effects of oxygenic photosynthesis Nelson, Nathan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 8 https://doi.org/10.1016/j.bbabio.2010.10.011	journal	August 2011
Excitation Migration, Quenching, and Regulation of Photosynthetic Light Harvesting in Photosystem II Valkunas, Leonas; Chmeliov, Jevgenij; Trinkunas, Gediminas The Journal of Physical Chemistry B, Vol. 115, Issue 29 https://doi.org/10.1021/jp2014385	journal	July 2011
Excitation Energy Transfer and Trapping in Higher Plant Photosystem II Complexes with Different Antenna Sizes Caffarri, Stefano; Broess, Koen; Croce, Roberta Biophysical Journal, Vol. 100, Issue 9 https://doi.org/10.1016/j.bpj.2011.03.049	journal	May 2011
Structural Correlates of Cytoplasmic and Chloroplast Lipid Body Synthesis in Chlamydomonas reinhardtii and Stimulation of Lipid Body Production with Acetate Boost Goodson, Carrie; Roth, Robyn; Wang, Zi Teng Eukaryotic Cell, Vol. 10, Issue 12 https://doi.org/10.1128/EC.05242-11	journal	October 2011
Photoprotective Energy Dissipation Involves the Reorganization of Photosystem II Light-Harvesting Complexes in the Grana Membranes of Spinach Chloroplasts Johnson, Matthew P.; Goral, Tomasz K.; Duffy, Christopher D. P. The Plant Cell, Vol. 23, Issue 4 https://doi.org/10.1105/tpc.110.081646	journal	April 2011
Three-Dimensional Organization of Higher-Plant Chloroplast Thylakoid Membranes Revealed by Electron Tomography Shimoni, Eyal; Rav-Hon, Ophir; Ohad, Itzhak The Plant Cell, Vol. 17, Issue 9 https://doi.org/10.1105/tpc.105.035030	journal	July 2005
The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis Shapiguzov, A.; Ingelsson, B.; Samol, I. Proceedings of the National Academy of Sciences, Vol. 107, Issue 10 https://doi.org/10.1073/pnas.0913810107	journal	February 2010
SIMcheck: a Toolbox for Successful Super-resolution Structured Illumination Microscopy Ball, Graeme; Demmerle, Justin; Kaufmann, Rainer Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15915	journal	November 2015
Regulation of Light Harvesting in Green Plants Horton, P.; Ruban, A. V.; Walters, R. G. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.arplant.47.1.655	journal	June 1996
Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production Roth, Melissa S.; Cokus, Shawn J.; Gallaher, Sean D. Proceedings of the National Academy of Sciences, Vol. 114, Issue 21 https://doi.org/10.1073/pnas.1619928114	journal	May 2017
Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii Schottkowski, M.; Peters, M.; Zhan, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1209860109	journal	November 2012
Light stress and photoprotection in Chlamydomonas reinhardtii Erickson, Erika; Wakao, Setsuko; Niyogi, Krishna K. The Plant Journal, Vol. 82, Issue 3 https://doi.org/10.1111/tpj.12825	journal	March 2015
Characterization of damage to the D1 protein of photosystem II under photoinhibitory illumination in non-phosphorylated and phosphorylated thylakoid membranes Mizusawa, N.; Yamamoto, N.; Miyao, M. Journal of Photochemistry and Photobiology B: Biology, Vol. 48, Issue 2-3 https://doi.org/10.1016/S1011-1344(99)00023-8	journal	February 1999
Tagged Mutagenesis and Gene-trap in the Moss, Physcomitrella patens by Shuttle Mutagenesis Nishiyama, T. DNA Research, Vol. 7, Issue 1 https://doi.org/10.1093/dnares/7.1.9	journal	January 2000
During State 1 to State 2 Transition in Arabidopsis thaliana , the Photosystem II Supercomplex Gets Phosphorylated but Does Not Disassemble Wientjes, Emilie; Drop, Bartlomiej; Kouřil, Roman Journal of Biological Chemistry, Vol. 288, Issue 46 https://doi.org/10.1074/jbc.M113.511691	journal	October 2013
Functional Genomics of Eukaryotic Photosynthesis Using Insertional Mutagenesis of Chlamydomonas reinhardtii Dent, Rachel M.; Haglund, Cat M.; Chin, Brian L. Plant Physiology, Vol. 137, Issue 2 https://doi.org/10.1104/pp.104.055244	journal	January 2005
Multi-Level Light Capture Control in Plants and Green Algae Wobbe, Lutz; Bassi, Roberto; Kruse, Olaf Trends in Plant Science, Vol. 21, Issue 1 https://doi.org/10.1016/j.tplants.2015.10.004	journal	January 2016
A Novel Type of Chloroplast Stromal Hexokinase Is the Major Glucose-phosphorylating Enzyme in the Moss Physcomitrella patens Olsson, Tina; Thelander, Mattias; Ronne, Hans Journal of Biological Chemistry, Vol. 278, Issue 45 https://doi.org/10.1074/jbc.M306265200	journal	August 2003
Light‐harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Goral, Tomasz K.; Johnson, Matthew P.; Duffy, Christopher D. P. The Plant Journal, Vol. 69, Issue 2 https://doi.org/10.1111/j.1365-313X.2011.04790.x	journal	October 2011
Cryo-Electron Tomography: Can it Reveal the Molecular Sociology of Cells in Atomic Detail? Beck, Martin; Baumeister, Wolfgang Trends in Cell Biology, Vol. 26, Issue 11 https://doi.org/10.1016/j.tcb.2016.08.006	journal	November 2016
The crosstalk between astaxanthin, fatty acids and reactive oxygen species in heterotrophic Chlorella zofingiensis Zhang, Zhao; Sun, Dongzhe; Mao, Xuemei Algal Research, Vol. 19 https://doi.org/10.1016/j.algal.2016.08.015	journal	November 2016
PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches Niyogi, Krishna K. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.333	journal	June 1999
Effects of Acetate on Facultative Autotrophy in Chlamydomonas reinhardtii Assessed by Photosynthetic Measurements and Stable Isotope Analyses Heifetz, Peter B.; Förster, Britta; Osmond, C. Barry Plant Physiology, Vol. 122, Issue 4 https://doi.org/10.1104/pp.122.4.1439	journal	April 2000
Identification of pH-sensing Sites in the Light Harvesting Complex Stress-related 3 Protein Essential for Triggering Non-photochemical Quenching in Chlamydomonas reinhardtii Ballottari, Matteo; Truong, Thuy B.; De Re, Eleonora Journal of Biological Chemistry, Vol. 291, Issue 14 https://doi.org/10.1074/jbc.M115.704601	journal	January 2016
Phosphorylation of Photosystem II Controls Functional Macroscopic Folding of Photosynthetic Membranes in Arabidopsis Fristedt, Rikard; Willig, Adrian; Granath, Pontus The Plant Cell, Vol. 21, Issue 12 https://doi.org/10.1105/tpc.109.069435	journal	December 2009
Live-cell visualization of excitation energy dynamics in chloroplast thylakoid structures Iwai, Masakazu; Yokono, Makio; Kurokawa, Kazuo Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29940	journal	July 2016
Regulation and Dynamics of the Light-Harvesting System Rochaix, Jean-David Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040226	journal	April 2014
Strategic and practical guidelines for successful structured illumination microscopy Demmerle, Justin; Innocent, Cassandravictoria; North, Alison J. Nature Protocols, Vol. 12, Issue 5 https://doi.org/10.1038/nprot.2017.019	journal	April 2017
Effect of biomass concentration on secondary carotenoids and triacylglycerol (TAG) accumulation in nitrogen-depleted Chlorella zofingiensis Mulders, Kim J. M.; Janssen, Jorijn H.; Martens, Dirk E. Algal Research, Vol. 6 https://doi.org/10.1016/j.algal.2014.08.006	journal	October 2014
Balance of power: a view of the mechanism of photosynthetic state transitions Haldrup, Anna; Jensen, Poul Erik; Lunde, Christina Trends in Plant Science, Vol. 6, Issue 7 https://doi.org/10.1016/S1360-1385(01)01953-7	journal	July 2001
A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism Mackinder, Luke C. M.; Chen, Chris; Leib, Ryan D. Cell, Vol. 171, Issue 1 https://doi.org/10.1016/j.cell.2017.08.044	journal	September 2017
Revisiting the Algal “Chloroplast Lipid Droplet”: The Absence of an Entity That Is Unlikely to Exist Moriyama, Takashi; Toyoshima, Masakazu; Saito, Masakazu Plant Physiology, Vol. 176, Issue 2 https://doi.org/10.1104/pp.17.01512	journal	October 2017
Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production Roth, Melissa S.; Cokus, Shawn J.; Gallaher, Sean D. Proceedings of the National Academy of Sciences, Vol. 114, Issue 21 https://doi.org/10.1073/pnas.1619928114	journal	May 2017
High-resolution restoration of 3D structures from widefield images with extreme low signal-to-noise-ratio Arigovindan, M.; Fung, J. C.; Elnatan, D. Proceedings of the National Academy of Sciences, Vol. 110, Issue 43 https://doi.org/10.1073/pnas.1315675110	journal	October 2013
Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage Ruban, Alexander V. Plant Physiology, Vol. 170, Issue 4 https://doi.org/10.1104/pp.15.01935	journal	February 2016
State transitions and light adaptation require chloroplast thylakoid protein kinase STN7 Bellafiore, Stéphane; Barneche, Frédy; Peltier, Gilles Nature, Vol. 433, Issue 7028 https://doi.org/10.1038/nature03286	journal	February 2005
Behavior of mitochondria in synchronized cells of Chlamydomonas reinhardtii (Chlorophyta) Ehara, T.; Osafune, T.; Hase, E. Journal of Cell Science, Vol. 108, Issue 2 https://doi.org/10.1242/jcs.108.2.499	journal	February 1995
The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis Shapiguzov, A.; Ingelsson, B.; Samol, I. National Academy of Sciences https://doi.org/10.5167/uzh-80910	text	January 2010
Role of Plastid Protein Phosphatase TAP38 in LHCII Dephosphorylation and Thylakoid Electron Flow Pribil, Mathias; Pesaresi, Paolo; Hertle, Alexander Universitätsbibliothek der Ludwig-Maximilians-Universität München https://doi.org/10.5282/ubm/epub.14710	text	January 2010

Cited By (5)

Regulation of Oxygenic Photosynthesis during Trophic Transitions in the Green Alga Chromochloris zofingiensis Roth, Melissa S.; Gallaher, Sean D.; Westcott, Daniel J. The Plant Cell, Vol. 31, Issue 3 https://doi.org/10.1105/tpc.18.00742	journal	February 2019
Macroorganisation and flexibility of thylakoid membranes Lambrev, Petar H.; Akhtar, Parveen Biochemical Journal, Vol. 476, Issue 20 https://doi.org/10.1042/bcj20190080	journal	October 2019
Chloroplast ultrastructure in plants Kirchhoff, Helmut New Phytologist, Vol. 223, Issue 2 https://doi.org/10.1111/nph.15730	journal	March 2019
Spatial organization of thylakoid network in higher plants Kowalewska, Łucja; Bykowski, Michał; Mostowska, Agnieszka Botany Letters, Vol. 166, Issue 3 https://doi.org/10.1080/23818107.2019.1619195	journal	May 2019
Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga Roth, Melissa S.; Westcott, Daniel J.; Iwai, Masakazu Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0577-1	journal	September 2019