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The Biogenesis and Assembly of Photosynthetic Proteins in Thylakoid Membranes1

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The Biogenesis and Assembly of Photosynthetic Proteins in Thylakoid Membranes1 Biochimica et Biophysica Acta 1411 (1999) 21^85 Review The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1 Francis-Andre Wollman a;*, Limor Minai b, Rachel Nechushtai b a UPR/CNRS 1261, Institut de Biologie Physico-chimique, 13 rue Pierre et Marie Curie, 75005 Paris, France b Department of Botany, The Hebrew University of Jerusalem, Jerusalem 91904, Israel Received 3 November 1998; received in revised form 27 January 1999; accepted 22 February 1999 Keywords: Chloroplast; Thylakoid membrane; Protein biogenesis; Protein assembly; Protein import; Protein processing Contents 1. Introduction .......................................................... 22 2. Production of the `substrate-subunits' for protein assembly . ....................... 24 2.1. Some distinctive features of photosynthetic prokaryotes and eukaryotes . ........ 24 2.2. Control mechanisms speci¢cally functioning in photosynthetic eukaryotes . ........ 27 3. Conveyance of the PPs to the thylakoid membranes . ............................ 30 3.1. Site of translation of the cyanobacterial and chloroplast-encoded PP subunits ....... 30 3.2. Targeting to the organelle and import . .................................. 32 3.3. Maturation of the precursor: the processing step ............................ 33 3.4. Insertion, assembly and translocation into the thylakoid membranes . ............. 34 4. The biogenesis of PPs: self-assembly or assisted process? . ....................... 35 5. Photosystem II . ...................................................... 36 5.1. The assembled protein ................................................ 37 5.2. Expression and assembly . ............................................ 40 6. Photosystem I . ...................................................... 46 6.1. The assembled protein ................................................ 46 6.2. Expression and assembly . ............................................ 48 7. Antenna proteins . ...................................................... 52 7.1. The assembled proteins . ............................................ 53 7.2. Expression and assembly . ............................................ 54 * Corresponding author. Fax: +33 (1) 4046-8331; E-mail: [email protected] 1 This article is dedicated to the memory of our colleague and friend, Alma Gal. Her presence played a major role in our decision to prepare this review article. 0005-2728 / 99 / $ ^ see front matter ß 1999 Elsevier Science B.V. All rights reserved. PII: S0005-2728(99)00043-2 BBABIO 44752 14-4-99 22 F.-A. Wollman et al. / Biochimica et Biophysica Acta 1411 (1999) 21^85 8. The cytochrome b6f complex . ............................................ 58 8.1. The assembled protein ................................................ 58 8.2. Expression and assembly of the constitutive subunits . ....................... 61 9. The chloroplast ATP synthase . ............................................ 66 9.1. The assembled protein ................................................ 66 9.2. Expression and assembly of the constitutive subunits . ....................... 67 10. Concluding remarks . ................................................. 71 10.1. Supercomplex formation . ............................................ 71 10.2. Future issues ...................................................... 72 Acknowledgements . ...................................................... 74 References ............................................................... 74 1. Introduction has tremendously improved our knowledge of the actual composition and topological organization of Oxygenic photosynthesis is an energy-transducing most of the photosynthetic proteins. Second, the ¢eld process whereby light energy is trapped and con- of protein biogenesis should bene¢t greatly from the verted into biochemical energy. This multi-step proc- implementation of whole genome sequencing pro- ess encompasses a series of electron transfer reactions jects. This global genetic approach, when combined from water molecules to NADP (nicotinamide ad- with new gene transformation strategies and the use enine dinucleotide phosphate), coupled to ATP syn- of reverse genetics, should complement and extend thesis. Oxygenic photosynthesis occurs within the our knowledge of the numerous biogenesis factors thylakoid membranes of photosynthetic prokaryotes which was originally based only on classical genetic and eukaryotes and is mainly borne by ¢ve types of approaches and membrane protein biochemistry. proteins which are embedded in these membranes: In recent years, some of the most signi¢cant in- photosystem II cores (CCII); cytochrome b6f com- sights into thylakoid protein assembly have come plexes; photosystem I cores (CCI); antenna proteins; from comparing the phenotype of mutants resulting and proton-ATP synthases (CF1^CF0). These pro- from similar gene disruptions or similar site-directed teins function in a concerted manner to generate mutagenesis in photosynthetic prokaryotes, and pho- ATP and a reducing power in the presence of light. tosynthetic eukaryotes. These approaches, together The major Photosynthetic Proteins, hereafter re- with the availability of in vitro expression systems ferred to as PPs, are multiple-subunit protein com- including the recent development of a promising ho- plexes (see Fig. 1). They span the thylakoid mem- mologous in vitro translation system [1], paved the branes and comprise both peripheral and integral way for a re¢ned study of the assembly pathways for membrane subunits. The functional proteins also en- photosynthetic proteins. compass a variety of cofactors, pigments, hemes, The present review does not cover the biogenesis iron^sulfur clusters and metal ions, that associate of PPs from prokaryotes performing anoxygenic with the protein moieties either by covalent or non- photosynthesis. Some aspects of their gene expres- covalent binding. The aim of the present review is to sion and assembly will occasionally be discussed, to- present events and steps involved in the biogenesis gether with aspects of mitochondrial protein expres- and assembly of PPs and to raise questions concern- sion, whenever we feel that they add to our ing these processes that remain elusive to date. understanding of the PP assembly in organisms per- The study of the biogenesis of these complex mul- forming oxygenic photosynthetic. Tissue speci¢city ti-molecular structures is entering a new phase for and developmental changes of PP assembly in vascu- two major reasons. First, the remarkable develop- lar plants, as well as the repair processes and changes ment of the structural biology of membrane proteins in protein expression and assembly under stress con- BBABIO 44752 14-4-99 F.-A. Wollman et al. / Biochimica et Biophysica Acta 1411 (1999) 21^85 23 Fig. 1. Photosynthetic complexes of the thylakoid membranes. The compositions of the di¡erent photosynthetic complexes and their dimensions are drawn according to structural data available in the literature. CCI is drawn from the 4-Aî resolution structure of cya- nobacteria [323]. The exact position of PSI-G, PSI-H, and PSI-N that are present only in higher plants, is presently unknown. The sketch of CCII follows the structure of Morris et al. [220]. The only structural data available for some light harvesting complexes comes from the 3.4-Aî resolution structure of LHCII [406]. The trimer is drawn based on [621]. Since the nature of the trimer, i.e. ho- motrimer or heterotrimer, is currently unknown, (i) stands for either LhcbI, II or III. The minor antenna complexes, PSII-S and Lhca antenna are not represented. The structural data available on the bc1 complex from bovine heart mitochondria [486] served as the ba- sis for drawing the cyt b6f complex. However, the dimensions of the Rieske protein and cyt f were taken from chloroplast structures î [480,489]. The ATP synthase sketch is based on the 2.8-A resolution structure of the F1 portion from bovine heart mitochondria and on the model recently suggested by Engelbrecht and Junge [549]. Arrows indicate the direction of movement of the rotor upon ATP synthesis. Black ¢lled subunits are nuclear-encoded; gray ¢lled subunits are chloroplast-encoded. ditions are beyond the scope of this review. We refer and temporal separation between these three proc- the reader to recent review articles which cover these esses may be somewhat virtual, each of these three matters, at least in part [2^5]. aspects allows one to raise speci¢c questions. In view of the above, we have chosen to address (1) Regarding the biogenesis of individual sub- the issue of thylakoid protein assembly under what units, here considered as the substrates in the multi- can be regarded as steady-state conditions. These ple order reaction leading to protein assembly, a key correspond to the conditions that prevail in the ex- issue is to identify the critical step(s) that control(s) panding mature chloroplast in vascular plants or in their actual intracellular concentration. These may the exponential phase of growth for unicellular pro- vary among organisms since we are considering pro- karyotes or eukaryotes. Although each PP may have teins that are well-conserved between prokaryotic speci¢c biogenesis features, there should be general and eukaryotic cells. There is now overwhelming evi- rules, or constraints, which govern some aspects of dence that the limiting steps in protein biogenesis in assembly. These rules require a transverse approach photosynthetic eukaryotes are post-transcriptional
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