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Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography.

Kawakami K, Umena Y, Kamiya N, Shen JR
Proc Natl Acad Sci U S A 106 8567-72 (2009)
Cited: 77 times
EuropePMC logo PMID: 19433803

Abstract

The chloride ion, Cl(-), is an essential cofactor for oxygen evolution of photosystem II (PSII) and is closely associated with the Mn(4)Ca cluster. Its detailed location and function have not been identified, however. We substituted Cl(-) with a bromide ion (Br(-)) or an iodide ion (I(-)) in PSII and analyzed the crystal structures of PSII with Br(-) and I(-) substitutions. Substitution of Cl(-) with Br(-) did not inhibit oxygen evolution, whereas substitution of Cl(-) with I(-) completely inhibited oxygen evolution, indicating the efficient replacement of Cl(-) by I(-). PSII with Br(-) and I(-) substitutions were crystallized, and their structures were analyzed. The results showed that there are 2 anion-binding sites in each PSII monomer; they are located on 2 sides of the Mn(4)Ca cluster at equal distances from the metal cluster. Anion-binding site 1 is close to the main chain of D1-Glu-333, and site 2 is close to the main chain of CP43-Glu-354; these 2 residues are coordinated directly with the Mn(4)Ca cluster. In addition, site 1 is located in the entrance of a proton exit channel. These results indicate that these 2 Cl(-) anions are required to maintain the coordination structure of the Mn(4)Ca cluster as well as the proposed proton channel, thereby keeping the oxygen-evolving complex fully active.

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  2. Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Kawakami K, Umena Y, Kamiya N, Shen JR. Proc Natl Acad Sci U S A 106 8567-8572 (2009)
  3. Ligation of D1-His332 and D1-Asp170 to the manganese cluster of photosystem II from Synechocystis assessed by multifrequency pulse EPR spectroscopy. Stich TA, Yeagle GJ, Service RJ, Debus RJ, Britt RD. Biochemistry 50 7390-7404 (2011)
  4. Multiple active centers of multi-subunit RNA polymerases. Yuzenkova Y, Roghanian M, Zenkin N. Transcription 3 115-118 (2012)
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Reviews citing this publication (20)

  1. The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis. Shen JR. Annu Rev Plant Biol 66 23-48 (2015)
  2. Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution. Kawakami K, Umena Y, Kamiya N, Shen JR. J Photochem Photobiol B 104 9-18 (2011)
  3. Recent progress in the crystallographic studies of photosystem II. Guskov A, Gabdulkhakov A, Broser M, Glöckner C, Hellmich J, Kern J, Frank J, Müh F, Saenger W, Zouni A. Chemphyschem 11 1160-1171 (2010)
  4. Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex. Ifuku K, Ido K, Sato F. J Photochem Photobiol B 104 158-164 (2011)
  5. Assessing the Effects of Water Deficit on Photosynthesis Using Parameters Derived from Measurements of Leaf Gas Exchange and of Chlorophyll a Fluorescence. Urban L, Aarrouf J, Bidel LPR. Front Plant Sci 8 2068 (2017)
  6. Chloride: not simply a 'cheap osmoticum', but a beneficial plant macronutrient. Wege S, Gilliham M, Henderson SW. J Exp Bot 68 3057-3069 (2017)
  7. Structural Coupling of Extrinsic Proteins with the Oxygen-Evolving Center in Photosystem II. Ifuku K, Noguchi T. Front Plant Sci 7 84 (2016)
  8. Assembly of the water-oxidizing complex in photosystem II. Becker K, Cormann KU, Nowaczyk MM. J Photochem Photobiol B 104 204-211 (2011)
  9. Structure and Function of the Photosystem Supercomplexes. Gao J, Wang H, Yuan Q, Feng Y. Front Plant Sci 9 357 (2018)
  10. Chloride as a Beneficial Macronutrient in Higher Plants: New Roles and Regulation. Colmenero-Flores JM, Franco-Navarro JD, Cubero-Font P, Peinado-Torrubia P, Rosales MA. Int J Mol Sci 20 E4686 (2019)
  11. The role of metals in production and scavenging of reactive oxygen species in photosystem II. Pospíšil P. Plant Cell Physiol 55 1224-1232 (2014)
  12. Lipids in photosystem II: multifunctional cofactors. Kern J, Guskov A. J Photochem Photobiol B 104 19-34 (2011)
  13. Application of computational chemistry to understanding the structure and mechanism of the Mn catalytic site in photosystem II--a review. Gatt P, Stranger R, Pace RJ. J Photochem Photobiol B 104 80-93 (2011)
  14. The nonheme iron in photosystem II. Müh F, Zouni A. Photosynth Res 116 295-314 (2013)
  15. The biological water-oxidizing complex at the nano-bio interface. Najafpour MM, Ghobadi MZ, Larkum AW, Shen JR, Allakhverdiev SI. Trends Plant Sci 20 559-568 (2015)
  16. Photosystem II: its function, structure, and implications for artificial photosynthesis. Barber J. Biochemistry (Mosc) 79 185-196 (2014)
  17. Binding and functions of the two chloride ions in the oxygen-evolving center of photosystem II. Imaizumi K, Ifuku K. Photosynth Res 153 135-156 (2022)
  18. Involvement of high-valent manganese-oxo intermediates in oxidation reactions: realisation in nature, nano and molecular systems. Balamurugan M, Saravanan N, Ha H, Lee YH, Nam KT. Nano Converg 5 18 (2018)
  19. Structural studies on photosystem II of cyanobacteria. Gabdulkhakov AG, Dontsova MV. Biochemistry (Mosc) 78 1524-1538 (2013)
  20. Photosystem 2 and the oxygen evolving complex: a brief overview. Yocum CF. Photosynth Res 152 97-105 (2022)

Articles citing this publication (52)

  1. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Umena Y, Kawakami K, Shen JR, Kamiya N. Nature 473 55-60 (2011)
  2. Structural-functional role of chloride in photosystem II. Rivalta I, Amin M, Luber S, Vassiliev S, Pokhrel R, Umena Y, Kawakami K, Shen JR, Kamiya N, Bruce D, Brudvig GW, Gunner MR, Batista VS. Biochemistry 50 6312-6315 (2011)
  3. Theoretical illumination of water-inserted structures of the CaMn4O5 cluster in the S2 and S3 states of oxygen-evolving complex of photosystem II: full geometry optimizations by B3LYP hybrid density functional. Isobe H, Shoji M, Yamanaka S, Umena Y, Kawakami K, Kamiya N, Shen JR, Yamaguchi K. Dalton Trans 41 13727-13740 (2012)
  4. Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II. Kale R, Hebert AE, Frankel LK, Sallans L, Bricker TM, Pospíšil P. Proc Natl Acad Sci U S A 114 2988-2993 (2017)
  5. Conformational control of cofactors in nature - the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles. Senge MO, MacGowan SA, O'Brien JM. Chem Commun (Camb) 51 17031-17063 (2015)
  6. Novel Features of Eukaryotic Photosystem II Revealed by Its Crystal Structure Analysis from a Red Alga. Ago H, Adachi H, Umena Y, Tashiro T, Kawakami K, Kamiya N, Tian L, Han G, Kuang T, Liu Z, Wang F, Zou H, Enami I, Miyano M, Shen JR. J Biol Chem 291 5676-5687 (2016)
  7. Structural basis of cyanobacterial photosystem II Inhibition by the herbicide terbutryn. Broser M, Glöckner C, Gabdulkhakov A, Guskov A, Buchta J, Kern J, Müh F, Dau H, Saenger W, Zouni A. J Biol Chem 286 15964-15972 (2011)
  8. Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. Chen YE, Liu WJ, Su YQ, Cui JM, Zhang ZW, Yuan M, Zhang HY, Yuan S. Physiol Plant 158 225-235 (2016)
  9. Evidence from FTIR difference spectroscopy of an extensive network of hydrogen bonds near the oxygen-evolving Mn(4)Ca cluster of photosystem II involving D1-Glu65, D2-Glu312, and D1-Glu329. Service RJ, Hillier W, Debus RJ. Biochemistry 49 6655-6669 (2010)
  10. Research Support, Non-U.S. Gov't Recent progress in the studies of structure and function of photosystem II. Allakhverdiev SI. J Photochem Photobiol B 104 1-8 (2011)
  11. Sequence variation at the oxygen-evolving centre of photosystem II: a new class of 'rogue' cyanobacterial D1 proteins. Murray JW. Photosynth Res 110 177-184 (2012)
  12. Crystal structure of monomeric photosystem II from Thermosynechococcus elongatus at 3.6-a resolution. Broser M, Gabdulkhakov A, Kern J, Guskov A, Müh F, Saenger W, Zouni A. J Biol Chem 285 26255-26262 (2010)
  13. Trigonal propeller-shaped [Mn(III)3M(II)Na] complexes (M = Mn, Ca): structural and functional models for the dioxygen evolving centre of PSII. Nayak S, Nayek HP, Dehnen S, Powell AK, Reedijk J. Dalton Trans 40 2699-2702 (2011)
  14. 'Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere'. Barber J. Q Rev Biophys 49 e14 (2016)
  15. Participation of glutamate-354 of the CP43 polypeptide in the ligation of manganese and the binding of substrate water in photosystem II. Service RJ, Yano J, McConnell I, Hwang HJ, Niks D, Hille R, Wydrzynski T, Burnap RL, Hillier W, Debus RJ. Biochemistry 50 63-81 (2011)
  16. Substrate-water exchange in photosystem II is arrested before dioxygen formation. Nilsson H, Rappaport F, Boussac A, Messinger J. Nat Commun 5 4305 (2014)
  17. Drought-induced changes in photosynthetic apparatus and antioxidant components of wheat (Triticum durum Desf.) varieties. Huseynova IM, Rustamova SM, Suleymanov SY, Aliyeva DR, Mammadov AC, Aliyev JA. Photosynth Res 130 215-223 (2016)
  18. Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of photosystem II as revealed by fourier transform infrared analysis. Suzuki H, Yu J, Kobayashi T, Nakanishi H, Nixon PJ, Noguchi T. Biochemistry 52 4748-4757 (2013)
  19. Diffusive and Metabolic Constraints to Photosynthesis in Quinoa during Drought and Salt Stress. Killi D, Haworth M. Plants (Basel) 6 E49 (2017)
  20. Nanoscale manganese oxide within Faujasite zeolite as an efficient and biomimetic water oxidizing catalyst. Najafpour MM, Pashaei B. Dalton Trans 41 10156-10160 (2012)
  21. The crystal structures of 4-methoxybenzoate bound CYP199A2 and CYP199A4: structural changes on substrate binding and the identification of an anion binding site. Bell SG, Yang W, Tan AB, Zhou R, Johnson EO, Zhang A, Zhou W, Rao Z, Wong LL. Dalton Trans 41 8703-8714 (2012)
  22. Mechanism, decomposition pathway and new evidence for self-healing of manganese oxides as efficient water oxidizing catalysts: new insights. Najafpour MM, Kompany-Zareh M, Zahraei A, Jafarian Sedigh D, Jaccard H, Khoshkam M, Britt RD, Casey WH. Dalton Trans 42 14603-14611 (2013)
  23. A 2-(2-hydroxyphenyl)-1H-benzimidazole-manganese oxide hybrid as a promising structural model for the tyrosine 161/histidine 190-manganese cluster in photosystem II. Najafpour MM, Amouzadeh Tabrizi M, Haghighi B, Govindjee. Dalton Trans 42 879-884 (2013)
  24. Role of chloride ion in hydroxyl radical production in photosystem II under heat stress: electron paramagnetic resonance spin-trapping study. Yadav DK, Pospíšil P. J Bioenerg Biomembr 44 365-372 (2012)
  25. Single-residue posttranslational modification sites at the N-terminus, C-terminus or in-between: To be or not to be exposed for enzyme access. Sirota FL, Maurer-Stroh S, Eisenhaber B, Eisenhaber F. Proteomics 15 2525-2546 (2015)
  26. Structural analysis of a Vibrio phospholipase reveals an unusual Ser-His-chloride catalytic triad. Wan Y, Wan Y, Liu C, Ma Q. J Biol Chem 294 11391-11401 (2019)
  27. Differences in the interactions between the subunits of photosystem II dependent on D1 protein variants in the thermophilic cyanobacterium Thermosynechococcus elongatus. Sugiura M, Iwai E, Hayashi H, Boussac A. J Biol Chem 285 30008-30018 (2010)
  28. Generalized approximate spin projection calculations of effective exchange integrals of the CaMn4O5 cluster in the S1 and S3 states of the oxygen evolving complex of photosystem II. Isobe H, Shoji M, Yamanaka S, Mino H, Umena Y, Kawakami K, Kamiya N, Shen JR, Yamaguchi K. Phys Chem Chem Phys 16 11911-11923 (2014)
  29. Synthesis, characterization, DFT studies and catalytic activities of manganese(II) complex with 1,4-bis(2,2':6,2''-terpyridin-4'-yl) benzene. Najafpour MM, Hillier W, Shamkhali AN, Amini M, Beckmann K, Jagličić Z, Jagodič M, Strauch P, Moghaddam AN, Beretta G, Bagherzadeh M. Dalton Trans 41 12282-12288 (2012)
  30. Structural and functional analysis of a novel haloalkane dehalogenase with two halide-binding sites. Chaloupkova R, Prudnikova T, Rezacova P, Prokop Z, Koudelakova T, Daniel L, Brezovsky J, Ikeda-Ohtsubo W, Sato Y, Kuty M, Nagata Y, Kuta Smatanova I, Damborsky J. Acta Crystallogr D Biol Crystallogr 70 1884-1897 (2014)
  31. Production of reactive oxygen species in decoupled, Ca(2+)-depleted PSII and their use in assigning a function to chloride on both sides of PSII. Semin BK, Davletshina LN, Timofeev KN, Ivanov II, Rubin AB, Seibert M. Photosynth Res 117 385-399 (2013)
  32. Chloride-assisted catalytic water oxidation. Chen Z, Concepcion JJ, Song N, Meyer TJ. Chem Commun (Camb) 50 8053-8056 (2014)
  33. Nanolayered manganese oxide/C(60) composite: a good water-oxidizing catalyst for artificial photosynthetic systems. Najafpour MM, Abasi M, Tomo T, Allakhverdiev SI. Dalton Trans 43 12058-12064 (2014)
  34. Census of halide-binding sites in protein structures. Skitchenko RK, Usoltsev D, Uspenskaya M, Kajava AV, Guskov A. Bioinformatics 36 3064-3071 (2020)
  35. Letter Functional analysis of the N-terminal region of an essential histidine kinase, Hik2, in the cyanobacterium Synechocystis sp. PCC 6803. Kotajima T, Shiraiwa Y, Suzuki I. FEMS Microbiol Lett 351 88-94 (2014)
  36. Similar Responses of Relatively Salt-Tolerant Plants to Na and K during Chloride Salinity: Comparison of Growth, Water Content and Ion Accumulation. Ievinsh G, Andersone-Ozola U, Jēkabsone A. Life (Basel) 12 1577 (2022)
  37. The double mutation ΔL6MW241F in PsbO, the photosystem II manganese stabilizing protein, yields insights into the evolution of its structure and function. Popelkova H, Commet A, Yocum CF. FEBS Lett 584 4009-4014 (2010)
  38. Understanding Two Different Structures in the Dark Stable State of the Oxygen-Evolving Complex of Photosystem II: Applicability of the Jahn-Teller Deformation Formula. Shoji M, Isobe H, Tanaka A, Fukushima Y, Kawakami K, Umena Y, Kamiya N, Nakajima T, Yamaguchi K. ChemPhotoChem 2 257-270 (2018)
  39. Characterization of ammonia binding to the second coordination shell of the oxygen-evolving complex of photosystem II. Mandal M, Askerka M, Banerjee G, Amin M, Brudvig GW, Batista VS, Gunner MR. Dalton Trans 46 16089-16095 (2017)
  40. Nano-sized Mn oxides on halloysite or high surface area montmorillonite as efficient catalysts for water oxidation with cerium(iv) ammonium nitrate: support from natural sources. Najafpour MM, Amini E. Dalton Trans 44 15441-15449 (2015)
  41. Sensitivity of the Photosynthetic Apparatus in Maize and Sorghum under Different Drought Levels. Stefanov M, Rashkov G, Borisova P, Apostolova E. Plants (Basel) 12 1863 (2023)
  42. An enzyme kinetics study of the pH dependence of chloride activation of oxygen evolution in photosystem II. Baranov S, Haddy A. Photosynth Res 131 317-332 (2017)
  43. Carbon for engineering of a water-oxidizing catalyst. Najafpour MM, Salimi S. Dalton Trans 44 20991-20998 (2015)
  44. Impact of Salinity on the Energy Transfer between Pigment-Protein Complexes in Photosynthetic Apparatus, Functions of the Oxygen-Evolving Complex and Photochemical Activities of Photosystem II and Photosystem I in Two Paulownia Lines. Stefanov MA, Rashkov GD, Yotsova EK, Dobrikova AG, Apostolova EL. Int J Mol Sci 24 3108 (2023)
  45. Optimizing Crystal Size of Photosystem II by Macroseeding: Toward Neutron Protein Crystallography. Hussein R, Ibrahim M, Chatterjee R, Coates L, Müh F, Yachandra VK, Yano J, Kern J, Dobbek H, Zouni A. Cryst Growth Des 18 85-94 (2018)
  46. D139N mutation of PsbP enhances the oxygen-evolving activity of photosystem II through stabilized binding of a chloride ion. Imaizumi K, Nishimura T, Nagao R, Saito K, Nakano T, Ishikita H, Noguchi T, Ifuku K. PNAS Nexus 1 pgac136 (2022)
  47. Effective binding of Tb3+ and La3+ cations on the donor side of Mn-depleted photosystem II. Lovyagina ER, Loktyushkin AV, Semin BK. J Biol Inorg Chem 26 1-11 (2021)
  48. Identification of the correct form of the mis-annotated response regulator Rre1 from the cyanobacterium Synechocystis sp. PCC 6803. Vidal R. FEMS Microbiol Lett 362 fnv030 (2015)
  49. Silicate Inhibits the Cytosolic Influx of Chloride in Protoplasts of Wheat and Affects the Chloride Transporters, TaCLC1 and TaNPF2.4/2.5. Premkumar A, Javed MT, Pawlowski K, Lindberg SM. Plants (Basel) 11 1162 (2022)
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  51. The Investigation of the Impact of Toxicity of Metals on Oxygen-Evolving Complex in Spinacia oleracea. Azmat R, Saleem A, Ahmed W, Qayyum A, El-Serehy HA, Ali S, Ali S. Antioxidants (Basel) 11 1802 (2022)
  52. Transcriptomic profiling of near-isogenic lines reveals candidate genes for a significant locus conferring metribuzin resistance in wheat. Bhattarai R, Liu H, Siddique KHM, Yan G. BMC Plant Biol 23 237 (2023)


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