Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP24185
REVIEW (Open Access)
Contents Vol 51(11)

Cyclic electron flow and Photosystem II-less photosynthesis

Maria Ermakova https://orcid.org/0000-0001-8466-4186 A B * , Duncan Fitzpatrick B and Anthony W. D. Larkum C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Monash University, Melbourne, Vic 3800, Australia.

B Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Australian National University, Acton, ACT 2600, Australia.

C Climate Change Cluster, University of Technology Sydney, Ultimo, NSW 2007, Australia.

* Correspondence to: maria.ermakova@monash.edu

Handling Editor: Rana Munns

Functional Plant Biology 51, FP24185 https://doi.org/10.1071/FP24185
Submitted: 15 July 2024  Accepted: 12 October 2024  Published: 29 October 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC)

Abstract

Oxygenic photosynthesis is characterised by the cooperation of two photo-driven complexes, Photosystem II (PSII) and Photosystem I (PSI), sequentially linked through a series of redox-coupled intermediates. Divergent evolution has resulted in photosystems exhibiting complementary redox potentials, spanning the range necessary to oxidise water and reduce CO2 within a single system. Catalysing nature’s most oxidising reaction to extract electrons from water is a highly specialised task that limits PSII’s metabolic function. In contrast, potential electron donors in PSI span a range of redox potentials, enabling it to accept electrons from various metabolic processes. This metabolic flexibility of PSI underpins the capacity of photosynthetic organisms to balance energy supply with metabolic demands, which is key for adaptation to environmental changes. Here, we review the phenomenon of ‘PSII-less photosynthesis’ where PSI functions independently of PSII by operating cyclic electron flow using electrons derived from non-photochemical reactions. PSII-less photosynthesis enables supercharged ATP production and is employed, for example, by cyanobacteria’s heterocysts to host nitrogen fixation and by bundle sheath cells of C4 plants to boost CO2 assimilation. We discuss the energetic benefits of this arrangement and the prospects of utilising it to improve the productivity and stress resilience of photosynthetic organisms.

Keywords: bundle sheath cell, crop improvement, cyclic electron flow, electron transport, heterocyst, nitrogen fixation, photosynthesis, Photosystem I.

References

Alcántara-Sánchez F, Leyva-Castillo LE, Chagolla-López A, González de la Vara L, Gómez-Lojero C (2017) Distribution of isoforms of ferredoxin-NADP+ reductase (FNR) in cyanobacteria in two growth conditions. The International Journal of Biochemistry & Cell Biology 85, 123-134.
| Crossref | Google Scholar | PubMed |

Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Cournac L, Aro E-M (2011) Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. Journal of Biological Chemistry 286, 24007-24014.
| Crossref | Google Scholar | PubMed |

Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro E-M (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proceedings of the National Academy of Sciences 110, 4111-4116.
| Crossref | Google Scholar |

Allahverdiyeva Y, Suorsa M, Tikkanen M, Aro E-M (2015) Photoprotection of photosystems in fluctuating light intensities. Journal of Experimental Botany 66, 2427-2436.
| Crossref | Google Scholar |

Allen RS, Gregg CM, Okada S, Menon A, Hussain D, Gillespie V, Johnston E, Devilla R, Warden AC, Taylor M, Byrne K, Colgrave M, Wood CC (2020) Plant expression of NifD protein variants resistant to mitochondrial degradation. Proceedings of the National Academy of Sciences 117, 23165-23173.
| Crossref | Google Scholar |

Almon H, Böhme H (1980) Components and activity of the photosynthetic electron transport system of intact heterocysts isolated from the blue-green alga Nostoc muscorum. Biochimica et Biophysica Acta – Bioenergetics 592, 113-120.
| Crossref | Google Scholar |

Asada K (2000) The water–water cycle as alternative photon and electron sinks. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 355, 1419-1431.
| Crossref | Google Scholar |

Asada K, Heber U, Schreiber U (1993) Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as detected in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant and Cell Physiology 34, 39-50.
| Crossref | Google Scholar |

Atkinson N, Mao Y, Chan KX, McCormick AJ (2020) Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts. Nature Communications 11, 6303.
| Crossref | Google Scholar |

Avenson TJ, Cruz JA, Kanazawa A, Kramer DM (2005) Regulating the proton budget of higher plant photosynthesis. Proceedings of the National Academy of Sciences 102, 9709-9713.
| Crossref | Google Scholar |

Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 355, 1433-1446.
| Crossref | Google Scholar |

Bag P, Shutova T, Shevela D, Lihavainen J, Nanda S, Ivanov AG, Messinger J, Jansson S (2023) Flavodiiron-mediated O2 photoreduction at photosystem I acceptor-side provides photoprotection to conifer thylakoids in early spring. Nature Communications 14, 3210.
| Crossref | Google Scholar |

Baier K, Lehmann H, Stephan DP, Lockau W (2004) NblA is essential for phycobilisome degradation in Anabaena sp. strain PCC 7120 but not for development of functional heterocysts. Microbiology 150, 2739-2749.
| Crossref | Google Scholar |

Battchikova N, Eisenhut M, Aro E-M (2011) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1807, 935-944.
| Crossref | Google Scholar |

Baysal C, Burén S, He W, Jiang X, Capell T, Rubio LM, Christou P (2022) Functional expression of the nitrogenase Fe protein in transgenic rice. Communications Biology 5, 1006.
| Crossref | Google Scholar |

Bellasio C, Ermakova M (2022) Reduction of bundle sheath size boosts cyclic electron flow in C4 Setaria viridis acclimated to low light. The Plant Journal 111, 1223-1237.
| Crossref | Google Scholar |

Bellasio C, Griffiths H (2014) The operation of two decarboxylases, transamination and partitioning of C4 metabolic processes between mesophyll and bundle sheath cells allows light capture to be balanced for the maize C4 pathway. Plant Physiology 164, 466-480.
| Crossref | Google Scholar |

Bellasio C, Lundgren MR (2024) The operation of PEPCK increases light harvesting plasticity in C4 NAD–ME and NADP–ME photosynthetic subtypes: a theoretical study. Plant, Cell & Environment 47, 2288-2309.
| Crossref | Google Scholar |

Blankenship RE (2021) ‘Molecular mechanisms of photosynthesis.’ (Wiley)

Böhme H, Schrautemier B (1987) Electron donation to nitrogenase in a cell-free system from heterocysts of Anabaena variabilis. Biochimica et Biophysica Acta (BBA) – Bioenergetics 891, 115-120.
| Crossref | Google Scholar |

Buchert F, Mosebach L, Gäbelein P, Hippler M (2020) PGR5 is required for efficient Q cycle in the cytochrome b6f complex during cyclic electron flow. Biochemical Journal 477, 1631-1650.
| Crossref | Google Scholar |

Bukhov N, Carpentier R (2004) Alternative Photosystem I-driven electron transport routes: mechanisms and functions. Photosynthesis Research 82, 17-33.
| Crossref | Google Scholar |

Bukhov N, Egorova E, Carpentier R (2002) Electron flow to photosystem I from stromal reductants in vivo: the size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units. Planta 215, 812-820.
| Crossref | Google Scholar |

Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. The EMBO Journal 17, 868-876.
| Crossref | Google Scholar |

Cabello AM, Turk-Kubo KA, Hayashi K, Jacobs L, Kudela RM, Zehr JP (2020) Unexpected presence of the nitrogen-fixing symbiotic cyanobacterium UCYN-A in Monterey Bay, California. Journal of Phycology 56, 1521-1533.
| Crossref | Google Scholar |

Cameron DD, Preiss K, Gebauer G, Read DJ (2009) The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist 183, 358-364.
| Crossref | Google Scholar |

Cardona T, Battchikova N, Zhang P, Stensjö K, Aro E-M, Lindblad P, Magnuson A (2009) Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1787, 252-263.
| Crossref | Google Scholar |

Cardona T, Sánchez-Baracaldo P, Rutherford AW, Larkum AW (2019) Early Archean origin of Photosystem II. Geobiology 17, 127-150.
| Crossref | Google Scholar |

Carrillo N, Ceccarelli EA (2003) Open questions in ferredoxin-NADP+ reductase catalytic mechanism. European Journal of Biochemistry 270, 1900-1915.
| Crossref | Google Scholar |

Casano LM, Martı́n M, Sabater B (2001) Hydrogen peroxide mediates the induction of chloroplastic Ndh complex under photooxidative stress in barley. Plant Physiology 125, 1450-1458.
| Crossref | Google Scholar |

Coale TH, Loconte V, Turk-Kubo KA, Vanslembrouck B, Mak WKE, Cheung S, Ekman A, Chen J-H, Hagino K, Takano Y, Nishimura T, Adachi M, Le Gros M, Larabell C, Zehr JP (2024) Nitrogen-fixing organelle in a marine alga. Science 384, 217-222.
| Crossref | Google Scholar |

Cohen Y, Jørgensen BB, Padan E, Shilo M (1975) Sulfide-dependent anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. Nature 257, 489-492.
| Crossref | Google Scholar |

Cooley JW, Howitt CA, Vermaas WF (2000) Succinate:quinol oxidoreductases in the cyanobacterium Synechocystis sp. strain PCC 6803: presence and function in metabolism and electron transport. Journal of Bacteriology 182, 714-722.
| Crossref | Google Scholar |

Cooley JW, Vermaas WFJ (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. Strain PCC 6803: capacity comparisons and physiological function. Journal of Bacteriology 183, 4251-4258.
| Crossref | Google Scholar |

Cournac L, Latouche G, Cerovic Z, Redding K, Ravenel J, Peltier G (2002) In vivo interactions between photosynthesis, mitorespiration, and chlororespiration in Chlamydomonas reinhardtii. Plant Physiology 129, 1921-1928.
| Crossref | Google Scholar |

Croce R, Carmo-Silva E, Cho YB, Ermakova M, Harbinson J, Lawson T, McCormick AJ, Niyogi KK, Ort DR, Patel-Tupper D, Pesaresi P, Raines C, Weber APM, Zhu X-G (2024) Perspectives on improving photosynthesis to increase crop yield. The Plant Cell 36, 3944-3943.
| Crossref | Google Scholar |

Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. Journal of Experimental Botany 56, 395-406.
| Crossref | Google Scholar |

DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, 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.
| Crossref | Google Scholar |

Dann M, Leister D (2019) Evidence that cyanobacterial Sll1217 functions analogously to PGRL1 in enhancing PGR5-dependent cyclic electron flow. Nature Communications 10, 5299.
| Crossref | Google Scholar |

Davis GA, Kramer DM (2020) Optimization of ATP synthase c–rings for oxygenic photosynthesis. Frontiers in Plant Science 10, 1778.
| Crossref | Google Scholar |

Degen GE, Pastorelli F, Johnson MP (2024) Proton gradient regulation 5 is required to avoid photosynthetic oscillations during light transitions. Journal of Experimental Botany 75, 947-961.
| Crossref | Google Scholar |

Desplats C, Mus F, Cuiné S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. Journal of Biological Chemistry 284, 4148-4157.
| Crossref | Google Scholar |

Drozak A, Romanowska E (2006) Acclimation of mesophyll and bundle sheath chloroplasts of maize to different irradiances during growth. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1757, 1539-1546.
| Crossref | Google Scholar |

Ehleringer J, Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiology 73, 555-559.
| Crossref | Google Scholar |

Emerson R (1957) Dependence of yield of photosynthesis in long-wave red on wavelength and intensity of supplementary light. Science 125, 746.
| Crossref | Google Scholar |

Emerson R, Arnold W (1932) The photochemical reaction in photosynthesis. Journal of General Physiology 16, 191-205.
| Crossref | Google Scholar |

Emerson R, Lewis CM (1943) The dependence of the quantum yield of Chlorella photosynthesis on wave lenghth of light. American Journal of Botany 30, 165-178.
| Crossref | Google Scholar |

Ermakova M, Battchikova N, Allahverdiyeva Y, Aro E-M (2013) Novel heterocyst-specific flavodiiron proteins in Anabaena sp. PCC 7120. FEBS Letters 587, 82-87.
| Crossref | Google Scholar |

Ermakova M, Battchikova N, Richaud P, Leino H, Kosourov S, Isojärvi J, Peltier G, Flores E, Cournac L, Allahverdiyeva Y, Aro E-M (2014) Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120. Proceedings of the National Academy of Sciences 111, 11205–11210. 10.1073/pnas.1407327111

Ermakova M, Huokko T, Richaud P, Bersanini L, Howe CJ, Lea-Smith DJ, Peltier G, Allahverdiyeva Y (2016) Distinguishing the roles of thylakoid respiratory terminal oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiology 171, 1307-1319.
| Crossref | Google Scholar |

Ermakova M, Lopez-Calcagno PE, Raines CA, Furbank RT, von Caemmerer S (2019) Overexpression of the Rieske FeS protein of the Cytochrome b6f complex increases C4 photosynthesis in Setaria viridis. Communications Biology 2, 314.
| Crossref | Google Scholar |

Ermakova M, Danila FR, Furbank RT, von Caemmerer S (2020) On the road to C4 rice: advances and perspectives. The Plant Journal 101, 940-950.
| Crossref | Google Scholar |

Ermakova M, Arrivault S, Giuliani R, Danila F, Alonso-Cantabrana H, Vlad D, Ishihara H, Feil R, Guenther M, Borghi GL, Covshoff S, Ludwig M, Cousins AB, Langdale JA, Kelly S, Lunn JE, Stitt M, von Caemmerer S, Furbank RT (2021a) Installation of C4 photosynthetic pathway enzymes in rice using a single construct. Plant Biotechnology Journal 19, 575-588.
| Crossref | Google Scholar |

Ermakova M, Bellasio C, Fitzpatrick D, Furbank RT, Mamedov F, von Caemmerer S (2021b) Upregulation of bundle sheath electron transport capacity under limiting light in C4Setaria viridis. The Plant Journal 106, 1443-1454.
| Crossref | Google Scholar |

Ermakova M, Woodford R, Taylor Z, Furbank RT, Belide S, von Caemmerer S (2023) Faster induction of photosynthesis increases biomass and grain yield in glasshouse-grown transgenic Sorghum bicolor overexpressing Rieske FeS. Plant Biotechnology Journal 21, 1206-1216.
| Crossref | Google Scholar |

Ermakova M, Woodford R, Fitzpatrick D, Nix SJ, Zwahlen SM, Farquhar GD, von Caemmerer S, Furbank RT (2024) Chloroplast NADH dehydrogenase-like complex-mediated cyclic electron flow is the main electron transport route in C4 bundle sheath cells. New Phytologist 243, 2187-2200.
| Crossref | Google Scholar |

Ernst A, Böhme H, Böger P (1983) Phosphorylation and nitrogenase activity in isolated heterocysts from Anabaena variabilis (ATCC 29413). Biochimica et Biophysica Acta (BBA) – Bioenergetics 723, 83-90.
| Crossref | Google Scholar |

Fan D-Y, Fitzpatrick D, Oguchi R, Ma W, Kou J, Chow WS (2016) Obstacles in the quantification of the cyclic electron flux around Photosystem I in leaves of C3 plants. Photosynthesis Research 129, 239-251.
| Crossref | Google Scholar |

Fei C, Wilson AT, Mangan NM, Wingreen NS, Jonikas MC (2022) Modelling the pyrenoid-based CO2-concentrating mechanism provides insights into its operating principles and a roadmap for its engineering into crops. Nature Plants 8, 583-595.
| Crossref | Google Scholar |

Ferimazova N, Felcmanová K, Šetlíková E, Küpper H, Maldener I, Hauska G, Šedivá B, Prášil O (2013) Regulation of photosynthesis during heterocyst differentiation in Anabaena sp. strain PCC 7120 investigated in vivo at single-cell level by chlorophyll fluorescence kinetic microscopy. Photosynthesis Research 116, 79-91.
| Crossref | Google Scholar |

Fitzpatrick D, Aro E-M, Tiwari A (2022) True oxygen reduction capacity during photosynthetic electron transfer in thylakoids and intact leaves. Plant Physiology 189, 112-128.
| Crossref | Google Scholar |

Flores E, Picossi S, Valladares A, Herrero A (2019) Transcriptional regulation of development in heterocyst-forming cyanobacteria. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms 1862, 673-684.
| Crossref | Google Scholar |

Franklin LA, Osmond CB, Larkum AW (2003) Photoinhibition, UV-B and algal photosynthesis. In ‘Photosynthesis in algae’. (Eds AWD Larkum, SE Douglas, JA Raven) pp. 351–384. (Springer)

Furbank R, Jenkins C, Hatch MD (1990) C4 photosynthesis: quantum requirement, C4 and overcycling and Q-cycle involvement. Functional Plant Biology 17, 1-7.
| Crossref | Google Scholar |

Furbank RT (2011) Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types? Journal of Experimental Botany 62, 3103-3108.
| Crossref | Google Scholar |

Furutani R, Ohnishi M, Mori Y, Wada S, Miyake C (2022) The difficulty of estimating the electron transport rate at photosystem I. Journal of Plant Research 135, 565-577.
| Crossref | Google Scholar |

Gao S, Wang G (2012) The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). Journal of Experimental Botany 63, 4349-4358.
| Crossref | Google Scholar |

Gao S, Shen S, Wang G, Niu J, Lin A, Pan G (2011) PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant and Cell Physiology 52, 885-893.
| Crossref | Google Scholar |

Gerotto C, Alboresi A, Meneghesso A, Jokel M, Suorsa M, Aro E-M, Morosinotto T (2016) Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proceedings of the National Academy of Sciences 113, 12322-12327.
| Crossref | Google Scholar |

Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant, Cell & Environment 30, 1240-1255.
| Crossref | Google Scholar |

Hagino K, Onuma R, Kawachi M, Horiguchi T (2013) Discovery of an endosymbiotic nitrogen-fixing cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae). PLoS ONE 8, e81749.
| Crossref | Google Scholar |

Hamilton TL, Klatt JM, De Beer D, Macalady JL (2018) Cyanobacterial photosynthesis under sulfidic conditions: insights from the isolate Leptolyngbya sp. strain hensonii. The ISME Journal 12, 568-584.
| Crossref | Google Scholar |

Hanelt D, Nultsch W (2003) Photoinhibition in seaweeds. In ‘Environmental signal processing and adaptation’. (Eds G Heldmaier, D Werner) pp. 141–167. (Springer: Berlin, Heidelberg)

Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta (BBA) – Reviews on Bioenergetics 895, 81-106.
| Crossref | Google Scholar |

Havaux M (1996) Short-term responses of Photosystem I to heat stress. Photosynthesis Research 47, 85-97.
| Crossref | Google Scholar |

Hennacy JH, Jonikas MC (2020) Prospects for engineering biophysical CO2 concentrating mechanisms into land plants to enhance yields. Annual Review of Plant Biology 71, 461-485.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Hill R, Bendall FAY (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186, 136-137.
| Crossref | Google Scholar |

Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Frontiers in Plant Science 4, 327.
| Crossref | Google Scholar |

Howe CJ, Barbrook AC, Nisbet RER, Lockhart PJ, Larkum AWD (2008) The origin of plastids. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 2675-2685.
| Crossref | Google Scholar |

Howitt CA, Udall PK, Vermaas WF (1999) Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. strain PCC 6803 are involved in regulation rather than respiration. Journal of Bacteriology 181, 3994-4003.
| Crossref | Google Scholar |

Howitt CA, Cooley JW, Wiskich JT, Vermaas WF (2001) A strain of Synechocystis sp. PCC 6803 without photosynthetic oxygen evolution and respiratory oxygen consumption: implications for the study of cyclic photosynthetic electron transport. Planta 214, 46-56.
| Crossref | Google Scholar |

Huang L-S, Cobessi D, Tung EY, Berry EA (2005) Binding of the respiratory chain inhibitor antimycin to the mitochondrial bc1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. Journal of Molecular Biology 351, 573-597.
| Crossref | Google Scholar |

Huang W, Yang Y-J, Zhang S-B, Liu T (2018) Cyclic electron flow around Photosystem I promotes ATP synthesis possibly helping the rapid repair of photodamaged Photosystem II at low light. Frontiers in Plant Science 9, 239.
| Crossref | Google Scholar |

Huokko T, Muth-Pawlak D, Battchikova N, Allahverdiyeva Y, Aro E-M (2017) Role of type 2 NAD(P)H dehydrogenase NdbC in redox regulation of carbon allocation in Synechocystis. Plant Physiology 174, 1863-1880.
| Crossref | Google Scholar |

Huokko T, Muth-Pawlak D, Aro E-M (2019) Thylakoid localized type 2 NAD(P)H dehydrogenase NdbA optimizes light-activated heterotrophic growth of Synechocystis sp. PCC 6803. Plant and Cell Physiology 60, 1386-1399.
| Crossref | Google Scholar |

Ibrahim IM, Mckenzie SD, Chung J, Aryal UK, Leon-Salas WD, Puthiyaveetil S (2022) Photosystem stoichiometry adjustment is a photoreceptor-mediated process in Arabidopsis. Scientific Reports 12, 10982.
| Crossref | Google Scholar |

Ikuma H, Bonner WD, Jr (1967) Properties of higher plant mitochondria. III. Effects of respiratory inhibitors. Plant Physiology 42, 1535-1544.
| Crossref | Google Scholar |

Ilík P, Pavlovič A, Kouřil R, Alboresi A, Morosinotto T, Allahverdiyeva Y, Aro E-M, Yamamoto H, Shikanai T (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytologist 214, 967-972.
| Crossref | Google Scholar |

Ishikawa N, Takabayashi A, Noguchi K, Tazoe Y, Yamamoto H, von Caemmerer S, Sato F, Endo T (2016) NDH-mediated cyclic electron flow around Photosystem I is crucial for C4 photosynthesis. Plant and Cell Physiology 57, 2020-2028.
| Crossref | Google Scholar |

Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464, 1210-1213.
| Crossref | Google Scholar |

Jackson PJ, Hitchcock A, Brindley AA, Dickman MJ, Hunter CN (2023) Absolute quantification of cellular levels of photosynthesis-related proteins in Synechocystis sp. PCC 6803. Photosynthesis Research 155, 219-245.
| Crossref | Google Scholar |

Jans F, Mignolet E, Houyoux P-A, Cardol P, Ghysels B, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proceedings of the National Academy of Sciences 105, 20546-20551.
| Crossref | Google Scholar |

Joët T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around Photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiology 128, 760-769.
| Crossref | Google Scholar |

Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryote Cell 12, 776-793.
| Crossref | Google Scholar |

Jokel M, Kosourov S, Battchikova N, Tsygankov AA, Aro EM, Allahverdiyeva Y (2015) Chlamydomonas flavodiiron proteins facilitate acclimation to anoxia during sulfur deprivation. Plant and Cell Physiology 56, 1598-1607.
| Crossref | Google Scholar |

Jüttner F (1983) 14C-labeled metabolites in heterocysts and vegetative cells of Anabaena cylindrica filaments and their presumptive function as transport vehicles of organic carbon and nitrogen. Journal of Bacteriology 155, 628-633.
| Crossref | Google Scholar |

Kämäräinen J, Huokko T, Kreula S, Jones PR, Aro E-M, Kallio P (2017) Pyridine nucleotide transhydrogenase PntAB is essential for optimal growth and photosynthetic integrity under low-light mixotrophic conditions in Synechocystis sp. PCC 6803. New Phytologist 214, 194-204.
| Crossref | Google Scholar |

Kimata Y, Hase T (1989) Localization of ferredoxin isoproteins in mesophyll and bundle sheath cells in maize leaf. Plant Physiology 89, 1193-1197.
| Crossref | Google Scholar |

Kimata-Ariga Y, Matsumura T, Kada S, Fujimoto H, Fujita Y, Endo T, Mano JI, Sato F, Hase T (2000) Differential electron flow around photosystem I by two C4-photosynthetic-cell-specific ferredoxins. The EMBO Journal 19, 5041-5050.
| Crossref | Google Scholar |

Kok B, Forbush B, Mcgloin M (1970) Cooperation of charges in photosynthetic O2 evolution–I. A linear four step mechanism. Photochemistry and Photobiology 11, 457-475.
| Crossref | Google Scholar |

Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiology 155, 70-78.
| Crossref | Google Scholar |

Lajkó F, Kadioglu A, Borbély G, Garab G (1997) Competition between the photosynthetic and the (chloro)respiratory electron transport chains in cyanobacteria, green algae and higher plants. Effect of heat stress. Photosynthetica 33, 217-226.
| Crossref | Google Scholar |

Landa M, Turk-Kubo KA, Cornejo-Castillo FM, Henke BA, Zehr JP (2021) Critical role of light in the growth and activity of the marine N2-fixing UCYN-A symbiosis. Frontiers in Microbiology 12, 666739.
| Crossref | Google Scholar |

Larkum AWD (2006) The evolution of chlorophylls and photosynthesis. In ‘Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications’. (Eds B Grimm, RJ Porra, W Rüdiger, H Scheer) pp. 261–282. (Springer: Dordrecht)

Larkum AWD (2020) Light-harvesting in cyanobacteria and eukaryote algae: an overview. In ‘Photosynthesis in algae: biochemical and physiological mechanisms’. (Eds AWD Larkum, AR Grossman, JA Raven) pp. 207–260. (Springer International Publishing: Cham)

Laughlin TG, Bayne AN, Trempe J-F, Savage DF, Davies KM (2019) Structure of the complex I-like molecule NDH of oxygenic photosynthesis. Nature 566, 411-414.
| Crossref | Google Scholar |

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 (BBA) - Bioenergetics 1861, 148254.
| Crossref | Google Scholar |

Lea-Smith DJ, Bombelli P, Vasudevan R, Howe CJ (2016) Photosynthetic, respiratory and extracellular electron transport pathways in cyanobacteria. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 247-255.
| Crossref | Google Scholar |

Leister D, Marino G, Minagawa J, Dann M (2022) An ancient function of PGR5 in iron delivery? Trends in Plant Science 27, 971-980.
| Crossref | Google Scholar |

Lewis S, Wheeler C, Mitchard E, Koch A (2019) Restoring natural forests is the best way to remove atmospheric carbon. Nature 568, 25-28.
| Crossref | Google Scholar |

Liu L-N (2016) Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 256-265.
| Crossref | Google Scholar |

Liu L-N, Bryan SJ, Huang F, Yu J, Nixon PJ, Rich PR, Mullineaux CW (2012) Control of electron transport routes through redox-regulated redistribution of respiratory complexes. Proceedings of the National Academy of Sciences 109, 11431-11436.
| Crossref | Google Scholar |

Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM (2010) An Arabidopsis mutant with high cyclic electron flow around Photosystem I (hcef) Involving the NADPH dehydrogenase complex. The Plant Cell 22, 221-233.
| Crossref | Google Scholar |

Logacheva MD, Schelkunov MI, Penin AA (2011) Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biology and Evolution 3, 1296-1303.
| Crossref | Google Scholar |

Long BM, Hee WY, Sharwood RE, Rae BD, Kaines S, Lim Y-L, Nguyen ND, Massey B, Bala S, von Caemmerer S, Badger MR, Price GD (2018) Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts. Nature Communications 9, 3570.
| Crossref | Google Scholar |

Lu X, Huan L, Gao S, He L, Wang G (2016) NADPH from the oxidative pentose phosphate pathway drives the operation of cyclic electron flow around photosystem I in high-intertidal macroalgae under severe salt stress. Physiologia Plantarum 156, 397-406.
| Crossref | Google Scholar |

Magnuson A (2019) Heterocyst thylakoid bioenergetics. Life 9, 13.
| Crossref | Google Scholar |

Magnuson A, Cardona T (2016) Thylakoid membrane function in heterocysts. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 309-319.
| Crossref | Google Scholar |

Majeran W, Cai Y, Sun Q, Van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. The Plant Cell 17, 3111-3140.
| Crossref | Google Scholar |

Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, Van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Molecular & Cellular Proteomics 7, 1609-1638.
| Crossref | Google Scholar |

Malone LA, Proctor MS, Hitchcock A, Hunter CN, Johnson MP (2021) Cytochrome b6f – orchestrator of photosynthetic electron transfer. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1862, 148380.
| Crossref | Google Scholar |

Marreiros BC, Sena FV, Sousa FM, Batista AP, Pereira MM (2016) Type II NADH:quinone oxidoreductase family: phylogenetic distribution, structural diversity and evolutionary divergences. Environmental Microbiology 18, 4697-4709.
| Crossref | Google Scholar |

Martín M, Sabater B (2010) Plastid ndh genes in plant evolution. Plant Physiology and Biochemistry 48, 636-645.
| Crossref | Google Scholar |

Martin WF, Bryant DA, Beatty JT (2017) A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiology Reviews 42, 205-231.
| Crossref | Google Scholar |

Marutani Y, Yamauchi Y, Kimura Y, Mizutani M, Sugimoto Y (2012) Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. Planta 236, 753-761.
| Crossref | Google Scholar |

Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: response to high temperature stress. Journal of Photochemistry and Photobiology B: Biology 137, 116-126.
| Crossref | Google Scholar |

McDowell NG, Williams AP, Xu C, Pockman WT, Dickman LT, Sevanto S, Pangle R, Limousin J, Plaut J, Mackay DS, Ogee J, Domec JC, Allen CD, Fisher RA, Jiang X, Muss JD, Breshears DD, Rauscher SA, Koven C (2016) Multi-scale predictions of massive conifer mortality due to chronic temperature rise. Nature Climate Change 6, 295-300.
| Crossref | Google Scholar |

McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiology 164, 2247-2261.
| Crossref | Google Scholar |

McKenzie SD, Ibrahim IM, Aryal UK, Puthiyaveetil S (2020) Stoichiometry of protein complexes in plant photosynthetic membranes. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1861, 148141.
| Crossref | Google Scholar |

Meierhoff K, Westhoff P (1993) Differential biogenesis of photosystem-II in mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants: the nonstoichiometric abundance of the subunits of photosystem-II in the bundle-sheath chloroplasts and the translational activity of the plastome-encoded genes. Planta 191, 23-33.
| Crossref | Google Scholar |

Menke W, Schmid GH (1976) Cyclic photophosphorylation in the mykotrophic orhid Neottia nidus-avis. Plant Physiology 57, 716-719.
| Crossref | Google Scholar |

Messant M, Hani U, Lai T-L, Wilson A, Shimakawa G, Krieger-Liszkay A (2024) Plastid terminal oxidase (PTOX) protects photosystem I and not photosystem II against photoinhibition in Arabidopsis thaliana and Marchantia polymorpha. The Plant Journal 117, 669-678.
| Crossref | Google Scholar |

Michalecka AM, Staffan Svensson Å, Johansson FI, Agius SC, Johanson U, Brennicke A, Binder S, Rasmusson AG (2003) Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiology 133, 642-652.
| Crossref | Google Scholar |

Miller NT, Vaughn MD, Burnap RL (2021) Electron flow through NDH-1 complexes is the major driver of cyclic electron flow-dependent proton pumping in cyanobacteria. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1862, 148354.
| Crossref | Google Scholar |

Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558-1566.
| Crossref | Google Scholar |

Munekage YN, Taniguchi YY (2016) Promotion of cyclic electron transport around photosystem I with the development of C4 photosynthesis. Plant and Cell Physiology 57, 897-903.
| Crossref | Google Scholar |

Munekage YN, Eymery F, Rumeau D, Cuiné S, Oguri M, Nakamura N, Yokota A, Genty B, Peltier G (2010) Elevated expression of PGR5 and NDH-H in bundle sheath chloroplasts in C4Flaveria species. Plant and Cell Physiology 51, 664-668.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1817, 1127-1133.
| Crossref | Google Scholar |

Nakamura N, Iwano M, Havaux M, Yokota A, Munekage YN (2013) Promotion of cyclic electron transport around photosystem I during the evolution of NADP–malic enzyme-type C4 photosynthesis in the genus Flaveria. New Phytologist 199, 832-842.
| Crossref | Google Scholar |

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 (BBA) – Bioenergetics 1860, 369-374.
| Crossref | Google Scholar |

Nawrocki WJ, Bailleul B, Picot D, Cardol P, Rappaport F, Wollman FA, Joliot P (2019a) The mechanism of cyclic electron flow. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1860, 433-438.
| Crossref | Google Scholar |

Nawrocki WJ, Bailleul B, Cardol P, Rappaport F, Wollman FA, Joliot P (2019b) Maximal cyclic electron flow rate is independent of PGRL1 in Chlamydomonas. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1860, 425-432.
| Crossref | Google Scholar |

Nawrocki WJ, Buchert F, Joliot P, Rappaport F, Bailleul B, Wollman F-A (2019c) Chlororespiration controls growth under intermittent light. Plant Physiology 179, 630-639.
| Crossref | Google Scholar |

Nellaepalli S, Kodru S, Tirupathi M, Subramanyam R (2012) Anaerobiosis induced state transition: a non photochemical reduction of PQ pool mediated by NDH in Arabidopsis thaliana. PLoS ONE 7, e49839.
| Crossref | Google Scholar |

Nieves-Morión M, Flores E, Foster RA (2020) Predicting substrate exchange in marine diatom-heterocystous cyanobacteria symbioses. Environmental Microbiology 22, 2027-2052.
| Crossref | Google Scholar |

Nikkanen L, Santana Sánchez A, Ermakova M, Rögner M, Cournac L, Allahverdiyeva Y (2020) Functional redundancy between flavodiiron proteins and NDH-1 in Synechocystis sp. PCC 6803. The Plant Journal 103, 1460-1476.
| Crossref | Google Scholar |

Nürnberg DJ, Mariscal V, Bornikoel J, Nieves-Morión M, Krauß N, Herrero A, Maldener I, Flores E, Mullineaux C (2015) Intercellular diffusion of a fluorescent sucrose analog via the septal junctions in a filamentous cyanobacterium. mBio 6, e02109.
| Crossref | Google Scholar |

Ogawa T, Kobayashi K, Taniguchi YY, Shikanai T, Nakamura N, Yokota A, Munekage YN (2023) Two cyclic electron flows around photosystem I differentially participate in C4 photosynthesis. Plant Physiology 191, 2288-2300.
| Crossref | Google Scholar |

Okutani S, Hanke GT, Satomi Y, Takao T, Kurisu G, Suzuki A, Hase T (2005) Three maize leaf ferredoxin:NADPH oxidoreductases vary in subchloroplast location, expression, and interaction with ferredoxin. Plant Physiology 139, 1451-1459.
| Crossref | Google Scholar |

Omairi-Nasser A, Galmozzi CV, Latifi A, Muro-Pastor MI, Ajlani G (2014) NtcA is responsible for accumulation of the small isoform of ferredoxin:NADP oxidoreductase. Microbiology 160, 789-794.
| Crossref | Google Scholar |

Orf GS, Gisriel C, Redding KE (2018) Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center. Photosynthesis Research 138, 11-37.
| Crossref | Google Scholar |

Osmond CB (1974) Carbon reduction and photosystem II deficiency in leaves of C4 plants. Australian Journal of Plant Physiology 1, 41-50.
| Google Scholar |

Ow SY, Cardona T, Taton A, Magnuson A, Lindblad P, Stensjö K, Wright PC (2008) Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. Journal of Proteome Research 7, 1615-1628.
| Crossref | Google Scholar |

Ow SY, Noirel J, Cardona T, Taton A, Lindblad P, Stensjö K, Wright PC (2009) Quantitative overview of N2 fixation in Nostoc punctiforme ATCC 29133 through cellular enrichments and iTRAQ shotgun proteomics. Journal of Proteome Research 8, 187-198.
| Crossref | Google Scholar |

Pan X, Cao D, Xie F, Xu F, Su X, Mi H, Zhang X, Li M (2020) Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nature communications 11, 610.
| Crossref | Google Scholar |

Peltier G, Cournac L (2002) Chlororespiration. Annual Review of Plant Biology 53, 523-550.
| Crossref | Google Scholar |

Peltier G, Aro E-M, Shikanai T (2016) NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annual Review of Plant Biology 67, 55-80.
| Crossref | Google Scholar |

Peltier G, Ravenel J, Verméglio A (1987) Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: evidence for a chlororespiration. Biochimica et Biophysica Acta (BBA) – Bioenergetics 893, 83-90.
| Crossref | Google Scholar |

Peng L, Fukao Y, Fujiwara M, Takami T, Shikanai T (2009) Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. The Plant Cell 21, 3623-3640.
| Crossref | Google Scholar |

Peterson RB, Schultes NP, Mchale NA, Zelitch I (2016) Evidence for a role for NAD(P)H dehydrogenase in concentration of CO2 in the bundle sheath cell of Zea mays. Plant Physiology 171, 125-138.
| Crossref | Google Scholar |

Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. Journal of Biological Chemistry 284, 32770-32781.
| Crossref | Google Scholar |

Piller LE, Besagni C, Ksas B, Rumeau D, Bréhélin C, Glauser G, Kessler F, Havaux M (2011) Chloroplast lipid droplet type II NAD(P)H quinone oxidoreductase is essential for prenylquinone metabolism and vitamin K1 accumulation. Proceedings of the National Academy of Sciences 108, 14354-14359.
| Crossref | Google Scholar |

Pogoryelov D, Reichen C, Klyszejko AL, Brunisholz R, Muller DJ, Dimroth P, Meier T (2007) The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. Journal of Bacteriology 189, 5895-5902.
| Crossref | Google Scholar |

Raghavendra AS, Padmasree K, Saradadevi K (1994) Interdependence of photosynthesis and respiration in plant cells: interactions between chloroplasts and mitochondria. Plant Science 97, 1-14.
| Crossref | Google Scholar |

Raven JA (2011) The cost of photoinhibition. Physiologia Plantarum 142, 87-104.
| Crossref | Google Scholar |

Rühle T, Dann M, Reiter B, Schünemann D, Naranjo B, Penzler J-F, Kleine T, Leister D (2021) PGRL2 triggers degradation of PGR5 in the absence of PGRL1. Nature Communications 12, 3941.
| Crossref | Google Scholar |

Sadekar S, Raymond J, Blankenship RE (2006) Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. Molecular Biology and Evolution 23, 2001-2007.
| Crossref | Google Scholar |

Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341-370.
| Crossref | Google Scholar |

Sage RF, Christin P-A, Edwards EJ (2011) The C4 plant lineages of planet Earth. Journal of Experimental Botany 62, 3155-3169.
| Crossref | Google Scholar |

Sagun JV, Badger MR, Chow WS, Ghannoum O (2019) Cyclic electron flow and light partitioning between the two photosystems in leaves of plants with different functional types. Photosynthesis Research 142, 321-334.
| Crossref | Google Scholar |

Sagun JV, Badger MR, Chow WS, Ghannoum O (2021) Mehler reaction plays a role in C3 and C4 photosynthesis under shade and low CO2. Photosynthesis Research 149(1–2), 171-185.
| Crossref | Google Scholar |

Sánchez-Baracaldo P (2015) Origin of marine planktonic cyanobacteria. Scientific Reports 5, 17418.
| Crossref | Google Scholar |

Sánchez-Baracaldo P, Cardona T (2020) On the origin of oxygenic photosynthesis and Cyanobacteria. New Phytologist 225, 1440-1446.
| Crossref | Google Scholar |

Santana-Sanchez A, Solymosi D, Mustila H, Bersanini L, Aro E-M, Allahverdiyeva Y (2019) Flavodiiron proteins 1–to-4 function in versatile combinations in O2 photoreduction in cyanobacteria. eLife 8, e45766.
| Crossref | Google Scholar |

Santana-Sánchez A, Nikkanen L, Werner E, Tóth G, Ermakova M, Kosourov S, Walter J, He M, Aro E-M, Allahverdiyeva Y (2023) Flv3A facilitates O2 photoreduction and affects H2 photoproduction independently of Flv1A in diazotrophic Anabaena filaments. New Phytologist 237, 126-139.
| Crossref | Google Scholar |

Sarewicz M, Pintscher S, Pietras R, Borek A, Bujnowicz Ł, Hanke G, Cramer WA, Finazzi G, Osyczka A (2021) Catalytic reactions and energy conservation in the Cytochrome bc1 and b6f complexes of energy-transducing membranes. Chemical Reviews 121, 2020-2108.
| Crossref | Google Scholar |

Sarkar D, Landa M, Bandyopadhyay A, Pakrasi HB, Zehr JP, Maranas CD (2021) Elucidation of trophic interactions in an unusual single-cell nitrogen-fixing symbiosis using metabolic modeling. PLoS Computational Biology 17, e1008983.
| Crossref | Google Scholar |

Saroussi SI, Wittkopp TM, Grossman AR (2016) The type II NADPH dehydrogenase facilitates cyclic electron flow, energy-dependent quenching, and chlororespiratory metabolism during acclimation of Chlamydomonas reinhardtii to nitrogen deprivation. Plant Physiology 170, 1975-1988.
| Crossref | Google Scholar |

Sato R, Kawashima R, Trinh MDL, Nakano M, Nagai T, Masuda S (2019) Significance of PGR5-dependent cyclic electron flow for optimizing the rate of ATP synthesis and consumption in Arabidopsis chloroplasts. Photosynthesis Research 139, 359-365.
| Crossref | Google Scholar |

Schopf JW (2011) The paleobiological record of photosynthesis. Photosynthesis Research 107, 87-101.
| Crossref | Google Scholar |

Schrautemeier B, Böhme H, Böger P (1984) In vitro studies on pathways and regulation of electron transport to nitrogenase with a cell-free extract from heterocysts of Anabaena variabilis. Archives of Microbiology 137, 14-20.
| Crossref | Google Scholar |

Schrautemeier B, Böhme H, Böger P (1985) Reconstitution of a light-dependent nitrogen-fixing and transhydrogenase system with heterocyst thylakoids. Biochimica et Biophysica Acta (BBA) – Bioenergetics 807, 147-154.
| Crossref | Google Scholar |

Schuller JM, Saura P, Thiemann J, Schuller SK, Gamiz-Hernandez AP, Kurisu G, Nowaczyk MM, Kaila VRI (2020) Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I. Nature Communications 11, 494.
| Crossref | Google Scholar |

Selinski J, Scheibe R (2019) Malate valves: old shuttles with new perspectives. Plant Biology 21, 21-30.
| Crossref | Google Scholar |

Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment 37, 153-161.
| Crossref | Google Scholar |

Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Current Opinion in Biotechnology 26, 25-30.
| Crossref | Google Scholar |

Shikanai T (2016) Chloroplast NDH: A different enzyme with a structure similar to that of respiratory NADH dehydrogenase. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 1015-1022.
| Crossref | Google Scholar |

Shikanai T (2024) Research on photosynthetic oscillations supports the classical concept of cyclic electron transport producing ATP. Journal of Experimental Botany 75, 667-669.
| Crossref | Google Scholar |

Simkin AJ, López-Calcagno PE, Raines CA (2019) Feeding the world: improving photosynthetic efficiency for sustainable crop production. Journal of Experimental Botany 70, 1119-1140.
| Crossref | Google Scholar |

Steinbeck J, Ross IL, Rothnagel R, Gäbelein P, Schulze S, Giles N, Ali R, Drysdale R, Sierecki E, Gambin Y, Stahlberg H, Takahashi Y, Hippler M, Hankamer B (2018) Structure of a PSI–LHCI–cyt b6f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions. Proceedings of the National Academy of Sciences 115, 10517-10522.
| Crossref | Google Scholar |

Stensjö K, Ow SY, Barrios-Llerena ME, Lindblad P, Wright PC (2007) An iTRAQ-based quantitative analysis to elaborate the proteomic response of Nostoc sp. PCC 7120 under N2 fixing conditions. Journal of Proteome Research 6, 621-635.
| Crossref | Google Scholar |

Stepien P, Johnson GN (2018) Plastid terminal oxidase requires translocation to the grana stacks to act as a sink for electron transport. Proceedings of the National Academy of Sciences 115, 9634-9639.
| Crossref | Google Scholar |

Strand DD, Walker BJ (2023) Energetic considerations for engineering novel biochemistries in photosynthetic organisms. Frontiers in Plant Science 14, 1116812.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM (2015) Activation of cyclic electron flow by hydrogen peroxide in vivo. Proceedings of the National Academy of Sciences 112, 5539-5544.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Suorsa M (2015) Cyclic electron flow provides acclimatory plasticity for the photosynthetic machinery under various environmental conditions and developmental stages. Frontiers in Plant Science 6, 800.
| Crossref | Google Scholar |

Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro E-M (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.
| Crossref | Google Scholar |

Tagawa K, Tsujimoto HY, Arnon DI (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proceedings of the National Academy of Sciences of the United States of America 49, 567-572.
| Crossref | Google Scholar |

Takabayashi A, Kishine M, Asada K, Endo T, Sato F (2005) Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. Proceedings of the National Academy of Sciences of the United States of America 102, 16898-16903.
| Crossref | Google Scholar |

Tazoe Y, Ishikawa N, Shikanai T, Ishiyama K, Takagi D, Makino A, Sato F, Endo T (2020) Overproduction of PGR5 enhances the electron sink downstream of Photosystem I in a C4 plant, Flaveria bidentis. The Plant Journal 103, 814-823.
| Crossref | Google Scholar |

Tel-Or E, Stewart WDP (1976) Photosynthetic electron transport, ATP synthesis and nitrogenase activity in isolated heterocysts of Anabaena cylindrica. Biochimica et Biophysica Acta (BBA) – Bioenergetics 423, 189-195.
| Crossref | Google Scholar |

Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Molecular & Cellular Proteomics 9, 1514-1532.
| Crossref | Google Scholar |

Theeuwen TPJM, Lawson AW, Tijink D, Fornaguera F, Becker FFM, Caracciolo L, Fisher N, Kramer DM, Wijnker E, Harbinson J, Aarts MGM (2022) The NDH complex reveals a trade-off that constrains maximising photosynthesis in Arabidopsis thaliana. bioRxiv
| Crossref | Google Scholar |

Thiel T, Hartnett Jr T, Pakrasi HB (1990) Examination of photosystem II in heterocysts of the cyanobacterium Nostoc sp. ATCC 29150. In ‘Current Research in Photosynthesis: Proceedings of the VIIIth International Conference on Photosynthesis Stockholm’, 6–11 August 1989, Sweden. (Ed. M Baltscheffsky) pp. 291–294. (Springer)

Thiel K, Patrikainen P, Nagy C, Fitzpatrick D, Pope N, Aro E-M, Kallio P (2019) Redirecting photosynthetic electron flux in the cyanobacterium Synechocystis sp. PCC 6803 by the deletion of flavodiiron protein Flv3. Microbial Cell Factories 18, 189.
| Crossref | Google Scholar |

Thomas J-C, Ughy B, Lagoutte B, Ajlani G (2006) A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation. Proceedings of the National Academy of Sciences 103, 18368-18373.
| Crossref | Google Scholar |

Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F, Affourtit JP, Zehr JP (2010) Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464, 90-94.
| Crossref | Google Scholar |

Turina P, Petersen J, Gräber P (2016) Thermodynamics of proton transport coupled ATP synthesis. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 653-664.
| Crossref | Google Scholar |

Valladares A, Muro-Pastor AM, Fillat MF, Herrero A, Flores E (1999) Constitutive and nitrogen-regulated promoters of the petH gene encoding ferredoxin:NADP+ reductase in the heterocyst-forming cyanobacterium Anabaena sp. FEBS Letters 449, 159-164.
| Crossref | Google Scholar |

Valladares A, Maldener I, Muro-Pastor AM, Flores E, Herrero A (2007) Heterocyst development and diazotrophic metabolism in terminal respiratory oxidase mutants of the cyanobacterium Anabaena sp. strain PCC 7120. Journal of Bacteriology 189, 4425-4430.
| Crossref | Google Scholar |

Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends in Plant Science 14, 200-205.
| Crossref | Google Scholar |

Vermaas WFJ (2001) Photosynthesis and respiration in cyanobacteria. Encyclopedia of Life Sciences. doi:10.1038/npg.els.0001670

von Caemmerer S, Furbank RT (2003) The C4 pathway: an efficient CO2 pump. Photosynthesis Research 77, 191-207.
| Crossref | Google Scholar |

von Caemmerer S, Furbank RT (2016) Strategies for improving C4 photosynthesis. Current Opinion in Plant Biology 31, 125-134.
| Crossref | Google Scholar |

von Caemmerer S, Quick WP, Furbank RT (2012) The development of C4 rice: current progress and future challenges. Science 336, 1671-1672.
| Crossref | Google Scholar |

Wada S, Yamamoto H, Suzuki Y, Yamori W, Shikanai T, Makino A (2018) Flavodiiron protein substitutes for cyclic electron flow without competing CO2 assimilation in rice. Plant Physiology 176, 1509-1518.
| Crossref | Google Scholar |

Walker BJ, Kramer DM, Fisher N, Fu X (2020) Flexibility in the energy balancing network of photosynthesis enables safe operation under changing environmental conditions. Plants 9, 301.
| Crossref | Google Scholar |

Walsby AE (1985) The permeability of heterocysts to the gases nitrogen and oxygen. Proceedings of the Royal Society of London. Series B. Biological Sciences 226, 345-366.
| Google Scholar |

Walter J, Kromdijk J (2022) Here comes the sun: how optimization of photosynthetic light reactions can boost crop yields. Journal of Integrative Plant Biology 64, 564-591.
| Crossref | Google Scholar |

Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye J-Y, Mi H (2006) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiology 141, 465-474.
| Crossref | Google Scholar |

Wang S, Li W, Wufuer R, Duo J, Pei L, Pan X (2023) The key role of cyclic electron flow in the recovery of photosynthesis in the photobiont during rehydration of the lichen Cladonia stellaris. Plants 12, 4011.
| Crossref | Google Scholar |

Wasserfallen A, Ragettli S, Jouanneau Y, Leisinger T (1998) A family of flavoproteins in the domains Archaea and Bacteria. European journal of Biochemistry 254, 325-332.
| Crossref | Google Scholar |

Weber APM, von Caemmerer S (2010) Plastid transport and metabolism of C3 and C4 plants—comparative analysis and possible biotechnological exploitation. Current Opinion in Plant Biology 13, 256-264.
| Crossref | Google Scholar |

Whatley FR, Allen MB, Arnon DI (1959) Photosynthesis by isolated chloroplasts: VII. Vitamin K and riboflavin phosphate as cofactors of cyclic photophosphorylation. Biochimica et Biophysica Acta 32, 32-46.
| Crossref | Google Scholar |

Woo KC, Anderson JM, Boardman NK, Downton WJS, Osmond CB, Thorne SW (1970) Deficient photosystem II in agranal bundle sheath chloroplasts of C4 plants. Proceedings of the National Academy of Sciences 67, 18-25.
| Crossref | Google Scholar |

Woodford R, Watkins J, Moore M, Nix SJ, Yee S, Chan KX, Pogson B, von Caemmerer S, Furbank RT, Ermakova M (2024) PGR5 promotes energy-dependent non-photochemical quenching to enable efficient C4 photosynthesis under fluctuating light. bioRxiv
| Crossref | Google Scholar |

Wu A, Brider J, Busch FA, Chen M, Chenu K, Clarke VC, Collins B, Ermakova M, Evans JR, Farquhar GD, Forster B, Furbank RT, Groszmann M, Hernandez-Prieto MA, Long BM, Mclean G, Potgieter A, Price GD, Sharwood RE, Stower M, van Oosterom E, von Caemmerer S, Whitney SM, Hammer GL (2023) A cross-scale analysis to understand and quantify the effects of photosynthetic enhancement on crop growth and yield across environments. Plant, Cell & Environment 46, 23-44.
| Crossref | Google Scholar |

Xu L, Law SR, Murcha MW, Whelan J, Carrie C (2013) The dual targeting ability of type II NAD(P)H dehydrogenases arose early in land plant evolution. BMC Plant Biology 13, 100.
| Crossref | Google Scholar |

Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nature Plants 2, 16012.
| Crossref | Google Scholar |

Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annual Review of Plant Biology 67, 81-106.
| Crossref | Google Scholar |

Yamori W, Shikanai T, Makino A (2015) Photosystem I cyclic electron flow via chloroplast NADH dehydrogenase-like complex performs a physiological role for photosynthesis at low light. Scientific Reports 5, 13908.
| Crossref | Google Scholar |

Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ, Vermaas WFJ, Havaux M, Matthijs HCP (2005) Open reading frame ssr2016 is required for antimycin A-sensitive Photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant and Cell Physiology 46, 1433-1436.
| Crossref | Google Scholar |

Yi X-P, Yao H-S, Fan D-Y, Zhu X-G, Losciale P, Zhang Y-L, Zhang W-F, Chow WS (2022) The energy cost of repairing photoinactivated photosystem II: an experimental determination in cotton leaf discs. New Phytologist 235, 446-456.
| Crossref | Google Scholar |

Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends in Microbiology 19, 162-173.
| Crossref | Google Scholar |

Zehr JP, Capone DG (2024) Unsolved mysteries in marine nitrogen fixation. Trends in Microbiology 32, 532-545.
| Crossref | Google Scholar |

Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110-1112.
| Crossref | Google Scholar |

Zhang C, Shuai J, Ran Z, Zhao J, Wu Z, Liao R, Wu J, Ma W, Lei M (2020) Structural insights into NDH-1 mediated cyclic electron transfer. Nature Communications 11, 888.
| Crossref | Google Scholar |

Zhang Q, Tian S, Chen G, Tang Q, Zhang Y, Fleming AJ, Zhu X-G, Wang P (2024) Regulatory NADH dehydrogenase-like complex optimizes C4 photosynthetic carbon flow and cellular redox in maize. New Phytologist 241, 82-101.
| Crossref | Google Scholar |

Zhou Q, Wang C, Yamamoto H, Shikanai T (2021) PTOX-dependent safety valve does not oxidize P700 during photosynthetic induction in the Arabidopsis pgr5 mutant. Plant Physiology 188, 1264-1276.
| Crossref | Google Scholar |

Zhou Q, Yamamoto H, Shikanai T (2022) Distinct contribution of two cyclic electron transport pathways to P700 oxidation. Plant Physiology 192, 326-341.
| Crossref | Google Scholar |

Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annual Review of Plant Biology 61, 235-261.
| Crossref | Google Scholar |

Zolotareva E, Polishchuk O (2022) Chlororespiration as a protective stress-inducible electron transport pathway in chloroplasts. The Open Agriculture Journal 16, e187433152208151.
| Crossref | Google Scholar |