Abstract
The peculiarities of interaction of cyanobacterial photosystem I with redox mediators 2,6-dichlorophenolindophenol (DCPIP) and N,N,N′,N′-tetramethyl-p-phenylenediamine (TMPD) were investigated. The higher donor efficiency of the reduced DCPIP form was demonstrated. The oxidized form of DCPIP was shown to be an efficient electron acceptor for terminal iron–sulfur cluster of photosystem I. Likewise methyl viologen, after one-electron reduction, DCPIP transfers an electron to the molecular oxygen. These results were discussed in terms of influence of these interactions on photosystem I reactions with the molecular oxygen and natural electron acceptors.
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Abbreviations
- Asc:
-
Ascorbate
- β-DM:
-
n-dodecyl-β-d-maltoside
- Chl:
-
Chlorophyll
- E m :
-
The midpoint potential
- ET:
-
Electron transfer
- DCPIP:
-
2,6-dichlorophenolindophenol
- DCPIP(H)· :
-
A semi-reduced form of DCPIP
- DCPIPH2 :
-
The fully reduced form of DCPIP
- DCPIPOX :
-
The fully oxidized form of DCPIP
- K m :
-
The apparent Michaelis constant
- MV:
-
Methyl viologen
- Pc:
-
Plastocyanin
- PS I, PS II:
-
Photosystem I, photosystem II
- R MV :
-
The ratio of the rate of oxygen uptake in the presence of MV to the rate of oxygen uptake in the absence of MV
- TMPD:
-
N,N,N′,N′-tetramethyl-p-phenylenediamine
- TMPD·+ :
-
A semi-oxidized form of TMPD
- VO2 :
-
Rate of oxygen uptake in the absence of MV
- VO2 MV :
-
Rate of oxygen uptake in the presence of MV
References
Asada K, Nakano Y (1978) Affinity for oxygen in photoreduction of molecular oxygen and scavenging of hydrogen peroxide in spinach chloroplasts. Photochem Photobiol 28:917–920. https://doi.org/10.1111/j.1751-1097.1978.tb07040.x
Ball EG (1937) Studies on oxidation-reduction. 23. Ascorbic acid. J Biol Chem 118:219–239
Boucher N, Carpentier R (1993) Heat-stress stimulation of oxygen uptake by Photosystem I involves the reduction of superoxide radicals by specific electron donors. Photosynth Res 35:213–218. https://doi.org/10.1007/BF00016552
Díaz-Quintana A, Leibl W, Bottin H, Sétif P (1998) Electron transfer in Photosystem I reaction centers follows a linear pathway in which iron—sulfur cluster FB is the immediate electron donor to soluble ferredoxin. Biochemistry 37:3429–3439. https://doi.org/10.1021/BI972469L
Dvoranová D, Barbieriková Z, Dorotíková S et al (2015) Redox processes of 2,6-dichlorophenolindophenolate in different solvents. A combined electrochemical, spectroelectrochemical, photochemical, and theoretical study. J Solid State Electrochem 19:2633–2642. https://doi.org/10.1007/s10008-015-2823-x
Fujii T, Yokoyama E, Inoue K, Sakurai H (1990) The sites of electron donation of Photosystem I to methyl viologen. Biochim Biophys Acta BBA 1015:41–48. https://doi.org/10.1016/0005-2728(90)90213-N
Golbeck JH (1999) A comparative analysis of the spin state distribution of in vitro and in vivo mutants of PsaC. A biochemical argument for the sequence of electron transfer in Photosystem I as FX → FA → FB → ferredoxin/flavodoxin. Photosynth Res 61:107–144. https://doi.org/10.1023/A:1006281802710
Gopta OA, Tyunyatkina AA, Kurashov VN et al (2008) Effect of redox mediators on the flash-induced membrane potential generation in Mn-depleted photosystem II core particles. Eur Biophys J 37:1045–1050. https://doi.org/10.1007/s00249-007-0231-6
Gourovskaya KN, Mamedov MD, Vassiliev IR et al (1997) Electrogenic reduction of the primary electron donor P700 + in photosystem I by redox dyes. FEBS Lett 414:193–196. https://doi.org/10.1016/S0014-5793(97)00994-0
Hervás M, Navarro JA (2011) Effect of crowding on the electron transfer process from plastocyanin and cytochrome c6 to photosystem I: a comparative study from cyanobacteria to green algae. Photosynth Res 107:279–286. https://doi.org/10.1007/s11120-011-9637-1
Hormann H, Neubauer C, Asada K, Schreiber U (1993) Intact chloroplasts display pH 5 optimum of O2-reduction in the absence of methyl viologen: Indirect evidence for a regulatory role of superoxide protonation. Photosynth Res 37:69–80. https://doi.org/10.1007/BF02185440
Ivanov B, Asada K, Kramer DM, Edwards G (2005) Characterization of photosynthetic electron transport in bundle sheath cells of maize. I. Ascorbate effectively stimulates cyclic electron flow around PSI. Planta 220:572–581. https://doi.org/10.1007/s00425-004-1367-6
Jajoo A, Bharti S (1993) Effect of anions on photosystem 1-mediated electron transport in spinach chloroplasts. J Exp Bot 44:785–790. https://doi.org/10.1093/jxb/44.4.785
Ke B (1967) Photoreduction sites for 2,6-dichlorophenolindophenol in chloroplasts. Plant Physiol 42:1310–1312
Kozuleva MA, Ivanov BN (2010) Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids. Photosynth Res 105:51–61. https://doi.org/10.1007/s11120-010-9565-5
Kozuleva MA, Ivanov BN (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant Cell Physiol 57:1397–1404. https://doi.org/10.1093/pcp/pcw035
Kozuleva MA, Petrova AA, Mamedov MD et al (2014) O2 reduction by photosystem I involves phylloquinone under steady-state illumination. FEBS Lett 588:4364–4368. https://doi.org/10.1016/j.febslet.2014.10.003
Kozuleva MA, Vetoshkina DV, Petrova AA et al (2015) The study of oxygen reduction in photosystem I of higher plants using electron donors for this photosystem in intact thylakoids. Biochem Mosc Suppl Ser Membr Cell Biol 9:246–251. https://doi.org/10.1134/S1990747814060026
Malavath T, Caspy I, Netzer-El SY et al (2018) Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis. Biochim Biophys Acta BBA. https://doi.org/10.1016/j.bbabio.2018.02.002
Mamedov MD, Gourovskaya KN, Vassiliev IR et al (1998) Electrogenicity accompanies photoreduction of the iron-sulfur clusters FA and FB in photosystem I. FEBS Lett 431:219–223. https://doi.org/10.1016/S0014-5793(98)00759-5
Mamedov MD, Mamedova AA, Chamorovsky SK, Semenov AY (2001) Electrogenic reduction of the primary electron donor P700 by plastocyanin in photosystem I complexes. FEBS Lett 500:172–176. https://doi.org/10.1016/S0014-5793(01)02615-1
Mamedova AA, Mamedov MD, Gourovskaya KN et al (1999) Electrometrical study of electron transfer from the terminal F A/FB iron-sulfur clusters to external acceptors in photosystem I. FEBS Lett 462:421–424. https://doi.org/10.1016/S0014-5793(99)01570-7
Mano J, Hideg É, Asada K (2004) Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch Biochem Biophys 429:71–80. https://doi.org/10.1016/J.ABB.2004.05.022
Marchanka A, Gastel M van (2012) Reversed freeze quench method near the solvent phase transition. J Phys Chem A 116:3899–3906. https://doi.org/10.1021/jp300555x
Milanovsky GE, Petrova AA, Cherepanov DA, Semenov AY (2017) Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors. Photosynth Res 133:185–199. https://doi.org/10.1007/s11120-017-0366-y
Nikandrov VV, Van Chan N, Brin GP, Krasnovskií AA (1978) Methylviologen photoreduction by chloroplasts. Mol Biol (Mosk) 12:1278–1287
Parrett KG, Mehari T, Warren PG, Golbeck JH (1989) Purification and properties of the intact P-700 and F Xcontaining Photosystem I core protein. Biochimica et Biophysica Acta (BBA)-Bioenergetics 973(2):324–332
Shen G, Antonkine ML, van der Est A, Vassiliev IR, Brettel K, Bittl R, Zech SG, Zhao J, Stehlik D, Bryant DA, Golbeck JH (2002) Assembly of Photosystem I II. RUBREDOXIN IS REQUIRED FOR THE IN VIVO ASSEMBLY OF FX IN SYNECHOCOCCUS SP. PCC 7002 AS SHOWN BY OPTICAL AND EPR SPECTROSCOPY. J Biological Chem 277(23):20355–20366
Takahashi M, Asada K (1982) Dependence of oxygen affinity for Mehler reaction on photochemical activity of chloroplast thylakoids. Plant Cell Physiol 23:1457–1461. https://doi.org/10.1093/oxfordjournals.pcp.a076495
Thomas DD, Keller H, McConnell HM (1963) Exciton magnetic resonance in Wurster’s Blue Perchlorate. J Chem Phys 39:2321–2329. https://doi.org/10.1063/1.1701437
Thomas PG, Quinn PJ, Williams WP (1986) The origin of photosystem-I-mediated electron transport stimulation in heat-stressed chloroplasts. Planta 167:133–139. https://doi.org/10.1007/BF00446380
Tóth SZ, Schansker G, Garab G (2013) The physiological roles and metabolism of ascorbate in chloroplasts. Physiol Plant 148:161–175. https://doi.org/10.1111/ppl.12006
Trubitsin BV, Mamedov MD, Semenov AY, Tikhonov AN (2014) Interaction of ascorbate with photosystem I. Photosynth Res 122:215–231. https://doi.org/10.1007/s11120-014-0023-7
Vassiliev IR, Jung YS, Mamedov MD et al (1997) Near-IR absorbance changes and electrogenic reactions in the microsecond-to-second time domain in photosystem I. Biophys J 72:301–315. https://doi.org/10.1016/S0006-3495(97)78669-7
Vassiliev IR, Jung Y-S, Yang F, Golbeck JH (1998) PsaC subunit of photosystem I is oriented with iron-sulfur cluster FB as the immediate electron donor to ferredoxin and flavodoxin. Biophys J 74:2029–2035. https://doi.org/10.1016/S0006-3495(98)77909-3
Yang X, Zhang YH, Yang ZL et al (2009) pH dependence of photosynthetic behavior of plant photosystem I particles. Russ J Plant Physiol 56:599–606. https://doi.org/10.1134/S1021443709050033
Acknowledgements
This work was supported by the Russian Science Foundation (Grant #17-14-01323). In part of higher plant thylakoid membranes (Table 1), the work was supported by the Russian Science Foundation (Grant #14-14-00535). The authors are grateful to Dr. Dmitry Cherepanov for valuable discussion.
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11120_2018_514_MOESM3_ESM.tif
Supplementary Figure 2—The effect of ascorbate concentration of O2 uptake rate (VO2) in the absence (squires, solid line) or presence (triangles, dashed line) of MV (A) and the steady-state P700+ level, ΔP700+, in the presence of MV (B). On A, VO2 values in the presence of 1 mM TMPD are shown for comparison (circles). Trimeric PS I at 2 (A) or 5 (B) µg Chl mL−1, pH 7.6. Data are shown as mean of 3 repetitions ± SE (TIF 104 KB)
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Petrova, A., Mamedov, M., Ivanov, B. et al. Effect of artificial redox mediators on the photoinduced oxygen reduction by photosystem I complexes. Photosynth Res 137, 421–429 (2018). https://doi.org/10.1007/s11120-018-0514-z
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DOI: https://doi.org/10.1007/s11120-018-0514-z