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Photosynthetic Energy Transfer and Charge Separation in Higher Plants

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The Biophysics of Photosynthesis

Abstract

In this chapter we introduce the physical models at the basis of photosynthetic light harvesting and energy conversion (charge separation). We discuss experiments that demonstrate the processes of light harvesting in the major plant light-harvesting complex (LHCII) and charge separation in the photosystem II reaction center (PSII RC) and how these processes can be modeled at a quantitative level. This is only possible by taking into account the exciton structure of the chromophores in the pigment–protein complexes, static (conformational) disorder, and coupling of electronic excitations and charge-transfer (CT) states to fast nuclear motions. We give examples of simultaneous fitting of linear and nonlinear (time-dependent) spectral responses based on modified Redfield theory that resulted in a consistent physical picture of the energy- and electron-transfer reactions. This picture, which includes the time scales and pathways of energy and charge transfer, allows for a visualization of the excitation dynamics, thus leading to a deeper understanding of how photosynthetic pigment-proteins perform their function in the harvesting and efficient conversion of solar energy. We show that LHCII has the intrinsic capacity to switch between different light-harvesting and energy-dissipating (quenched) states. We introduce the conformational “switching” model for the LHCII protein to explain its role both in light harvesting and in photoprotection. This model explains how the local environment of the protein controls its intrinsic conformational disorder to serve a functional role. Finally, we demonstrate that the PSII RC performs charge separation via two competing pathways of which the selection depends on the conformational disorder induced by slow protein motions. Therefore, we show that the pigment–protein interactions play a decisive role in controlling the functionality of the pigment–protein complexes at work in photosynthesis.

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Abbreviations

2DES:

Two-dimensional electronic spectroscopy

CD:

Circular dichroism

Chl:

Chlorophyll

ChlZ :

Additional chlorophylls bound at the periphery of the photosystem II reaction center

CS:

Charge separation

CT:

Charge transfer, D1/D2/Cytb 559 —reaction center of photosystem II

FL:

Fluorescence

FLN:

Fluorescence line-narrowing

LD:

Linear dichroism

LHCII:

Major light-harvesting complex II of plants

NPQ:

Nonphotochemical quenching of chlorophyll a fluorescence

OD:

Optical density (absorption)

P:

Special pair of chlorophylls in reaction center

Phe:

Pheophytin

PR:

Participation ratio

PSI, PSII:

Photosystem I, photosystem II

qE:

Major, energy-dependent component of NPQ

Qy, Qx :

Lowest electronic transitions of Chl and Phe

RC:

Reaction center

RC5:

RC6, reaction center of photosystem II lacking one peripheral Chl, and containing all peripheral Chls

SMS:

Single-molecule spectroscopy

TA:

Transient absorption

ZPL:

Zero-phonon line

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Acknowledgments

This work was supported by the EU FP6 Marie Curie Early Stage Training Network via the Advanced Training in Laser Sciences project (T.P.J.K.); a visitor’s grant from the Netherlands Organization for Scientific Research (NWO) (V.N.), the Russian Foundation for Basic Research (12-04-01085) (V.N.); TOP grant (700.58.305) from the Foundation of Chemical Sciences (CW), part of the NWO (T.P.J.K. and R.v.G.), and the Advanced Investigator Grant (267333, PHOTPROT) from the European Research Council (ERC) (T.P.J.K., E.R., and R.v.G.).

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Correspondence to Tjaart P. J. Krüger Ph.D. or Rienk van Grondelle Ph.D. .

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Krüger, T.P.J., Novoderezhkin, V.I., Romero, E., van Grondelle, R. (2014). Photosynthetic Energy Transfer and Charge Separation in Higher Plants. In: Golbeck, J., van der Est, A. (eds) The Biophysics of Photosynthesis. Biophysics for the Life Sciences, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1148-6_3

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