Granal thylakoid structure and function: explaining an enduring mystery of higher plants

Gu, Lianhong; Grodzinski, Bernard; Han, Jimei; Marie, Telesphore; Zhang, Yong‐Jiang; Song, Yang C.; Sun, Ying

doi:10.1111/nph.18371

Title: Granal thylakoid structure and function: explaining an enduring mystery of higher plants

Journal Article · 02 August 2022 · New Phytologist

DOI: https://doi.org/10.1111/nph.18371 · OSTI ID:1879566

^[1]; Grodzinski, Bernard ^[2];

^[3]; Marie, Telesphore ^[2];

^[4];

^[5];

^[3]

Environmental Sciences Division and Climate Change Science Institute Oak Ridge National Laboratory Oak Ridge TN 37831 USA
Department of Plant Agriculture University of Guelph Guelph ON N1G 2W1 Canada
School of Integrative Plant Science Cornell University Ithaca NY 14853 USA
School of Biology and Ecology University of Maine Orono ME 04469 USA
Department of Hydrology and Atmospheric Sciences University of Arizona Tucson AZ 85721 USA

Summary In higher plants, photosystems II and I are found in grana stacks and unstacked stroma lamellae, respectively. To connect them, electron carriers negotiate tortuous multi‐media paths and are subject to macromolecular blocking. Why does evolution select an apparently unnecessary, inefficient bipartition? Here we systematically explain this perplexing phenomenon. We propose that grana stacks, acting like bellows in accordions, increase the degree of ultrastructural control on photosynthesis through thylakoid swelling/shrinking induced by osmotic water fluxes. This control coordinates with variations in stomatal conductance and the turgor of guard cells, which act like an accordion's air button. Thylakoid ultrastructural dynamics regulate macromolecular blocking/collision probability, direct diffusional pathlengths, division of function of Cytochrome b ₆ f complex between linear and cyclic electron transport, luminal pH via osmotic water fluxes, and the separation of pH dynamics between granal and lamellar lumens in response to environmental variations. With the two functionally asymmetrical photosystems located distantly from each other, the ultrastructural control, nonphotochemical quenching, and carbon‐reaction feedbacks maximally cooperate to balance electron transport with gas exchange, provide homeostasis in fluctuating light environments, and protect photosystems in drought. Grana stacks represent a dry/high irradiance adaptation of photosynthetic machinery to improve fitness in challenging land environments. Our theory unifies many well‐known but seemingly unconnected phenomena of thylakoid structure and function in higher plants.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: Cornell Initiative for Digital Agriculture Research Innovation; National Science Foundation; Ontario Ministry of Agriculture, Food and Rural Affairs; USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER); United States Department of Agriculture

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1879566

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 2 Vol. 236; ISSN 0028-646X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (74)

Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy Li, Meng; Mukhopadhyay, Roma; Svoboda, Václav Plant Direct, Vol. 4, Issue 11 https://doi.org/10.1002/pld3.280	journal	November 2020
Grana stacking and protection of Photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: An hypothesis Anderson, Jan M.; Aro, Eva-Mari Photosynthesis Research, Vol. 41, Issue 2 https://doi.org/10.1007/BF00019409	journal	August 1994
Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins Bj�rkman, Olle; Demmig, Barbara Planta, Vol. 170, Issue 4 https://doi.org/10.1007/BF00402983	journal	April 1987
Measurement of photochemical quenching of absorbed quanta in photosystem I of intact leaves using simultaneous measurements of absorbance changes at 830 nm and thermal dissipation Bukhov, Nikolai G.; Carpentier, Robert Planta, Vol. 216, Issue 4 https://doi.org/10.1007/s00425-002-0886-2	journal	February 2003
Dynamic flexibility in the structure and function of photosystem II in higher plant thylakoid membranes: the grana enigma Anderson, Jan M.; Chow, Wah Soon; De Las Rivas, Javier Photosynthesis Research, Vol. 98, Issue 1-3 https://doi.org/10.1007/s11120-008-9381-3	journal	October 2008
Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Laisk, Agu; Talts, Eero; Oja, Vello Photosynthesis Research, Vol. 103, Issue 2 https://doi.org/10.1007/s11120-009-9513-4	journal	December 2009
Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts Andersson, Bertil; Anderson, Jan M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 593, Issue 2 https://doi.org/10.1016/0005-2728(80)90078-X	journal	December 1980
The plastoquinone diffusion coefficient in chloroplasts and its mechanistic implications Blackwell, Mary; Gibas, Cynthia; Gygax, Scott Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1183, Issue 3 https://doi.org/10.1016/0005-2728(94)90081-7	journal	January 1994
The swelling behaviour of clays Madsen, Fritz T.; Müller-Vonmoos, Max Applied Clay Science, Vol. 4, Issue 2 https://doi.org/10.1016/0169-1317(89)90005-7	journal	June 1989
Why do thylakoid membranes from higher plants form grana stacks? Trissl, Hans-Wilhelm; Wilhelm, Christian Trends in Biochemical Sciences, Vol. 18, Issue 11 https://doi.org/10.1016/0968-0004(93)90136-B	journal	November 1993
Vertical variability of spectral ratios in a mature mixed forest stand Hertel, Christian; Leuchner, Michael; Menzel, Annette Agricultural and Forest Meteorology, Vol. 151, Issue 8 https://doi.org/10.1016/j.agrformet.2011.03.013	journal	August 2011
Quantification of photosystem I and II in different parts of the thylakoid membrane from spinach Danielsson, Ravi; Albertsson, Per-Åke; Mamedov, Fikret Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1608, Issue 1 https://doi.org/10.1016/j.bbabio.2003.10.005	journal	January 2004
Molecular mechanisms of photodamage in the Photosystem II complex Vass, Imre Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1 https://doi.org/10.1016/j.bbabio.2011.04.014	journal	January 2012
Oxidation of plastohydroquinone by photosystem II and by dioxygen in leaves Laisk, Agu; Eichelmann, Hillar; Oja, Vello Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 6-7 https://doi.org/10.1016/j.bbabio.2015.03.003	journal	June 2015
The mechanism of cyclic electron flow Nawrocki, W. J.; Bailleul, B.; Picot, D. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 5 https://doi.org/10.1016/j.bbabio.2018.12.005	journal	May 2019
Cytochrome b6f – Orchestrator of photosynthetic electron transfer Malone, Lorna A.; Proctor, Matthew S.; Hitchcock, Andrew Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1862, Issue 5 https://doi.org/10.1016/j.bbabio.2021.148380	journal	May 2021
Assessment of the requirement for aquaporins in the thylakoid membrane of plant chloroplasts to sustain photosynthetic water oxidation Beebo, Azeez; Mathai, John C.; Schoefs, Benoît FEBS Letters, Vol. 587, Issue 14 https://doi.org/10.1016/j.febslet.2013.05.046	journal	May 2013
Alternative electron transport pathways in photosynthesis: a confluence of regulation Alric, Jean; Johnson, Xenie Current Opinion in Plant Biology, Vol. 37 https://doi.org/10.1016/j.pbi.2017.03.014	journal	June 2017
The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways Tikhonov, Alexander N. Plant Physiology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.plaphy.2013.12.011	journal	August 2014
Function and evolution of grana Mullineaux, Conrad W. Trends in Plant Science, Vol. 10, Issue 11 https://doi.org/10.1016/j.tplants.2005.09.001	journal	November 2005
Sublocalization of Cytochrome b6f Complexes in Photosynthetic Membranes Kirchhoff, Helmut; Li, Meng; Puthiyaveetil, Sujith Trends in Plant Science, Vol. 22, Issue 7 https://doi.org/10.1016/j.tplants.2017.04.004	journal	July 2017
Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction Jegerschoeld, Caroline; Virgin, Ivar; Styring, Stenbjoern Biochemistry, Vol. 29, Issue 26 https://doi.org/10.1021/bi00478a010	journal	July 1990
Probing the Organization of Photosystem II in Photosynthetic Membranes by Atomic Force Microscopy † Kirchhoff, Helmut; Lenhert, Steven; Büchel, Claudia Biochemistry, Vol. 47, Issue 1 https://doi.org/10.1021/bi7017877	journal	January 2008
A voltage-dependent chloride channel fine-tunes photosynthesis in plants Herdean, Andrei; Teardo, Enrico; Nilsson, Anders K. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11654	journal	May 2016
Surface charge dynamics in photosynthetic membranes and the structural consequences Puthiyaveetil, Sujith; van Oort, Bart; Kirchhoff, Helmut Nature Plants, Vol. 3, Issue 4 https://doi.org/10.1038/nplants.2017.20	journal	March 2017
Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection Li, Meng; Svoboda, Vaclav; Davis, Geoffry Nature Plants, Vol. 7, Issue 7 https://doi.org/10.1038/s41477-021-00947-5	journal	June 2021
Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue Chow, Wah Soon; Kim, Eun-Ha; Horton, Peter Photochemical & Photobiological Sciences, Vol. 4, Issue 12 https://doi.org/10.1039/b507310n	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
Regulation of cyclic and linear electron flow in higher plants Joliot, Pierre; Johnson, Giles N. Proceedings of the National Academy of Sciences, Vol. 108, Issue 32 https://doi.org/10.1073/pnas.1110189108	journal	July 2011
Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis Kunz, H. -H.; Gierth, M.; Herdean, A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1323899111	journal	May 2014
Regulation of photosystem I light harvesting by zeaxanthin Ballottari, M.; Alcocer, M. J. P.; D'Andrea, C. Proceedings of the National Academy of Sciences, Vol. 111, Issue 23 https://doi.org/10.1073/pnas.1404377111	journal	May 2014
Alternative outlets for sustaining photosynthetic electron transport during dark-to-light transitions Saroussi, Shai; Karns, Devin A. J.; Thomas, Dylan C. Proceedings of the National Academy of Sciences, Vol. 116, Issue 23 https://doi.org/10.1073/pnas.1903185116	journal	May 2019
Fundamental helical geometry consolidates the plant photosynthetic membrane Bussi, Yuval; Shimoni, Eyal; Weiner, Allon Proceedings of the National Academy of Sciences, Vol. 116, Issue 44 https://doi.org/10.1073/pnas.1905994116	journal	October 2019
Plastocyanin is the long-range electron carrier between photosystem II and photosystem I in plants Höhner, Ricarda; Pribil, Mathias; Herbstová, Miroslava Proceedings of the National Academy of Sciences, Vol. 117, Issue 26 https://doi.org/10.1073/pnas.2005832117	journal	June 2020
Determining RuBisCO activation kinetics and other rate and equilibrium constants by simultaneous multiple non-linear regression of a kinetic model McNevin, Dennis; von Caemmerer, Susanne; Farquhar, Graham Journal of Experimental Botany, Vol. 57, Issue 14 https://doi.org/10.1093/jxb/erl156	journal	October 2006
Photosynthetic control of electron transport and the regulation of gene expression Foyer, Christine H.; Neukermans, Jenny; Queval, Guillaume Journal of Experimental Botany, Vol. 63, Issue 4 https://doi.org/10.1093/jxb/ers013	journal	February 2012
Structure and dynamics of thylakoids in land plants Pribil, Mathias; Labs, Mathias; Leister, Dario Journal of Experimental Botany, Vol. 65, Issue 8 https://doi.org/10.1093/jxb/eru090	journal	March 2014
Impact of the ion transportome of chloroplasts on the optimization of photosynthesis Szabò, Ildikò; Spetea, Cornelia Journal of Experimental Botany, Vol. 68, Issue 12 https://doi.org/10.1093/jxb/erx063	journal	March 2017
Cyclic Electron Flow within PSII Protects PSII from its Photoinhibition in Thylakoid Membranes from Spinach Chloroplasts Miyake, Chikahiro; Okamura, Mitsutaka Plant and Cell Physiology, Vol. 44, Issue 4 https://doi.org/10.1093/pcp/pcg053	journal	April 2003
Gymnosperms Have Increased Capacity for Electron Leakage to Oxygen (Mehler and PTOX reactions) in Photosynthesis Compared with Angiosperms Shirao, Masayoshi; Kuroki, Shu; Kaneko, Kaoru Plant and Cell Physiology, Vol. 54, Issue 7 https://doi.org/10.1093/pcp/pct066	journal	May 2013
Chloride: from Nutrient to Toxicant Geilfus, Christoph-Martin Plant and Cell Physiology, Vol. 59, Issue 5 https://doi.org/10.1093/pcp/pcy071	journal	April 2018
Sunflecks in trees and forests: from photosynthetic physiology to global change biology Way, D. A.; Pearcy, R. W. Tree Physiology, Vol. 32, Issue 9 https://doi.org/10.1093/treephys/tps064	journal	August 2012
Is the Donnan effect sufficient to explain swelling in brain tissue slices? Lang, Georgina E.; Stewart, Peter S.; Vella, Dominic Journal of The Royal Society Interface, Vol. 11, Issue 96 https://doi.org/10.1098/rsif.2014.0123	journal	July 2014
Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase Badger, Murray R.; von Caemmerer, Susanne; Ruuska, Sari Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402 https://doi.org/10.1098/rstb.2000.0704	journal	October 2000
Towards elucidation of dynamic structural changes of plant thylakoid architecture Anderson, Jan M.; Horton, Peter; Kim, Eun-Ha Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1608 https://doi.org/10.1098/rstb.2012.0373	journal	December 2012
Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts Kirchhoff, Helmut Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1640 https://doi.org/10.1098/rstb.2013.0225	journal	April 2014
Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions: Figure 1. Asada, Kozi Plant Physiology, Vol. 141, Issue 2 https://doi.org/10.1104/pp.106.082040	journal	June 2006
The Importance of Energy Balance in Improving Photosynthetic Productivity Kramer, David M.; Evans, John R. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.166652	journal	November 2010
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
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
Temporal Dynamics of Stomatal Behavior: Modeling and Implications for Photosynthesis and Water Use Vialet-Chabrand, Silvere R. M.; Matthews, Jack S. A.; McAusland, Lorna Plant Physiology, Vol. 174, Issue 2 https://doi.org/10.1104/pp.17.00125	journal	March 2017
Mitochondria Affect Photosynthetic Electron Transport and Photosensitivity in a Green Alga Larosa, Véronique; Meneghesso, Andrea; La Rocca, Nicoletta Plant Physiology, Vol. 176, Issue 3 https://doi.org/10.1104/pp.17.01249	journal	December 2017
The Photosystem II Repair Cycle Requires FtsH Turnover through the EngA GTPase Kato, Yusuke; Hyodo, Kiwamu; Sakamoto, Wataru Plant Physiology, Vol. 178, Issue 2 https://doi.org/10.1104/pp.18.00652	journal	August 2018
Photosynthetic Quantum Yield Dynamics: From Photosystems to Leaves Hogewoning, Sander W.; Wientjes, Emilie; Douwstra, Peter The Plant Cell, Vol. 24, Issue 5 https://doi.org/10.1105/tpc.112.097972	journal	May 2012
The dissipation of excess excitation energy in British plant species Johnson, G. N.; Young, A. J.; Scholes, J. D. Plant, Cell and Environment, Vol. 16, Issue 6 https://doi.org/10.1111/j.1365-3040.1993.tb00485.x	journal	August 1993
Composition, architecture and dynamics of the photosynthetic apparatus in higher plants: The photosynthetic apparatus in higher plants Nevo, Reinat; Charuvi, Dana; Tsabari, Onie The Plant Journal, Vol. 70, Issue 1 https://doi.org/10.1111/j.1365-313X.2011.04876.x	journal	March 2012
Photoinhibition of photosystem I Sonoike, Kintake Physiologia Plantarum, Vol. 142, Issue 1 https://doi.org/10.1111/j.1399-3054.2010.01437.x	journal	April 2011
Closing gaps: linking elements that control stomatal movement Kollist, Hannes; Nuhkat, Maris; Roelfsema, M. Rob G. New Phytologist, Vol. 203, Issue 1 https://doi.org/10.1111/nph.12832	journal	May 2014
Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms Ilík, Petr; Pavlovič, Andrej; Kouřil, Roman New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14536	journal	March 2017
Balancing protection and efficiency in the regulation of photosynthetic electron transport across plant evolution Alboresi, Alessandro; Storti, Mattia; Morosinotto, Tomas New Phytologist, Vol. 221, Issue 1 https://doi.org/10.1111/nph.15372	journal	August 2018
Chloroplast ultrastructure in plants Kirchhoff, Helmut New Phytologist, Vol. 223, Issue 2 https://doi.org/10.1111/nph.15730	journal	March 2019
How do stomata respond to water status? Buckley, Thomas N. New Phytologist, Vol. 224, Issue 1 https://doi.org/10.1111/nph.15899	journal	June 2019
The structural and functional domains of plant thylakoid membranes Koochak, Haniyeh; Puthiyaveetil, Sujith; Mullendore, Daniel L. The Plant Journal, Vol. 97, Issue 3 https://doi.org/10.1111/tpj.14127	journal	November 2018
Dynamic non‐photochemical quenching in plants: from molecular mechanism to productivity Murchie, Erik H.; Ruban, Alexander V. The Plant Journal, Vol. 101, Issue 4 https://doi.org/10.1111/tpj.14601	journal	December 2019
Stomatal Opening: Role of Potassium Uptake by Guard Cells Fischer, R. A. Science, Vol. 160, Issue 3829 https://doi.org/10.1126/science.160.3829.784	journal	May 1968
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth Science, Vol. 354, Issue 6314 https://doi.org/10.1126/science.aai8878	journal	November 2016
Plastoglobuli: Plastid Microcompartments with Integrated Functions in Metabolism, Plastid Developmental Transitions, and Environmental Adaptation van Wijk, Klaas J.; Kessler, Felix Annual Review of Plant Biology, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-arplant-043015-111737	journal	April 2017
Physiological Functions of Cyclic Electron Transport Around Photosystem I in Sustaining Photosynthesis and Plant Growth Yamori, Wataru; Shikanai, Toshiharu Annual Review of Plant Biology, Vol. 67, Issue 1 https://doi.org/10.1146/annurev-arplant-043015-112002	journal	April 2016
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo Baker, Neil R. Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092759	journal	June 2008
Osmotic Swelling of Vesicles: Its Role in the Fusion of Vesicles with Planar Phospholipid Bilayer Membranes and its Possible Role in Exocytosis Finkelstein, A.; Zimmerberg, J.; Cohen, F. S. Annual Review of Physiology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.ph.48.030186.001115	journal	October 1986
Plant Photosystem I – The Most Efficient Nano-Photochemical Machine Nelson, Nathan Journal of Nanoscience and Nanotechnology, Vol. 9, Issue 3 https://doi.org/10.1166/jnn.2009.SI01	journal	March 2009
A Comparison Between Plant Photosystem I and Photosystem II Architecture and Functioning Caffarri, Stefano; Tibiletti, Tania; Jennings, Robert Current Protein & Peptide Science, Vol. 15, Issue 4 https://doi.org/10.2174/1389203715666140327102218	journal	April 2014
Live-cell Microscopy and Fluorescence-based Measurement of Luminal pH in Intracellular Organelles Ma, Li; Ouyang, Qing; Werthmann, Gordon C. Frontiers in Cell and Developmental Biology, Vol. 5 https://doi.org/10.3389/fcell.2017.00071	journal	August 2017
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

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