Photosystem II

Last updated
Cyanobacteria photosystem II, Dimer, PDB 2AXT PhotosystemII.PNG
Cyanobacteria photosystem II, Dimer, PDB 2AXT

Photosystem II (or water-plastoquinone oxidoreductase) is the first protein complex in the light-dependent reactions of oxygenic photosynthesis. It is located in the thylakoid membrane of plants, algae, and cyanobacteria. Within the photosystem, enzymes capture photons of light to energize electrons that are then transferred through a variety of coenzymes and cofactors to reduce plastoquinone to plastoquinol. The energized electrons are replaced by oxidizing water to form hydrogen ions and molecular oxygen.

Contents

By replenishing lost electrons with electrons from the splitting of water, photosystem II provides the electrons for all of photosynthesis to occur. The hydrogen ions (protons) generated by the oxidation of water help to create a proton gradient that is used by ATP synthase to generate ATP. The energized electrons transferred to plastoquinone are ultimately used to reduce NADP+
 to NADPH or are used in non-cyclic electron flow. [1] DCMU is a chemical often used in laboratory settings to inhibit photosynthesis. When present, DCMU inhibits electron flow from photosystem II to plastoquinone.

Structure of complex

Cyanobacterial photosystem II, Monomer, PDB 2AXT. Photosystem-II 2AXT.PNG
Cyanobacterial photosystem II, Monomer, PDB 2AXT.
Schematic of PSII, highlighting electron transfer. Photosystem II - multilingual.svg
Schematic of PSII, highlighting electron transfer.

The core of PSII consists of a pseudo-symmetric heterodimer of two homologous proteins D1 and D2. [2] Unlike the reaction centers of all other photosystems in which the positive charge sitting on the chlorophyll dimer that undergoes the initial photoinduced charge separation is equally shared by the two monomers, in intact PSII the charge is mostly localized on one chlorophyll center (70−80%). [3] Because of this, P680+ is highly oxidizing and can take part in the splitting of water. [2]

Photosystem II (of cyanobacteria and green plants) is composed of around 20 subunits (depending on the organism) as well as other accessory, light-harvesting proteins. Each photosystem II contains at least 99 cofactors: 35 chlorophyll a, 12 beta-carotene, two pheophytin, two plastoquinone, two heme, one bicarbonate, 20 lipids, the Mn
4CaO
5 cluster (including two chloride ions), one non heme Fe2+
 and two putative Ca2+
 ions per monomer. [4] There are several crystal structures of photosystem II. [5] The PDB accession codes for this protein are 3WU2, 3BZ1, 3BZ2 (3BZ1 and 3BZ2 are monomeric structures of the Photosystem II dimer), [4] 2AXT, 1S5L, 1W5C, 1ILX, 1FE1, 1IZL.

Protein Subunits (only with known function)
SubunitFamilyFunction
D1 (PsbA) Photosynthetic reaction centre protein family Reaction center protein, binds Chlorophyll P680, pheophytin, beta-carotene, quinone and manganese center
D2 (PsbD)Reaction center protein
CP43 (PsbC) Photosystem II light-harvesting protein Binds manganese center
CP47 (PsbB)
O Manganese-stabilising protein (InterPro :  IPR002628 )Manganese Stabilizing Protein
By convention, gene names are formed by Psb + subunit letter. For example, subunit O is PsbO. The exceptions are D1 (PsbA) and D2 (PsbD).
Coenzymes/Cofactors
CofactorFunction
Chlorophyll Absorbs light energy and converts it to chemical energy
Beta-carotene Quench excess photoexcitation energy
Heme B559Bound to Cytochrome b559 (PsbE–PsbF) as a secondary/protective electron carrier
Pheophytin Primary electron acceptor
Plastoquinone Mobile intra-thylakoid membrane electron carrier
Manganese center Also known as the oxygen evolving center, or OEC
Photosystem II
Identifiers
EC no. 1.10.3.9
Databases
IntEnz IntEnz view
BRENDA BRENDA entry
ExPASy NiceZyme view
KEGG KEGG entry
MetaCyc metabolic pathway
PRIAM profile
PDB structures RCSB PDB PDBe PDBsum
Search
PMC articles
PubMed articles
NCBI proteins

Oxygen-evolving complex (OEC)

Proposed structure of Manganese Center Manganese cluster in the oxygen-evolving complex.svg
Proposed structure of Manganese Center

The oxygen-evolving complex is the site of water oxidation. It is a metallo-oxo cluster comprising four manganese ions (in oxidation states ranging from +3 to +4) [6] and one divalent calcium ion. When it oxidizes water, producing oxygen gas and protons, it sequentially delivers the four electrons from water to a tyrosine (D1-Y161) sidechain and then to P680 itself. It is composed of three protein subunits, OEE1 (PsbO), OEE2 (PsbP) and OEE3 (PsbQ); a fourth PsbR peptide is associated nearby.

The first structural model of the oxygen-evolving complex was solved using X-ray crystallography from frozen protein crystals with a resolution of 3.8Å in 2001. [7] Over the next years the resolution of the model was gradually increased to 2.9Å. [8] [9] [10] While obtaining these structures was in itself a great feat, they did not show the oxygen-evolving complex in full detail. In 2011 the OEC of PSII was resolved to a level of 1.9Å revealing five oxygen atoms serving as oxo bridges linking the five metal atoms and four water molecules bound to the Mn
4CaO
5 cluster; more than 1,300 water molecules were found in each photosystem II monomer, some forming extensive hydrogen-bonding networks that may serve as channels for protons, water or oxygen molecules. [11] At this stage, it is suggested that the structures obtained by X-ray crystallography are biased, since there is evidence that the manganese atoms are reduced by the high-intensity X-rays used, altering the observed OEC structure. This incentivized researchers to take their crystals to a different X-ray facilities, called X-ray Free Electron Lasers, such as SLAC in the USA. In 2014 the structure observed in 2011 was confirmed. [12] Knowing the structure of Photosystem II did not suffice to reveal how it works exactly. So now the race has started to solve the structure of Photosystem II at different stages in the mechanistic cycle (discussed below). Currently structures of the S1 state and the S3 state's have been published almost simultaneously from two different groups, showing the addition of an oxygen molecule designated O6 between Mn1 and Mn4, [13] [14] suggesting that this may be the site on the oxygen evolving complex, where oxygen is produced.

Water splitting

Water-splitting process: Electron transport and regulation. The first level (A) shows the original Kok model of the S-states cycling, the second level (B) shows the link between the electron transport (S-states advancement) and the relaxation process of the intermediate S-states ([YzSn], n=0,1,2,3) formation Water splitting process.jpg
Water-splitting process: Electron transport and regulation. The first level (A) shows the original Kok model of the S-states cycling, the second level (B) shows the link between the electron transport (S-states advancement) and the relaxation process of the intermediate S-states ([YzSn], n=0,1,2,3) formation

Photosynthetic water splitting (or oxygen evolution) is one of the most important reactions on the planet, since it is the source of nearly all the atmosphere's oxygen. Moreover, artificial photosynthetic water-splitting may contribute to the effective use of sunlight as an alternative energy-source.

The mechanism of water oxidation is understood in substantial detail. [15] [16] [17] The oxidation of water to molecular oxygen requires extraction of four electrons and four protons from two molecules of water. The experimental evidence that oxygen is released through cyclic reaction of oxygen evolving complex (OEC) within one PSII was provided by Pierre Joliot et al. [18] They have shown that, if dark-adapted photosynthetic material (higher plants, algae, and cyanobacteria) is exposed to a series of single turnover flashes, oxygen evolution is detected with typical period-four damped oscillation with maxima on the third and the seventh flash and with minima on the first and the fifth flash (for review, see [19] ). Based on this experiment, Bessel Kok and co-workers [20] introduced a cycle of five flash-induced transitions of the so-called S-states, describing the four redox states of OEC: When four oxidizing equivalents have been stored (at the S4-state), OEC returns to its basic S0-state. In the absence of light, the OEC will "relax" to the S1 state; the S1 state is often described as being "dark-stable". The S1 state is largely considered to consist of manganese ions with oxidation states of Mn3+, Mn3+, Mn4+, Mn4+. [21] Finally, the intermediate S-states [22] were proposed by Jablonsky and Lazar as a regulatory mechanism and link between S-states and tyrosine Z.

In 2012, Renger expressed the idea of internal changes of water molecules into typical oxides in different S-states during water splitting. [23]

Inhibitors

Inhibitors of PSII are used as herbicides. There are two main chemical families, the triazines derived from cyanuric chloride [24] of which atrazine and simazine are the most commonly used and the aryl ureas which include chlortoluron and diuron (DCMU). [25] [26]

See also

Related Research Articles

<span class="mw-page-title-main">Photosynthesis</span> Biological process to convert light into chemical energy

Photosynthesis is a system of biological processes by which photosynthetic organisms, such as most plants, algae, and cyanobacteria, convert light energy, typically from sunlight, into the chemical energy necessary to fuel their metabolism. Photosynthesis usually refers to oxygenic photosynthesis, a process that produces oxygen. Photosynthetic organisms store the chemical energy so produced within intracellular organic compounds like sugars, glycogen, cellulose and starches. To use this stored chemical energy, an organism's cells metabolize the organic compounds through cellular respiration. Photosynthesis plays a critical role in producing and maintaining the oxygen content of the Earth's atmosphere, and it supplies most of the biological energy necessary for complex life on Earth.

<span class="mw-page-title-main">Thylakoid</span> Membrane enclosed compartments in chloroplasts and cyanobacteria

Thylakoids are membrane-bound compartments inside chloroplasts and cyanobacteria. They are the site of the light-dependent reactions of photosynthesis. Thylakoids consist of a thylakoid membrane surrounding a thylakoid lumen. Chloroplast thylakoids frequently form stacks of disks referred to as grana. Grana are connected by intergranal or stromal thylakoids, which join granum stacks together as a single functional compartment.

<span class="mw-page-title-main">Photosystem</span> Structural units of protein involved in photosynthesis

Photosystems are functional and structural units of protein complexes involved in photosynthesis. Together they carry out the primary photochemistry of photosynthesis: the absorption of light and the transfer of energy and electrons. Photosystems are found in the thylakoid membranes of plants, algae, and cyanobacteria. These membranes are located inside the chloroplasts of plants and algae, and in the cytoplasmic membrane of photosynthetic bacteria. There are two kinds of photosystems: PSI and PSII.

Chlorophyll <i>a</i> Chemical compound

Chlorophyll a is a specific form of chlorophyll used in oxygenic photosynthesis. It absorbs most energy from wavelengths of violet-blue and orange-red light, and it is a poor absorber of green and near-green portions of the spectrum. Chlorophyll does not reflect light but chlorophyll-containing tissues appear green because green light is diffusively reflected by structures like cell walls. This photosynthetic pigment is essential for photosynthesis in eukaryotes, cyanobacteria and prochlorophytes because of its role as primary electron donor in the electron transport chain. Chlorophyll a also transfers resonance energy in the antenna complex, ending in the reaction center where specific chlorophylls P680 and P700 are located.

<span class="mw-page-title-main">Oxygen-evolving complex</span>

The oxygen-evolving complex (OEC), also known as the water-splitting complex, is a water-oxidizing enzyme involved in the photo-oxidation of water during the light reactions of photosynthesis. OEC is surrounded by 4 core proteins of photosystem II at the membrane-lumen interface. The mechanism for splitting water involves absorption of three photons before the fourth provides sufficient energy for water oxidation. Based on a widely accepted theory from 1970 by Kok, the complex can exist in 5 states, denoted S0 to S4, with S0 the most reduced and S4 the most oxidized. Photons trapped by photosystem II move the system from state S0 to S1 to S2 to S3 and finally to S4. S4 reacts with water producing free oxygen:

Photodissociation, photolysis, photodecomposition, or photofragmentation is a chemical reaction in which molecules of a chemical compound are broken down by absorption of light or photons. It is defined as the interaction of one or more photons with one target molecule that dissociates into two fragments.

<span class="mw-page-title-main">Photosynthetic reaction centre</span> Molecular unit responsible for absorbing light in photosynthesis

A photosynthetic reaction center is a complex of several proteins, biological pigments, and other co-factors that together execute the primary energy conversion reactions of photosynthesis. Molecular excitations, either originating directly from sunlight or transferred as excitation energy via light-harvesting antenna systems, give rise to electron transfer reactions along the path of a series of protein-bound co-factors. These co-factors are light-absorbing molecules (also named chromophores or pigments) such as chlorophyll and pheophytin, as well as quinones. The energy of the photon is used to excite an electron of a pigment. The free energy created is then used, via a chain of nearby electron acceptors, for a transfer of hydrogen atoms (as protons and electrons) from H2O or hydrogen sulfide towards carbon dioxide, eventually producing glucose. These electron transfer steps ultimately result in the conversion of the energy of photons to chemical energy.

<span class="mw-page-title-main">Photoinhibition</span>

Photoinhibition is light-induced reduction in the photosynthetic capacity of a plant, alga, or cyanobacterium. Photosystem II (PSII) is more sensitive to light than the rest of the photosynthetic machinery, and most researchers define the term as light-induced damage to PSII. In living organisms, photoinhibited PSII centres are continuously repaired via degradation and synthesis of the D1 protein of the photosynthetic reaction center of PSII. Photoinhibition is also used in a wider sense, as dynamic photoinhibition, to describe all reactions that decrease the efficiency of photosynthesis when plants are exposed to light.

Oxygen evolution is the chemical process of generating elemental diatomic oxygen (O2) by a chemical reaction, usually from water, the most abundant oxide compound in the universe. Oxygen evolution on Earth is effected by biotic oxygenic photosynthesis, photodissociation, hydroelectrolysis, and thermal decomposition of various oxides and oxyacids. When relatively pure oxygen is required industrially, it is isolated by distilling liquefied air.

<span class="mw-page-title-main">Pheophytin</span> Chlorophyll molecules lacking a central Mg2+ ion

Pheophytin or phaeophytin is a chemical compound that serves as the first electron carrier intermediate in the electron transfer pathway of Photosystem II in plants, and the type II photosynthetic reaction center found in purple bacteria. In both PS II and RC P870, light drives electrons from the reaction center through pheophytin, which then passes the electrons to a quinone (QA) in RC P870 and RC P680. The overall mechanisms, roles, and purposes of the pheophytin molecules in the two transport chains are analogous to each other.

<span class="mw-page-title-main">Photosynthetic reaction centre protein family</span>

Photosynthetic reaction centre proteins are main protein components of photosynthetic reaction centres (RCs) of bacteria and plants. They are transmembrane proteins embedded in the chloroplast thylakoid or bacterial cell membrane.

<span class="mw-page-title-main">Cytochrome b559</span> Family of protein complexes

Cytochrome b559 is an important component of Photosystem II (PSII) is a multisubunit protein-pigment complex containing polypeptides both intrinsic and extrinsic to the photosynthetic membrane. Within the core of the complex, the chlorophyll and beta-carotene pigments are mainly bound to the antenna proteins CP43 (PsbC) and CP47 (PsbB), which pass the excitation energy on to chlorophylls in the reaction centre proteins D1 and D2 that bind all the redox-active cofactors involved in the energy conversion process. The PSII oxygen-evolving complex (OEC) provides electrons to re-reduce the PSII reaction center, and oxidizes 2 water molecules to recover its reduced initial state. It consists of OEE1 (PsbO), OEE2 (PsbP) and OEE3 (PsbQ). The remaining subunits in PSII are of low molecular weight, and are involved in PSII assembly, stabilisation, dimerization, and photoprotection.

Dioxygen plays an important role in the energy metabolism of living organisms. Free oxygen is produced in the biosphere through photolysis of water during photosynthesis in cyanobacteria, green algae, and plants. During oxidative phosphorylation in cellular respiration, oxygen is reduced to water, thus closing the biological water-oxygen redox cycle.

<span class="mw-page-title-main">Light-dependent reactions</span> Photosynthetic reactions

Light-dependent reactions are certain photochemical reactions involved in photosynthesis, the main process by which plants acquire energy. There are two light dependent reactions: the first occurs at photosystem II (PSII) and the second occurs at photosystem I (PSI).

<span class="mw-page-title-main">Anoxygenic photosynthesis</span> Process used by obligate anaerobes

Anoxygenic photosynthesis is a special form of photosynthesis used by some bacteria and archaea, which differs from the better known oxygenic photosynthesis in plants in the reductant used and the byproduct generated.

<span class="mw-page-title-main">Ycf9 protein domain</span> Plastid protein involved in photosynthesis

In molecular biology, the PsbZ (Ycf9) is a protein domain, which is low in molecular weight. It is a transmembrane protein and therefore is located in the thylakoid membrane of chloroplasts in cyanobacteria and plants. More specifically, it is located in Photosystem II (PSII) and in the light-harvesting complex II (LHCII). Ycf9 acts as a structural linker, that stabilises the PSII-LHCII supercomplexes. Moreover, the supercomplex fails to form in PsbZ-deficient mutants, providing further evidence to suggest Ycf9's role as a structural linker. This may be caused by a marked decrease in two LHCII antenna proteins, CP26 and CP29, found in PsbZ-deficient mutants, which result in structural changes, as well as functional modifications in PSII.

Plastid terminal oxidase or plastoquinol terminal oxidase (PTOX) is an enzyme that resides on the thylakoid membranes of plant and algae chloroplasts and on the membranes of cyanobacteria. The enzyme was hypothesized to exist as a photosynthetic oxidase in 1982 and was verified by sequence similarity to the mitochondrial alternative oxidase (AOX). The two oxidases evolved from a common ancestral protein in prokaryotes, and they are so functionally and structurally similar that a thylakoid-localized AOX can restore the function of a PTOX knockout.

<span class="mw-page-title-main">Bill Rutherford</span>

Alfred William Rutherford is Professor and Chair in Biochemistry of Solar energy in the Department of Life sciences at Imperial College London.

<span class="mw-page-title-main">Water oxidation catalysis</span>

Water oxidation catalysis (WOC) is the acceleration (catalysis) of the conversion of water into oxygen and protons:

<span class="mw-page-title-main">Wolfgang Lubitz</span> German chemist and biophysicist

Wolfgang Lubitz is a German chemist and biophysicist. He is currently a director emeritus at the Max Planck Institute for Chemical Energy Conversion. He is well known for his work on bacterial photosynthetic reaction centres, hydrogenase enzymes, and the oxygen-evolving complex using a variety of biophysical techniques. He has been recognized by a Festschrift for his contributions to electron paramagnetic resonance (EPR) and its applications to chemical and biological systems.

References

  1. ↑ Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (December 2005). "Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II". Nature. 438 (7070): 1040–4. Bibcode:2005Natur.438.1040L. doi:10.1038/nature04224. PMID   16355230. S2CID   4394735.
  2. 1 2 Rutherford AW, Faller P (January 2003). "Photosystem II: evolutionary perspectives". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 358 (1429): 245–53. doi:10.1098/rstb.2002.1186. PMC   1693113 . PMID   12594932.
  3. ↑ Okubo T, Tomo T, Sugiura M, Noguchi T (April 2007). "Perturbation of the structure of P680 and the charge distribution on its radical cation in isolated reaction center complexes of photosystem II as revealed by fourier transform infrared spectroscopy". Biochemistry. 46 (14): 4390–7. doi:10.1021/bi700157n. PMID   17371054.
  4. 1 2 Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (March 2009). "Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride". Nature Structural & Molecular Biology. 16 (3): 334–42. doi:10.1038/nsmb.1559. PMID   19219048. S2CID   23034289.
  5. ↑ Junko Y, Kern J, Yachandra VK, Nilsson H, Koroidov S, Messinger J (2015). "Chapter 2, Section 3 X-Ray Diffraction and Spectroscopy of Photosystem II at Room Temperature Using Femtosecond X-Ray Pulses". In Kroneck PM, Sosa Torres ME (eds.). Sustaining Life on Planet Earth: Metalloenzymes Mastering Dioxygen and Other Chewy Gases. Metal Ions in Life Sciences. Vol. 15. Springer. pp. 13–43. doi:10.1007/978-3-319-12415-5_2. ISBN   978-3-319-12414-8. PMC   4688042 . PMID   25707465.
  6. ↑ Cox, Nicholas; Pantazis, Dimitrios A.; Lubitz, Wolfgang (2020). "Current Understanding of the Mechanism of Water Oxidation in Photosystem II and Its Relation to XFEL Data". Annual Review of Biochemistry. 89: 795–820. doi: 10.1146/annurev-biochem-011520-104801 . PMID   32208765. S2CID   214645936.
  7. ↑ Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (February 2001). "Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution". Nature. 409 (6821): 739–43. doi:10.1038/35055589. PMID   11217865. S2CID   4344756.
  8. ↑ Kamiya N, Shen JR (January 2003). "Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution". Proceedings of the National Academy of Sciences of the United States of America. 100 (1): 98–103. Bibcode:2003PNAS..100...98K. doi: 10.1073/pnas.0135651100 . PMC   140893 . PMID   12518057.
  9. ↑ Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (March 2004). "Architecture of the photosynthetic oxygen-evolving center". Science. 303 (5665): 1831–8. Bibcode:2004Sci...303.1831F. doi: 10.1126/science.1093087 . PMID   14764885. S2CID   31521054.
  10. ↑ Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (March 2009). "Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride". Nature Structural & Molecular Biology. 16 (3): 334–42. doi:10.1038/nsmb.1559. PMID   19219048. S2CID   23034289.
  11. ↑ Umena Y, Kawakami K, Shen JR, Kamiya N (May 2011). "Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å" (PDF). Nature. 473 (7345): 55–60. Bibcode:2011Natur.473...55U. doi:10.1038/nature09913. PMID   21499260. S2CID   205224374.
  12. ↑ Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen JR (January 2015). "Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses". Nature. 517 (7532): 99–103. Bibcode:2015Natur.517...99S. doi:10.1038/nature13991. PMID   25470056. S2CID   205241611.
  13. ↑ Young ID, Ibrahim M, Chatterjee R, Gul S, Fuller F, Koroidov S, et al. (December 2016). "Structure of photosystem II and substrate binding at room temperature". Nature. 540 (7633): 453–457. Bibcode:2016Natur.540..453Y. doi:10.1038/nature20161. PMC   5201176 . PMID   27871088.
  14. ↑ Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y, Nakane T, et al. (March 2017). "Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL". Nature. 543 (7643): 131–135. Bibcode:2017Natur.543..131S. doi:10.1038/nature21400. PMID   28219079. S2CID   205254025.
  15. ↑ Vinyard DJ, Brudvig GW (May 2017). "Progress Toward a Molecular Mechanism of Water Oxidation in Photosystem II". Annual Review of Physical Chemistry. 68 (1): 101–116. Bibcode:2017ARPC...68..101V. doi:10.1146/annurev-physchem-052516-044820. PMID   28226223.
  16. ↑ Cox N, Pantazis DA, Lubitz W (June 2020). "Current Understanding of the Mechanism of Water Oxidation in Photosystem II and Its Relation to XFEL Data". Annual Review of Biochemistry. 89 (1): 795–820. doi: 10.1146/annurev-biochem-011520-104801 . PMID   32208765.
  17. ↑ Ibrahim M, Fransson T, Chatterjee R, Cheah MH, Hussein R, Lassalle L, et al. (June 2020). "Untangling the sequence of events during the S2 → S3 transition in photosystem II and implications for the water oxidation mechanism". Proceedings of the National Academy of Sciences of the United States of America. 117 (23): 12624–12635. Bibcode:2020PNAS..11712624I. doi: 10.1073/pnas.2000529117 . PMC   7293653 . PMID   32434915.
  18. ↑ Joliot P.; Barbieri G.; Chabaud R. (1969). "Un nouveau modele des centres photochimiques du systeme II". Photochemistry and Photobiology. 10 (5): 309–329. doi:10.1111/j.1751-1097.1969.tb05696.x. S2CID   96744015.
  19. ↑ Joliot P (2003). "Period-four oscillations of the flash-induced oxygen formation in photosynthesis". Photosynthesis Research. 76 (1–3): 65–72. doi:10.1023/A:1024946610564. PMID   16228566. S2CID   8742213.
  20. ↑ Kok B, Forbush B, McGloin M (June 1970). "Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism". Photochemistry and Photobiology. 11 (6): 457–75. doi:10.1111/j.1751-1097.1970.tb06017.x. PMID   5456273. S2CID   31914925.
  21. ↑ Kuntzleman T, Yocum CF (February 2005). "Reduction-induced inhibition and Mn(II) release from the photosystem II oxygen-evolving complex by hydroquinone or NH2OH are consistent with a Mn(III)/Mn(III)/Mn(IV)/Mn(IV) oxidation state for the dark-adapted enzyme". Biochemistry. 44 (6): 2129–42. doi:10.1021/bi048460i. PMID   15697239.
  22. ↑ Jablonsky J, Lazar D (April 2008). "Evidence for intermediate S-states as initial phase in the process of oxygen-evolving complex oxidation". Biophysical Journal. 94 (7): 2725–36. Bibcode:2008BpJ....94.2725J. doi:10.1529/biophysj.107.122861. PMC   2267143 . PMID   18178650.
  23. ↑ Renger G (August 2012). "Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms". Biochimica et Biophysica Acta (BBA) - Bioenergetics. 1817 (8): 1164–76. doi: 10.1016/j.bbabio.2012.02.005 . PMID   22353626.
  24. ↑ "Chlorotraizine herbicides". alanwood.net. Retrieved 2021-03-26.
  25. ↑ "Urea herbicides". alanwood.net. Retrieved 2021-03-26.
  26. ↑ Oettmeier W (1992). "Herbicides of photosystem II". The Photosystems. pp. 349–408. doi:10.1016/B978-0-444-89440-3.50018-7. ISBN   9780444894403.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.