Abstract
Historically, two modeling approaches have been developed independently to describe photosynthetic electron transport (PET) from water to plastoquinone within Photosystem II (PSII): Markov models account for losses from finite redox transition probabilities but predict no reaction kinetics, and ordinary differential equation (ODE) models account for kinetics but not for redox inefficiencies. We have developed an ODE mathematical framework to calculate Markov inefficiencies of transition probabilities as defined in Joliot–Kok-type catalytic cycles. We adapted a previously published ODE model for PET within PSII that accounts for 238 individual steps to enable calculation of the four photochemical inefficiency parameters (miss, double hit, inactivation, backward transition) and the four redox accumulation states (S-states) that are predicted by the most advanced of the Joliot–Kok-type models (VZAD). Using only reaction kinetic parameters without other assumptions, the RODE-calculated time-averaged (e.g., equilibrium) inefficiency parameters and equilibrium S-state populations agree with those calculated by time-independent Joliot–Kok models. RODE also predicts their time-dependent values during transient photochemical steps for all 96 microstates involving PSII redox cofactors. We illustrate applications to two cyanobacteria, Arthrospira maxima and Synechococcus sp. 7002, where experimental data exists for the inefficiency parameters and the S-state populations, and historical data for plant chloroplasts as benchmarks. Significant findings: RODE predicts the microstates responsible for period-4 and period-2 oscillations of O2 and fluorescence yields and the four inefficiency parameters; the latter parameters are not constant for each S state nor in time, in contrast to predictions from Joliot–Kok models; some of the recombination pathways that contribute to the backward transition parameter are identified and found to contribute when their rates exceed the oxidation rate of the terminal acceptor pool (PQH2); prior reports based on the assumptions of Joliot–Kok parameters may require reinterpretation.
This is a preview of subscription content, log in via an institution to check access.
Reprinted from Vinyard et al. (2013b, Fig. 1, p. 862), with permission from Elsevier
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Ananyev G, Dismukes GC (2005) How fast can Photosystem II split water? Kinetic performance at high and low frequencies. Photosynth Res. https://doi.org/10.1007/s11120-004-7081-1
Ananyev G, Gates C, Dismukes GC (2016) The Oxygen quantum yield in diverse algae and cyanobacteria is controlled by partitioning of flux between linear and cyclic electron flow within photosystem II. Biochim Biophys Acta Bioenerget 1857(9):1380–1391. https://doi.org/10.1016/j.bbabio.2016.04.056
Ananyev G, Gates C, Kaplan A, Dismukes GC (2017) Photosystem II-cyclic electron flow powers exceptional photoprotection and record growth in the microalga Chlorella ohadii. Biochim Biophys Acta Bioenerget 1858(11):873–883. https://doi.org/10.1016/j.bbabio.2017.07.001
Baake E, Schlöder JP (1992) Modelling the fast fluorescence rise of photosynthesis. Bull Math Biol. https://doi.org/10.1007/BF02460663
Belyaeva NE, Pashchenko VZ, Renger G, Riznichenko GY, Rubin AB (2006) Application of a photosystem II model for analysis of fluorescence induction curves in the 100 ns to 10 s time domain after excitation with a saturating light pulse. Biophysics. https://doi.org/10.1134/S0006350906060030
Belyaeva NE, Bulychev AA, Riznichenko GY, Rubin AB (2011) A model of photosystem II for the analysis of fast fluorescence rise in plant leaves. Biophysics. https://doi.org/10.1134/S0006350911030055
Belyaeva NE, Bulychev AA, Riznichenko GY, Rubin AB (2016) Thylakoid membrane model of the Chl a fluorescence transient and P700 induction kinetics in plant leaves. Photosynth Res. https://doi.org/10.1007/s11120-016-0289-z
Belyaeva NE, Bulychev AA, Riznichenko GY, Rubin AB (2019) Analyzing both the fast and the slow phases of chlorophyll a fluorescence and P700 absorbance changes in dark-adapted and preilluminated pea leaves using a Thylakoid Membrane model. Photosynth Res. https://doi.org/10.1007/s11120-019-00627-8
Carrieri D, Ananyev G, Brown T, Dismukes GC (2007) In vivo bicarbonate requirement for water oxidation by Photosystem II in the hypercarbonate-requiring cyanobacterium Arthrospira maxima. J Inorg Biochem 101(11–12):1865–1874. https://doi.org/10.1016/j.jinorgbio.2007.06.039
De Wijn R, Van Gorkom HJ (2002) S-state dependence of the miss probability in Photosystem II. Photosynth Res 72:217–222
Delrieu MJ, Rosengard F (1987) Fundamental differences between period-4 oscillations of the oxygen and fluorescence yield induced by flash excitation in inside-out thylakoids. Biochim Biophys Acta Bioenerget. https://doi.org/10.1016/0005-2728(87)90171-X
Falkowski PG, Fujita Y, Ley A, Mauzerall D (1986) Evidence for cyclic electron flow around Photosystem II in Chlorella pyrenoidosa. Plant Physiol 81(1):310–312. https://doi.org/10.1104/pp.81.1.310
Gorbunov MY (2015) Construction of advanced fluorescence systems for automatic measurements of phytoplankton biomass, physiology, and photosynthetic rates aboard R/V araon. Retrieved from https://repository.kopri.re.kr/bitstream/201206/8921/1/000000029847.pdf
Jablonsky J, Lazar D (2008) Evidence for intermediate S-states as initial phase in the process of oxygen-evolving complex oxidation. Biophys J. https://doi.org/10.1529/biophysj.107.122861
Jenson DL, Evans A, Barry BA (2007) Proton-coupled electron transfer and tyrosine D of photosystem II. J Phys Chem B 111(43):12599–12604. https://doi.org/10.1021/jp075726x
Joliot P, Barbieri G, Chabaud R (1969) A new model of photochemical centers in system-2. Photochem Photobiol 10(5):309
Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution—I. A linear four step mechanism. Photochem Photobiol 11(6):457–475. https://doi.org/10.1111/j.1751-1097.1970.tb06017.x
Kolber ZS, Prášil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta Bioenerget. https://doi.org/10.1016/S0005-2728(98)00135-2
Laisk A, Oja V (2018a) Kinetics of photosystem II electron transport: a mathematical analysis based on chlorophyll fluorescence induction. Photosynth Res. https://doi.org/10.1007/s11120-017-0439-y
Laisk A, Oja V (2018b) Kinetics of photosystem II electron transport: a mathematical analysis based on chlorophyll fluorescence induction. Photosynth Res 136:63–82. https://doi.org/10.1007/s11120-017-0439-y
Lavergne J, Trissl HW (1995) Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J. https://doi.org/10.1016/S0006-3495(95)80429-7
Lazár D (2003) Chlorophyll a fluorescence rise induced by high light lllumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. J Theor Biol. https://doi.org/10.1006/jtbi.2003.3140
Lebedeva GV, Belyaeva NE, Demin OV, Riznichenko GY, Rubin AB (2002) A kinetic model of primary photosynthetic processes. Description of the fast phase of chlorophyll fluorescence induction at different light intensities. Biofizika 47:1044–1058
Messinger J, Schroder WP, Renger G (1993) Structure-function relations in photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry 32.30(1993):7658–7668
Morales A, Yin X, Harbinson J, Driever SM, Molenaar J, Kramer DM, Struik PC (2018) In silico analysis of the regulation of the photosynthetic electron transport Chain in C3 plants. Plant Physiol 176(2):1247–1261. https://doi.org/10.1104/pp.17.00779
Ohad I, Dal Bosco C, Herrmann RG, Meurer J (2004) Photosystem II proteins PsbL and PsbJ regulate electron flow to the plastoquinone pool. Biochemistry 43(8):2297–2308. https://doi.org/10.1021/bi0348260
Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around Photosystem II in vivo. Photosynth Res 48(3):395–410. https://doi.org/10.1007/BF00029472
Renger G (2010) The light reactions of photosynthesis. Curr Sci 98(10):1305–1319
Riznichenko GY, Belyaeva NE, Kovalenko IB, Rubin AB (2009) Mathematical and computer modeling of primary photosynthetic processes. Biophysics. https://doi.org/10.1134/S0006350909010035
Shampine LF, Reichelt MW (1997) The MATLAB ode suite. SIAM J Sci Comput. https://doi.org/10.1137/S1064827594276424
Shinkarev VP (2003) Oxygen evolution in photosynthesis: simple analytical solution for the Kok model. Biophys J 85(1):435–441. https://doi.org/10.1016/S0006-3495(03)74488-9
Shinkarev VP (2005) Flash-induced oxygen evolution in photosynthesis: simple solution for the extended S-state model that includes misses, double-hits, inactivation, and backward-transitions. Biophys J. https://doi.org/10.1529/biophysj.104.050898
Shinkarev VP, Wraight CA (1993) Oxygen evolution in photosynthesis: from unicycle to bicycle. Proc Natl Acad Sci USA 90(5):1834–1838. https://doi.org/10.1073/pnas.90.5.1834
Takagi D, Ifuku K, Nishimura T, Miyake C (2019) Antimycin A inhibits cytochrome b 559 -mediated cyclic electron flow within photosystem II. Photosynth Res 139(1–3):487–498. https://doi.org/10.1007/s11120-018-0519-7
Vinyard DJ, Ananyev GM, Dismukes GC (2013a) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 2013(82):577–606. https://doi.org/10.1146/annurev-biochem-070511-100425
Vinyard DJ, Zachary CE, Ananyev G, Dismukes GC (2013b) Thermodynamically accurate modeling of the catalytic cycle of photosynthetic oxygen evolution: a mathematical solution to asymmetric Markov chains. Biochim Biophys Acta Bioenerget. https://doi.org/10.1016/j.bbabio.2013.04.008
Zhang X, Ma F, Zhu X, Zhu J, Rong J, Zhan J, Chen H, He C, Wang Q (2017) The acceptor side of photosystem II is the initial target of nitrite stress in Synechocystis sp. strain PCC 6803. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02952-16
Zhu XG, Govindjee, Baker NR, DeSturler E, Ort DR, Long SP (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with Photosystem II. Planta. https://doi.org/10.1007/s00425-005-0064-4
Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61(1):235–261. https://doi.org/10.1146/annurev-arplant-042809-112206
Acknowledgements
We thank Dr. Marie-Claire ten Veldhuis, TU Delft, for technical discussions. This work was funded by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy (Grant DE-SC0019460) to GCD.
Author information
Authors and Affiliations
Corresponding author
Additional information
This manuscript is dedicated to Gennady Ananyev on the occasion of his retirement from academic research and in appreciation for 28 years of scientific collaboration and friendship.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mani, K., Zournas, A. & Dismukes, G.C. Bridging the gap between Kok-type and kinetic models of photosynthetic electron transport within Photosystem II. Photosynth Res 151, 83–102 (2022). https://doi.org/10.1007/s11120-021-00868-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-021-00868-6