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Photosynthesis Research 80: 109–124, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.

109

Historical review

Unraveling the Photosystem I reaction center: a history, or the sum of many efforts
Petra Fromme1,∗ & Paul Mathis2,∗
1 Department

of Chemistry and Biochemistry, Arizona State University, Main Campus Room PSC-307, PO Box 871604, Tempe, AZ 85287-1604, USA; 2Section de Bio´ nerg´ tique, D´ partement de Biologie Cellue e e laire et Mol´ culaire CEA Saclay, 91191 Gif-sur-Yvette, Cedex, France; ∗ Authors for correspondence (e-mail: e pfromme@asu.edu; mathis.paul@wanadoo.fr; fax: +1-480-965-2747; +33-1-69088717)

Received 29 July 2003; accepted in revised form 12 December 2003

Key words: Herv´ Bottin, Klaus Brettel, crystal structure,crystallization, electron transfer, Petra Fromme, Olaf e Klukas, Norbert Krauß, Bernard Lagoutte, light harvesting, Paul Mathis, membrane protein, microgravity, photosynthesis, Photosystem I, Bill Rutherford, Wolfram Saenger, Wolf-Dieter Schubert, Pierre S´ tif, space shuttle, e Horst T. Witt, X-ray crystallography

Abstract This article describes some aspects of the history of the discovery of the structureand function of Photosystem I (PS I). PS I is the largest and most complex membrane protein for which detailed structural and functional information is now available. This short historical review cannot cover all the work that has been carried out over more than 50 years, nor provide a deep insight into the structure and function of this protein complex. Instead, this review focuses on morepersonal views of some of the key discoveries, starting in the 1950s with the discovery of the existence of two photoreactions in oxygenic photosynthesis, and ending with the race towards an atomic structure of PS I. Abbreviations: CD – circular dicroism; DCMU – 3-(3,4-dichlorophenyl)-1,1-dimethylurea; DPIP – 2,6dichlorophenol-indophenol; EM – electron microscopy; EPR – electron paramagnetic resonance;FNR – ferredoxin:NADP+ oxidoreductase; PC – plastocyanin; RC – reaction center The search for a reasonable model It has long been known that photosynthesis is the main process on earth that converts light energy from the sun into chemical energy. The primary processes of photosynthesis in plants are located in special organelles, the chloroplasts, and chlorophyll plays a key role in this process.However, the nature of the biomolecules involved in this process long remained a mystery (Rabinowitch 1956). Light was shed on the process in the middle of the last century, when the concept of two photosystems was introduced and confirmed by experimental evidence. The idea of System 1 and System 2 as physical parts of the photosynthetic apparatus and the seats of light-induced charge separation,each with specific antenna pigments, was first introduced by Duysens in 1960 (Duysens 1960; Duysens et al. 1961; see also the historical reviews of Duysens 1989 and Witt, this issue). A few properties of Photosystem I (PS I) had already been discovered as separate observations made in oxygen-evolving organisms, but they were not yet integrated in a coherent scheme. These observations included thefollowing: • The specific action of far-red light, in the so-called Emerson effect. • The existence of non-fluorescing chlorophyll a. • The ability of chloroplasts to photo-reduce NADP+ for the reduction of CO2 .

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Figure 1. The pathway of electron transfer (thin arrows) from water to NADP+ in oxygenic photosynthesis. Broad vertical arrows indicate transfer of absorbed excitation energy (hν)from the light-harvesting antennae to the reaction center of each of the two photosystems, PS I and PS II. The wavy line indicates the site of inhibition of electron transfer by DCMU (3(3,4-dichlorophenyl)-1,1 -dimethylurea).

• P700, discovered by Kok (1956) as a chlorophyll species giving rise to a bleaching at 705 nm under the effect of light. • A light-induced EPR signal, discovered in 1956,...
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