Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Dynamics of the energy flow through photosystem II under changing light conditions: a model approach

Albert Porcar-Castell A B , Jaana Bäck A , Eija Juurola A and Pertti Hari A
+ Author Affiliations
- Author Affiliations

A Department of Forest Ecology, University of Helsinki, Latokartanonkaari 7, PO Box 27, 00014 Helsinki, Finland.

B Corresponding author. Email: joan.porcar@helsinki.fi

Functional Plant Biology 33(3) 229-239 https://doi.org/10.1071/FP05133
Submitted: 2 June 2005  Accepted: 19 October 2005   Published: 2 March 2006

Abstract

Several biochemical models of photosynthesis exist that consider the effects of the dynamic adjustment of enzymatic and stomatal processes on carbon assimilation under fluctuating light. However, the rate of electron transport through the light reactions is commonly modelled by means of an empirical equation, parameterised with data obtained at the steady state. A steady-state approach cannot capture the dynamic nature of the adjustment of the light reactions under fluctuating light. Here we present a dynamic model approach for photosystem II that considers the adjustments in the regulative non-photochemical processes. The model is initially derived to account for changes occurring at the seconds-to-minutes time-scale under field conditions, and is parameterised and tested with chlorophyll fluorescence data. Results derived from this model show good agreement with experimentally obtained photochemical and non-photochemical quantum yields, providing evidence for the effect that the dark reactions exert in the adjustment of the energy flows at the light reactions. Finally, we compare the traditional steady-state approach with our dynamic approach and find that the steady-state approach produces an underestimation of the modelled electron transport rate (ETR) under rapidly fluctuating light (1 s or less), whereas it produces overestimations under slower fluctuations of light (5 s or more).

Keywords: chlorophyll fluorescence, dynamic model, electron transport rate, fluctuating light, non-photochemical quenching, xanthophyll-cycle.


Acknowledgments

This work was supported by the Academy of Finland (Pr. No. 45750 and 47506) as well as the Maj and Tor Nessling Foundation (Pr. No. 2004131). The authors thank Prof. Esa Tyystjärvi for his valuable comments.


References


Allen MT, Pearcy RW (2000) Stomatal versus biochemical limitations to dynamic photosynthetic performance in four tropical rainforest shrub species. Oecologia 122, 479–486.
Crossref | GoogleScholarGoogle Scholar | open url image1

Amerongen, H ,  and  Dekker, JP (2003). Light-harvesting in photosystem II. In ‘Light-harvesting antennas in photosynthesis’. pp. 219–251. (Kluwer Academic Publishers: Dordrecht)

Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113–134.
PubMed |
open url image1

Barber J, Malkin S, Telfer A (1989) The origin of chlorophyll fluorescence in vivo and its quenching by the photosystem II reaction centre. Philosophical Transactions of the Royal Society of London B 323, 227–239. open url image1

Bernhardt K, Trissl H-W (1999) Theories for kinetics and yields of fluorescence and photochemistry: how, if at all, can different models of antenna organisation be distinguished experimentally? Biochimica et Biophysica Acta 1409, 125–142.
PubMed |
open url image1

Bruce, D ,  and  Vasil’ev, S (2004). Excess light stress: multiple dissipative processes of excess excitation. In ‘Chlorophyll fluorescence: a signature of photosynthesis’. pp. 497–523. (Springer: Dordrecht)

Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochemistry and Photobiology 60, 1–23. open url image1

Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Adams WW, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98, 253–264.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Moeller DL, Logan BA, Adams WW (1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Scheffera arboricola (Hayata) Merrill. Planta 205, 367–374.
Crossref | GoogleScholarGoogle Scholar | open url image1

Eskling, M , Emanuelsson, A ,  and  Åkerlund, H-E (2001). Enzymes and mechanisms for violaxanthin–zeaxanthin conversion. In ‘Regulation of photosynthesis’. pp. 433–452. (Kluwer Academic Publishers: Dordrecht)

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
Crossref | GoogleScholarGoogle Scholar | open url image1

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92. open url image1

Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99, 197–209.
Crossref | GoogleScholarGoogle Scholar | open url image1

Govindjee (2004). Chlorophyll a fluorescence: a bit of basics and history. In ‘Chlorophyll fluorescence: a signature of photosynthesis’. pp. 1–42. (Springer: Dordrecht)

Gross LJ (1982) Photosynthetic dynamics in varying light environments: a model and its application to whole leaf carbon gain. Ecology 63, 84–93. open url image1

Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state-transitions. Trends in Plant Science 6, 301–305.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hari P, Mäkelä A, Korpilahti E, Holmberg M (1986) Optimal control of gas exchange. Tree Physiology 2, 169–175.
PubMed |
open url image1

Hari P, Mäkelä A (2003) Annual pattern of photosynthesis in Scots pine in the boreal zone. Tree Physiology 23, 145–155.
PubMed |
open url image1

Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences USA 96, 8762–8767.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynthesis Research 82, 73–81.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224–230.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta 376, 105–115.
PubMed |
open url image1

Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209–218.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krause, GH ,  and  Jahns, P (2003). Pulse amplitude modulated chlorophyll fluorometry and its application in plant science. In ‘Light-harvesting antennas in hotosynthesis’. pp. 373–399. (Kluwer Academic Publishers: Dordrecht)

Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Functional Plant Biology 31, 743–756.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kruse O (2001) Light-induced short-term adaptation mechanisms under redox control in the PSII–LHCII supercomplex: LHCII state transitions and PSII repair cycle. Die Naturwissenschaften 88, 284–292.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Laisk A, Oja V, Rasulov B, Eichelmann H, Sumberg A (1997) Quantum yields and rate constants of photochemical and nonphotochemical excitation quenching. Plant Physiology 115, 803–815.
PubMed |
open url image1

Lawlor, DW (2001). ‘Photosynthesis.’ (BIOS Scientific publishers: Oxford)

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence — a practical guide. Journal of Experimental Botany 51, 659–668.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Morosinotto T, Caffarri S, Dall’Osto L, Bassi R (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiologia Plantarum 119, 347–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Naumburg E, Ellsworth DS (2002) Short-term light and leaf photosynthesis dynamics affect estimates of daily understory photosynthesis in four tree species. Tree Physiology 22, 393–401.
PubMed |
open url image1

Nixon, PJ ,  and  Mullineaux, CW (2001). Regulation of photosynthetic electron transport. In ‘Regulation of photosynthesis’. pp. 533–555. (Kluwer Academic Publishers: Dordrecht)

Parson, WW ,  and  Nagarajan, V (2003). Optical spectroscopy in photosynthetic antennas. In ‘Light-harvesting antennas in hotosynthesis’. pp. 83–127. (Kluwer Academic Publishers: Dordrecht)

Pearcy RW, Gross LJ, He D (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant, Cell and Environment 20, 411–424.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pfündel E (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynthesis Research 56, 185–195.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rabinowich, E ,  and  Govindjee, (1969). ‘Photosynthesis.’ (John Wiley and Sons: New York)

Rintamäki E, Salonen M, Suoranta U-M, Carlberg I, Andersson B, Aro E-M (1997) Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo.  Journal of Biological Chemistry 272, 30476–30482.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Roden JS, Pearcy RW (1993) Photosynthetic gas exchange response of poplars to steady-state and dynamic light environments. Oecologia 93, 208–214.
Crossref | GoogleScholarGoogle Scholar | open url image1