Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise

Journal of Theoretical Biology

Volumn 335, Issue , 2013, Pages 249-264

  Lazár, Dušan ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Chlorophyll fluorescence induction; Model; Photosystem I; Theory; Variable fluorescence

Indexed keywords

CHLOROPHYLL A; CHLOROPHYLL B; FERREDOXIN; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; OXYGEN; PHEOPHYTIN; PLASTOCYANIN; SUPEROXIDE;

CHLOROPHYLL A; COMPUTER SIMULATION; FLUORESCENCE; NUMERICAL MODEL; THEORETICAL STUDY;

ARTICLE; CHLOROPHYLL FLUORESCENCE; COMPUTER MODEL; ELECTRON TRANSPORT; FLUORESCENCE; FLUORESCENCE RISE; ILLUMINATION; IN VIVO STUDY; LIGHT HARVESTING SYSTEM; OXIDATION REDUCTION STATE; PHOTOSYSTEM I; PHOTOSYSTEM II; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SIMULATION; STOICHIOMETRY;

CHLOROPHYLL FLUORESCENCE INDUCTION; MODEL; PHOTOSYSTEM I; THEORY; VARIABLE FLUORESCENCE;

CHLOROPHYLL; COMPUTER SIMULATION; FLUORESCENCE; MODELS, CHEMICAL; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS;

EID: 84881248603     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2013.06.028     Document Type: Article

References (105)

1. Agati G., Cerovic Z.G., Moya I. The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: the role of the photosystem I contribution to the 735nm fluorescence band. Photochem. Photobiol. 2010, 72:75-84.
2. Albertsson P.-A. A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 2001, 6:349-354.
3. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50:601-639.
4. Asada K., Kiso K., Yoshikawa K. Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J. Biol. Chem. 1974, 249:2175-2181.
5. Baake E., Schlöder J.P. Modelling the fast fluorescence rise of photosynthesis. Bull. Math. Biol. 1992, 54:999-1021.
6. Backhausen J.E., Kitzmann C., Horton P., Scheibe R. Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons. Photosynth. Res. 2000, 64:1-13.
7. Bukhov N., Carpetntier R. Alternative Photosystem I-driven electron transport routes: mechanisms and functions. Photosynth. Res. 2004, 82:17-33.
8. Butler W.L., Kitajama M. A tripartite model for chloroplast fluorescence. Proceedings of the Third International Congress on Photosynthesis 1974, 13-24. Elsevier, Amsterdam. M. Avron (Ed.).
9. Butler W.L., Kitajima M. Energy-transfer between photosystem-2 and photosystem-1 in chloroplasts. Biochim. Biophys. Acta 1975, 396:72-85.
10. Byrdin M., Rimke J., Schlodder E., Stehlik D., Roelofs T.A. Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer-limited?. Biophys. J. 2000, 79:992-1007.
11. Chow W.S., Fan D.-Y., Oguchi R., Jia H., Losciale P., Park Y.-I., He J., Öquist G., Shen Y.-G., Anderson J.M. Quantifying and monitoring functional photosystem II and the stoichiometry of the two photosystems in leaf segments: approaches and approximations. Photosynth. Res. 2012, 113:63-74.
12. Croce R., Zucchelli G., Garlaschi F.M., Bassi R., Jennings R.C. Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochem. 1996, 35:8572-8579.
13. Croce R., Dorra D., Holzwarth A.R., Jennings R.C. Fluorescence decay and spectral evolution in intact photosystem I of higher plants. Biochem. 2000, 39:6341-6348.
14. Crofts A.R., Wraight C.A. The electrochemical domain of photosynthesis. Biochim. Biophys. Acta 1983, 726:149-185.
15. b in wild type and herbicide resistant mutants of Chlamydomonas reinhardtii. Z. Naturforsch., C: Biosci. 1993, 48:259-266.
16. Dau H. Molecular mechanism and quantitative models of variable photosystem II fluorescence. Photochem. Photobiol. 1994, 60:1-23.
17. Duysens L.N.M., Sweers H.E. Mechanism of the two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists (Ed.), Studies on Microalgae and Photosynthetic Bacteria 1963, 353-372. University of Tokyo Press, Tokyo.
18. Dědic R., Svoboda A., Pšenčík J., Lupínková L., Komenda J., Hála J. Time and spectral resolved phosphorescence of singlet oxygen and pigments in photosystem II particles. J. Lumin. 2003, 102-103:313-317.
19. Ebenhöh O., Houwaart T., Lokstein H., Schlede S., Tirok K. A minimal mathematical model of nonphotochemical quenching of chlorophyll fluorescence. Biosystems 2011, 103:196-204.
20. Fan D.-Y., Hope A.B., Smith P.J., Jia H., Pace R.J., Anderson J.M., Chow W.S. The stoichiometry of the two photosystems in higher plants revisited. Biochim. Biophys. Acta, Bioenerg. 2007, 1767:1064-1072.
21. Franck F., Juneau P., Popovic R. Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim. Biophys. Acta 2002, 1556:239-246.
22. 0 in leaves is emission wavelength dependent: consequences for quenching analysis and its interpretation. Photosynth. Res. 1990, 26:133-139.
23. Gilmore A.M., Itoh S., Govindjee Global spectral-kinetic analysis of room temperature chlorophyll a fluorescence from light-harvesting antenna mutants of barley. Philos. Trans. R. Soc. London, Ser. B 2000, 355:1371-1384.
24. Govindjee Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust. J. Plant Physiol. 1995, 22:131-160.
25. + reduction in leaves: a novel in situ probe of thylakoid functioning. Plant Cell Environ. 1989, 12:357-369.
26. Heber Irrungen U. Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth. Res. 2002, 73:223-231.
27. Holzwarth A.R., Müller G.M., Niklas J., Lubitz W. Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 2: Mutations near the P700 reaction center chlorophylls provide new insight into the nature of the primary electron donor. Biophys. J. 2006, 90:552-565.
28. Ikegami I. Fluorescence changes related in the primary photochemical reaction in the P-700-enriched particles isolated from spinach chloroplasts. Biochim. Biophys. Acta 1976, 449:245-258.
29. Ilík P., Kouřil R., Fiala J., Nauš J., Vácha F. Spectral characterization of chlorophyll fluorescence in barley leaves during linear heating. Analysis of high-temperature fluorescence rise around 60°C. J. Photochem. Photobiol., B 2000, 59:103-114.
30. Ilík P., Schansker G., Kotabová E., Váczi P., Strasser R.J., Barták M. A dip in the chlorophyll fluorescence induction at 0.2-2s in Trebouxia-possessing lichens reflects a fast reoxidation of photosystem I. A comparison with higher plants. Biochim. Biophys. Acta, Bioenerg. 2006, 1757:12-20.
31. Itoh S., Sugiura K. Fluorescence of photosystem I. Advances in Photosynthesis and Respiration 2004, vol. 19:231-250. Springer, Dordrecht, Chlorophyll a Fluorescence: A Signature of Photosynthesis.
32. Jablonsky J., Lazar D. Evidence for intermediate S-states as initial phase in the process of oxygen-evolving complex oxidation. Biophys. J. 2008, 94:2725-2736.
33. Jablonsky J., Susila P., Lazar D. Impact of dimeric organization of enzyme on its function: the case of photosynthetic water splitting. Bioinormatics 2008, 24:2755-2759.
34. Johnson G.N. Physiology of PSI cyclic electron transport in higher plants. Biochim. Biophys. Acta, Bioenerg. 2011, 1807:384-389.
35. Kautsky H., Hirsch A. Neue Versuche zur Kohlensureassimilation. Naturwissenschaften 1931, 19:964.
36. Kaňa R., Lazár D., Prášil O., Nauš J. Experimental and theoretical studies on the excess capacity of Photosystem II. Photosynth. Res. 2002, 72:271-284.
37. Kaňa R., Kotabová E., Komárek O., Šedivá B., Papageorgiou G.C., Govindjee, Prášil O. The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim. Biophys. Acta, Bioenerg. 2012, 1817:1237-1247.
38. Kirchhoff H., Schöttler M.A., Maurer J., Weis E. Plastocyanin redox kinetics in spinach chloroplasts: evidence for disequilibrium in the high potential chain. Biochim. Biophys. Acta, Bioenerg. 2004, 1659:63-72.
39. Kitajama M., Butler W.L. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim. Biophys. Acta 1975, 376:105-115.
40. Klimov V.V., Klevanik A.V., Shuvalov V.A., Krasvsky A.A. Reduction of pheophytin in the primary light reaction of photosystem II. FEBS Lett. 1977, 82:183-186.
41. Klughammer C., Schreiber U. Analysis of light-induced absorbance changes in the near-infrared spectral region; I. Characterization of various components in isolated chloroplasts. Z. Naturforsch., C: Biosci. 1991, 46:233-244.
42. Kouřil R., Lazár D., Ilík P., Skotnica J., Krchňák P., Nauš J. High-temperature induced chlorophyll fluorescence rise in plants at 40-50°C: experimental and theoretical approach. Photosynth. Res. 2004, 81:49-66.
43. Krause G.H., Weis E. Chlorophyll fluorescence and photosynthesis: the basis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991, 42:313-349.
44. Krekov G.M., Krekova M.M., Lisenko A.A., Matvienko G.G. Statistical modelling of laser induced fluorescence in plant cover. J. Appl. Spectrosc. 2009, 76:386-393.
45. Kroon B.M.A., Thoms S. From electron to biomass: a mechanistic model to describe phytoplankton photosynthesis and steady-state growth rates. J. Phycol. 2006, 42:593-609.
46. Krüger T.P.J., Wientjes E., Croce R., van Grondelle R. Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:13516-13521.
47. 2. Biochim. Biophys. Acta, Bioenerg. 2011, 1807:336-347.
48. 3 photosynthesis in silico. Photosynth. Res. 2006, 90:45-66.
49. Advances in Photosynthesis and Respiration 2009, vol. 29. Springer, Dordrech.
50. Lazár D. Chlorophyll a fluorescence induction. Biochim. Biophys. Acta 1999, 1412:1-28.
51. Lazár D. Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. J. Theor. Biol. 2003, 220:469-503.
52. Lazár D. The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct. Plant Biol. 2006, 33:9-30.
53. Lazár D. Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820nm-transmittance signal of photosynthesis. Photosynthetica 2009, 47:483-498.
54. Lazár D., Jablonský J. On the approaches applied in formulation of a kinetic model of photosystem II: different approaches lead to different simulations of the chlorophyll a fluorescence transients. J. Theor. Biol. 2009, 257:260-269.
55. Lazár D., Pospíšil P. Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3',4'-dichlorophenyl)-1,1-dimethylurea-treted barley leaves at room and high temperatures. Eur. Biophys. J. 1999, 28:468-477.
56. Lazár D., Schansker G. Models of chlorophyll a fluorescence transients. Photosynthesis in silico: understanding complexity from molecules to ecosystems, Advances in Photosynthesis and Respiration 2009, vol. 29:85-123. Springer, Dordrecht.
57. Lazár D., Nauš J., Matoušková M., Flašarová M. Mathematical modelling of canges in chlorophyll fluorescence induction caused by herbicides. Pest. Biochem. Physiol. 1997, 57:200-210.
58. Lazár D., Brokeš M., Nauš J., Dvořák L. Mathematical modelling of 3-(3',4'-dichlorophenyl)-1,1-dimethyl urea action in plant leaves. J. Theor. Biol. 1998, 191:79-86.
59. 2. Photosynthetica 2005, 43:13-27.
60. M). Implications for photoinhibition of photosystem II. J. Theor. Biol. 2005, 233:287-300.
61. Lebedeva G.V., Belyaeva N.E., Demin O.V., Riznichenko G.Y., Rubin A.B. Kinetic model of primary photosynthetic processes in chloroplasts. Description of the fast phase of chlorophyll fluorescence induction under different light intensities. Biophysics 2002, 47:968-980.
62. Mehler A.H. Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 1951, 33:65-77.
63. Mendes P. GEPASI: a software package for modelling the dynamics, steady states and control of biochemical and other systems. Comput. Appl. Biosci. 1993, 9:563-571.
64. Munday J.C., Govindjee Light-induced changes in the fluorescence yield of chlorophyll a in vivo III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys. J. 1969, 9:1-21.
65. Murata N. The discovery of state transitions in photosynthesis 40 years ago. Photosynth. Res. 2009, 99:155-160.
66. m' without measuring Fo'. Photosynth. Res. 1997, 54:135-142.
67. Palombi L., Cecchi G., Lognoli D., Raimondi V., Toci G., Agati G. A retrieval algorithm to evaluate the Photosystem I and Photosystem II spectral contributions to leaf chlorophyll fluorescence at physiological temperatures. Photosynth. Res. 2011, 108:225-239.
68. Papageorgiou G.C., Govindjee Photosystem II fluorescence: slow changes-Scaling from the past. J. Photochem. Photobiol., B 2011, 104:258-270.
69. Pfündel E. Estimating the contribution of Photosystem I to total leaf chlorophyll fluorescence. Photosynth. Res. 1998, 56:185-195.
70. 0 fluorescence in leaves of Arabidopsis thaliana and Zea mays. Photosynth. Res. 2013, 114:189-206.
71. Polle A. Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol. 2001, 126:445-462.
72. Polm M., Brettel K. Secondary pair charge recombination in photosystem I under strongly reducing conditions: temperature dependence and suggested mechanism. Biophys. J. 1998, 74:3173-3181.
73. Roháček K. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 2002, 40:13-29.
74. Ruban A.V., Johnson M.P. Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynth. Res. 2009, 99:173-183.
75. Samson G., Prášil O., Yaakoubd B. Photochemical and thermal phases of chlorophyll a fluorescence. Photosynthetica 1999, 37:163-182.
76. Šafránek D., Červený J., Klement M., Pospíšilová J., Brim L., Lazár D., Nedbal L. E-photosynthesis: Web-based platform for modeling of complex photosynthetic processes. Biosystems 2011, 103:115-124.
77. X. Biochim. Biophys. Acta, Bioenerg. 2005, 1708:283-310.
78. Satoh K., Strasser R., Butler W.L. A demonstration of energy transfer from photosystem II to photosystem I in chloroplasts. Biochim. Biophys. Acta 1976, 440:337-345.
79. Schansker G., Srivastava A., Govindjee R.J. Strasser, Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct. Plant Biol. 2003, 30:785-796.
80. Schansker G., Tóth S.Z., Strasser R.J. Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim. Biophys. Acta, Bioenerg. 2005, 1706:250-261.
81. B-quenching. Plant Spectrofluorometry: Applications and Basic Research, Rozenberg 2002, 23-47. Publishers, Amsterdam. O. van Kooten, J.F.H. Snel (Eds.).
82. Schreiber U., Klughammer C. Saturation pulse method for assessment of energy conversion in PSI. PAM Appl. Notes 2008, 1:11-14.
83. Schreiber U., Vidaver W. Rapid light-induced changes of energy distribution between photosystem I and II. FEBS Lett. 1976, 62:194-197.
84. Schreiber U., Nubauer C., Klughammer C. Devices and methods for room-temperature fluorescence analysis. Philos. Trans. R. Soc. London, Ser. B 1989, 323:241-251.
85. Shubin V.V., Bezsmertnaya I.N., Karapetyan N.V. Efficient energy transfer from the long-wavelength antenna chlorophylls to P700 in photosystem I complexes from Spirulina platensis. J. Photochem. Photobiol., B 1995, 30:153-160.
86. Stahl U., Tusov V.B., Paschenko V., Voight J. Spectroscopic investigations of fluorescence behavior, role and function of the long-wavelength pigments of photosystem I. Biochim. Biophys. Acta 1989, 973:198-204.
87. Stirbet A., Govindjee On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. J. Photochem. Photobiol., B 2011, 104:236-257.
88. Stirbet A., Govindjee Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth. Res. 2012, 113:15-61.
89. Stirbet A., Govindjee B.J., Strasser R.J. Strasser, Chlorophyll a fluorescence induction in higher plants: modelling and numerical simulation. J. Theor. Biol. 1998, 193:131-151.
90. Strasser R.J., Stirbet A.D. Estimation of the energetic connectivity of PS II centres in plants using the fluorescence rise O-J-I-P. Fitting of experimental data to three different PS II models. Math. Comput. Simul. 2001, 56:451-461.
91. Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim. Biophys. Acta, Bioenerg. 2010, 1797:1313-1326.
92. Sušila P., Lazár D., Ilík P., Tomek P., Nauš J. The gradient of exciting radiation within a sample affects relative heights of steps in the fast chlorophyll a fluorescence rise. Photosynthetica 2004, 42:161-172.
93. Telfer A., Barber J., Heathcote P., Evans M.C.W. Variable chlorophyll a fluorescence from P-700 enriched photosystem I particles dependent on the redox state of the reaction centre. Biochim. Biophys. Acta 1978, 504:153-164.
94. + reductase in a cyanobacterium. Biochem. 1999, 38:12735-12746.
95. Tomek P., Lazár D., Ilík P., Nauš J. On the intermediate steps between the O and P steps in chlorophyll a fluorescence rise measured at different intensities of exciting light. Aust. J. Plant Physiol. 2001, 28:1151-1160.
96. B-non-reducing photosystem II centers from chlorophyll a fluorescence induction. Plant Sci. 2003, 164:665-670.
97. Tripathy B.C., Draheim J.E., Anderson G.P., Gross E.L. Variable fluorescence of photosystem I particles and its application to the study of the structure and function of photosystem I. Arch. Biochem. Biophys. 1984, 235:449-460.
98. +: implications for the trapping mechanism. Photosynth. Res. 1997, 54:237-240.
99. Trissl H.-W., Wilhelm C. Why do thylakoid membranes from higher plants form grana stacks?. Trends. Biochem. Sci. 1993, 18:415-419.
100. Trissl H.W., Gao Y., Wulf K. Theoretical fluorescence induction curves derived from coupled differential equations describing the primary photochemistry of photosystem II by an exciton-radical pair equilibrium. Biophys. J 1993, 64:974-988.
101. Tsimilli-Michael M., Pêcheux M., Strasser R.J. Vitality and stress adaptation of the symbionts of coral reef and temperature foraminifers probed in hospite by the fluorescence kinetics OJIP. Arch. Sci. Genéve 1998, 51:205-240.
102. Valero E., González-Sánchez M.I., Maciá H., García-Carmona F. Computer simulation of the dynamic behavior of the glutathione-ascorbate redox cycle in chloroplasts. Plant Physiol. 2009, 149:1958-1969.
103. Vredenberg W.J. A three-state model for energy trapping and chlorophyllfluorescence in photosystem II incorporating radical pair recombination. Biophys. J. 2000, 79:26-38.
104. Wientjes E., Croce R. PMS: photosystem I electron donor or fluorescence quencher. Photosynth. Res. 2012, 111:185-191.
105. Zhu X.-G., Govindjee, Baker N.R., deSturler E., Ort D.R., Long S.P. Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with Photosystem II. Planta 2005, 223:114-133.