In natural environments, plants are exposed to rapidly changing light. Maintaining photosynthetic efficiency while avoiding photodamage requires equally rapid regulation of photoprotective mechanisms. We asked what the operation frequency range of regulation is in which plants can efficiently respond to varying light. Chlorophyll fluorescence, P700, plastocyanin, and ferredoxin responses of wild-types Arabidopsis thaliana were measured in oscillating light of various frequencies. We also investigated the npq1 mutant lacking violaxanthin de-epoxidase, the npq4 mutant lacking PsbS protein, and the mutants crr2-2, and pgrl1ab impaired in different pathways of the cyclic electron transport. The fastest was the PsbS-regulation responding to oscillation periods longer than 10 s. Processes involving violaxanthin de-epoxidase dampened changes in chlorophyll fluorescence in oscillation periods of 2 min or longer. Knocking out the PGR5/PGRL1 pathway strongly reduced variations of all monitored parameters, probably due to congestion in the electron transport. Incapacitating the NDH-like pathway only slightly changed the photosynthetic dynamics. Our observations are consistent with the hypothesis that nonphotochemical quenching in slow light oscillations involves violaxanthin de-epoxidase to produce, presumably, a largely stationary level of zeaxanthin. We interpret the observed dynamics of photosystem I components as being formed in slow light oscillations partially by thylakoid remodeling that modulates the redox rates.

Department of Biological Sciences Macquarie University North Ryde NSW 2109 Australia

Department of Biophysics Faculty of Science Palacký University Šlechtitelů 27 783 71 Olomouc Czech Republic

Department of Physics and Astronomy Faculty of Science Vrije Universiteit Amsterdam De Boelelaan 1105 NL 1081 HV Amsterdam the Netherlands

Institute of Bio and Geosciences Plant Sciences Forschungszentrum Jülich Wilhelm Johnen Straße D 52428 Jülich Germany

MSU DOE Plant Research Laboratory Michigan State University East Lansing MI 48824 USA

PASTEUR Department of Chemistry École Normale Supérieure Université PSL Sorbonne Université CNRS 24 rue Lhomond 75005 Paris France

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von Bismarck T, Korkmaz K, Ruß J, Skurk K, Kaiser E, Correa Galvis V, Cruz JA, Strand DD, Köhl K, Eirich J et al. 2023. Light acclimation interacts with thylakoid ion transport to govern the dynamics of photosynthesis in Arabidopsis. New Phytologist 237: 160-176.

Chazdon RL, Pearcy RW. 1991. The importance of sunflecks for forest understory plants - photosynthetic machinery appears adapted to brief, unpredictable periods of radiation. Bioscience 41: 760-766.

Colombo M, Suorsa M, Rossi F, Ferrari R, Tadini L, Barbato R, Pesaresi P. 2016. Photosynthesis control: an underrated short-term regulatory mechanism essential for plant viability. Plant Signaling & Behavior 11: e1165382.

Cruz JA, Savage LJ, Zegarac R, Hall CC, Satoh-Cruz M, Davis GA, Kovac WK, Chen J, Kramer DM. 2016. Dynamic environmental photosynthetic imaging reveals emergent phenotypes. Cell Systems 2: 365-377.

DalCorso G, Pesaresi P, Masiero S, Aseeva E, Nemann DS, Finazzi G, Joliot P, Barbato R, Leister D. 2008. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132: 273-285.

De Souza AP, Burgess SJ, Doran L, Hansen J, Manukyan L, Maryn N, Gotarkar D, Leonelli L, Niyogi KK, Long SP. 2022. Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. Science 377: 541-854.

Delieu TJ, Walker DA. 1983. Simultaneous measurement of oxygen evolution and chlorophyll fluorescence from leaf pieces. Plant Physiology 73: 534-541.

Demmig-Adams B, Adams WW, Garab G, Govindjee G. 2014. Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria preface. Dordrecht, the Netherlands: Springer Netherlands.

Frommolt R, Goss R, Wilhelm C. 2001. The de-epoxidase and epoxidase reactions of Mantoniella squamata (Prasinophyceae) exhibit different substrate-specific reaction kinetics compared to spinach. Planta 213: 446-456.

Ganusov VV. 2016. Strong inference in mathematical modeling: a method for robust science in the twenty-first century. Frontiers in Microbiology 7: 1131.

Gilmore AM. 1997. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99: 197-209.

Graham PJ, Nguyen B, Burdyny T, Sinton D. 2017. A penalty on photosynthetic growth in fluctuating light. Scientific Reports 7: 12513.

Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T. 2003. A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. The Plant Journal 36: 541-549.

Hepworth C, Wood WHJ, Emrich-Mills TZ, Proctor MS, Casson S, Johnson MP. 2021. Dynamic thylakoid stacking and state transitions work synergistically to avoid acceptor-side limitation of photosystem I. Nature Plants 7: 87-98.

Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D. 2013. PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Molecular Cell 49: 511-523.

Höhner R, Pribil M, Herbstová M, Lopez LS, Kunz HH, Li M, Wood M, Svoboda V, Puthiyaveetil S, Leister D et al. 2020. Plastocyanin is the long-range electron carrier between photosystem II and photosystem I in plants. Proceedings of the National Academy of Sciences, USA 117: 15354-15362.

Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P. 2009. Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chemical Physics Letters 483: 262-267.

Horton P, Ruban A. 2005. Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. Journal of Experimental Botany 56: 365-373.

Jahns P, Holzwarth AR. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta - Bioenergetics 1817: 182-193.

Johnson JE, Berry JA. 2021. The role of cytochrome b6f in the control of steady-state photosynthesis: a conceptual and quantitative model. Photosynthesis Research 148: 101-136.

Johnson MP, Wientjes E. 2020. The relevance of dynamic thylakoid organisation to photosynthetic regulation. Biochimica et Biophysica Acta - Bioenergetics 1861: 148039.

Joliot P, Lavergne J, Béal D. 1992. Plastoquinone compartmentation in chloroplasts. I. Evidence for domains with different rates of photo-reduction. Biochimica et Biophysica Acta - Bioenergetics 1101: 1-12.

Kaiser E, Morales A, Harbinson J. 2018. Fluctuating light takes crop photosynthesis on a rollercoaster ride. Plant Physiology 176: 977-989.

Kaiser E, Morales A, Harbinson J, Heuvelink E, Prinzenberg AE, Marcelis LF. 2016. Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana. Scientific Reports 6: 31252.

Kihara M, Ushijima T, Yamagata Y, Tsuruda Y, Higa T, Abiko T, Kubo T, Wada M, Suetsugu N, Gotoh E. 2020. Light-induced chloroplast movements in Oryza species. Journal of Plant Research 133: 525-535.

Kirchhoff H, Hall C, Wood M, Herbstová M, Tsabari O, Nevo R, Charuvi D, Shimoni E, Reich Z. 2011. Dynamic control of protein diffusion within the granal thylakoid lumen. Proceedings of the National Academy of Sciences, USA 108: 20248-20253.

Kirchhoff H, Horstmann S, Weis E. 2000. Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochimica et Biophysica Acta - Bioenergetics 1459: 148-168.

Kitano H. 2001. Foundations of systems biology. Cambridge, MA, USA; London, UK: The MIT Press.

Klughammer C, Schreiber U. 2016. Deconvolution of ferredoxin, plastocyanin, and P700 transmittance changes in intact leaves with a new type of kinetic LED array spectrophotometer. Photosynthesis Research 128: 195-214.

Knapp AK, Smith WK. 1987. Stomatal and photosynthetic responses during sun/shade transitions in subalpine plants: influence on water use efficiency. Oecologia 74: 62-67.

Kono M, Noguchi K, Terashima I. 2014. Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant and Cell Physiology 55: 990-1004.

Kono M, Terashima I. 2014. Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. Journal of Photochemistry and Photobiology B: Biology 137: 89-99.

Kouřil R, Strouhal O, Nosek L, Lenobel R, Chamrád I, Boekema EJ, Šebela M, Ilík P. 2014. Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. The Plant Journal 77: 568-576.

Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP. 2016. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354: 587-860.

Külheim C, Ågren J, Jansson S. 2002. Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91-93.

Laughlin TG, Savage DF, Davies KM. 2020. Recent advances on the structure and function of NDH-1: the complex I of oxygenic photosynthesis. Biochimica et Biophysica Acta - Bioenergetics 1861: 148254.

Lazár D, Kaňa R, Klinkovský T, Nauš J. 2005. Experimental and theoretical study on high temperature induced changes in chlorophyll a fluorescence oscillations in barley leaves upon 2% CO2. Photosynthetica 43: 13-27.

Lazár D, Niu Y, Nedbal L. 2022. Insights on the regulation of photosynthesis in pea leaves exposed to oscillating light. Journal of Experimental Botany 73: 6380-6393.

Li M, Mukhopadhyay R, Svoboda V, Oung HMO, Mullendore DL, Kirchhoff H. 2020. Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy. Plant Direct 4: e00280.

Li TY, Shi Q, Sun H, Yue M, Zhang SB, Huang W. 2021. Diurnal response of photosystem I to fluctuating light is affected by stomatal conductance. Cell 10: 3128.

Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK. 2000. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395.

Li X-P, Gilmore AM, Niyogi KK. 2002. Molecular and global time-resolved analysis of a psbS gene dosage effect on pH- and xanthophyll cycle-dependent nonphotochemical quenching in photosystem II. Journal of Biological Chemistry 277: 33590-33597.

Long SP, Taylor SH, Burgess SJ, Carmo-Silva E, Lawson T, De Souza AP, Leonelli L, Wang Y. 2022. Into the shadows and back into sunlight: photosynthesis in fluctuating light. Annual Review of Plant Biology 73: 617-648.

Malone LA, Proctor MS, Hitchcock A, Hunter CN, Johnson MP. 2021. Cytochrome b6f - orchestrator of photosynthetic electron transfer. Biochimica et Biophysica Acta - Bioenergetics 1862: 148380.

Matthews JSA, Vialet-Chabrand S, Lawson T. 2018. Acclimation to fluctuating light impacts the rapidity of response and diurnal rhythm of stomatal conductance. Plant Physiology 176: 1939-1951.

Mitchell-Olds T. 2001. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends in Ecology & Evolution 16: 693-700.

Muller P, Li XP, Niyogi KK. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology 125: 1558-1566.

Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T. 2002. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371.

Murchie EH, Ruban AV. 2020. Dynamic non-photochemical quenching in plants: from molecular mechanism to productivity. The Plant Journal 101: 885-896.

Nakano H, Yamamoto H, Shikanai T. 2019. Contribution of NDH-dependent cyclic electron transport around photosystem I to the generation of proton motive force in the weak mutant allele of pgr5. Biochimica et Biophysica Acta - Bioenergetics 1860: 369-374.

Nedbal L, Březina V. 2002. Complex metabolic oscillations in plants forced by harmonic irradiance. Biophysical Journal 83: 2180-2189.

Nedbal L, Březina V, Červený J, Trtílek M. 2005. Photosynthesis in dynamic light: systems biology of unconventional chlorophyll fluorescence transients in Synechocystis sp. PCC 6803. Photosynthesis Research 84: 99-106.

Nedbal L, Lazár D. 2021. Photosynthesis dynamics and regulation sensed in the frequency domain. Plant Physiology 187: 646-661.

Nilkens M, Kress E, Lambrev P, Miloslavina Y, Muller M, Holzwarth AR, Jahns P. 2010. Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochimica et Biophysica Acta - Bioenergetics 1797: 466-475.

Niyogi KK, Grossman AR, Björkman O. 1998. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134.

Ogata K. 2010. Modern control engineering. Boston, MA, USA: Prentice-Hall.

Pantazopoulou CK, Bongers FJ, Pierik R. 2021. Reducing shade avoidance can improve Arabidopsis canopy performance against competitors. Plant, Cell & Environment 44: 1130-1141.

Peltier G, Aro EM, Shikanai T. 2016. NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annual Review of Plant Biology 67: 55-80.

Peressotti A, Marchiol L, Zerbi G. 2001. Photosynthetic photon flux density and sunfleck regime within canopies of wheat, sunflower and maize in different wind conditions. Italian Journal of Agronomy 4: 87-92.

Pintelon R, Schoukens J. 2012. System identification: a frequency domain approach. Hoboken, NJ, USA: John Wiley & Sons.

Pospíšil P. 2009. Production of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta - Bioenergetics 1787: 1151-1160.

Roach T, Krieger-Liszkay A. 2012. The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana. Biochimica et Biophysica Acta - Bioenergetics 1817: 2158-2165.

Ruban AV. 2016. Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiology 170: 1903-1916.

Ruban AV, Johnson MP. 2015. Visualizing the dynamic structure of the plant photosynthetic membrane. Nature Plants 1: 15161.

Schreiber U, Klughammer C. 2016. Analysis of photosystem I donor and acceptor sides with a new type of online-deconvoluting kinetic LED-array spectrophotometer. Plant and Cell Physiology 57: 1454-1467.

Schwartz L. 2008. Mathematics for the physical sciences. Mineola, NY, USA: Courier Dover.

Sétif P, Boussac A, Krieger-Liszkay A. 2019. Near-infrared in vitro measurements of photosystem I cofactors and electron-transfer partners with a recently developed spectrophotometer. Photosynthesis Research 142: 307-319.

Shikanai T. 2014. Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Current Opinion in Biotechnology 26: 25-30.

Shimakawa G, Miyake C. 2018. Changing frequency of fluctuating light reveals the molecular mechanism for P700 oxidation in plant leaves. Plant Direct 2: e00073.

Smith WK, Berry ZC. 2013. Sunflecks? Tree Physiology 33: 233-237.

Strand DD, Fisher N, Kramer DM. 2017. The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow. Journal of Biological Chemistry 292: 11850-11860.

Sugimoto K, Okegawa Y, Tohri A, Long TA, Covert SF, Hisabori T, Shikanai T. 2013. A single amino acid alteration in PGR5 confers resistance to antimycin A in cyclic electron transport around PSI. Plant and Cell Physiology 54: 1525-1534.

Suorsa M, Grieco M, Jarvi S, Gollan PJ, Kangasjarvi S, Tikkanen M, Aro EM. 2013. PGR5 ensures photosynthetic control to safeguard photosystem I under fluctuating light conditions. Plant Signaling & Behavior 8: e22741.

Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S et al. 2012. PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24: 2934-2948.

Suorsa M, Rossi F, Tadini L, Labs M, Colombo M, Jahns P, Kater Martin M, Leister D, Finazzi G, Aro E-M et al. 2016. PGR5-PGRL1-dependent cyclic electron transport modulates linear electron transport rate in Arabidopsis thaliana. Molecular Plant 9: 271-288.

Thormählen I, Zupok A, Rescher J, Leger J, Weissenberger S, Groysman J, Orwat A, Chatel-Innocenti G, Issakidis-Bourguet E, Armbruster U et al. 2017. Thioredoxins play a crucial role in dynamic acclimation of photosynthesis in fluctuating light. Molecular Plant 10: 168-182.

Ünnep R, Zsiros O, Hörcsik Z, Markó M, Jajoo A, Kohlbrecher J, Garab G, Nagy G. 2017. Low-pH induced reversible reorganizations of chloroplast thylakoid membranes - as revealed by small-angle neutron scattering. Biochimica et Biophysica Acta - Bioenergetics 1858: 360-365.

Wada S, Amako K, Miyake C. 2021. Identification of a novel mutation exacerbated the PSI photoinhibition in pgr5/pgrl1 mutants; caution for overestimation of the phenotypes in Arabidopsis pgr5-1 mutant. Cells 10: 2884.

Wang CJ, Yamamoto H, Shikanai T. 2015. Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochimica et Biophysica Acta - Bioenergetics 1847: 931-938.

Ware MA, Belgio E, Ruban AV. 2015. Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. Journal of Experimental Botany 66: 1259-1270.

Way DA, Pearcy RW. 2012. Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiology 32: 1066-1081.

Wehner A, Grasses T, Jahns P. 2006. De-epoxidation of violaxanthin in the minor antenna proteins of photosystem II, lhcb4, lhcb5, and lhcb6. Journal of Biological Chemistry 281: 21924-21933.

Wood WHJ, MacGregor-Chatwin C, Barnett SFH, Mayneord GE, Huang X, Hobbs JK, Hunter CN, Johnson MP. 2018. Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer. Nature Plants 4: 116-127.

Yamamoto H, Peng L, Fukao Y, Shikanai T. 2011. An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23: 1480-1493.

Yamamoto H, Shikanai T. 2019. PGR5-dependent cyclic electron flow protects photosystem I under fluctuating light at donor and acceptor sides. Plant Physiology 179: 588-600.

Yamori W, Makino A, Shikanai T. 2016. A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Scientific Reports 6: 20147.

From leaf to multiscale models of photosynthesis: applications and challenges for crop improvement