Peter Westhoff

Institut für Entwicklungs- und Molekularbiologie der Pflanzen der Heinrich-Heine-Universität, Universitätsstr. 1, D-40226 Düsseldorf, Germany

I. Introduction 2

II. Aspects of Chloroplast and Plant Genome Evolution—Plant Genome Structure 5

III. Functional Consequences of Genome Rearrangement—Regulatory Levels 11

A. Nuclear Gene Expression 11

1. Promoter Structure and Evolution 11

2. Protein Import into Chloroplasts—Assembly Processes 12

1. Transcriptional Control 15

2. Posttranscriptional Regulation 16

4. Nuclear Regulatory Control 18

IV. The Impact of Multicellularity and Terrestrial Life upon Thylakoid Biogenesis 18

V. Maintenance and Acclimation of Thylakoids 19

B. Transcri ptomics and Proteomics 22

Acknowledgments 23

Summary

Biogenesis, maintenance, and adaptation of the thylakoid system in photosynthetic organelles are embodied in the genetic machinery of the plant cell. Plant cells are descendants of endosymbioses. Their genomes are compartmentalized and the result of a complex restructurating of the genetic potentials of (depending on the organism) three to five symbiotic partner cells during evolution that led to a common metabolism and a common inheritance in the entity. It appears that much of the thylakoid biogenesis and dynamics can be understood from the history of the plant cell. Inter-endosymbiotic genome restructuration included loss, gain, and intracellular transfer of genetic material. It was accompanied (i) by the generation of an integrated genetic system (rather

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Eva-Mari Aro and Bertil Andersson (eds): Regulation of Photosynthesis, pp. 1-28. © 2001 Kluwer Academic Publishers. Printed in The Netherlands.

than a nucleus and semiautonomous organelles) that in its entirety is spatiotemporally regulated, (ii) by a massive intermixing of structural genes, (iii) a fundamental change in expression signals in the entire system which included the evolution of an exquisite set ofregulatory mechanisms that operate in concert with basically ancient regulatory circuits originating in the organelle ancestors, and (iv) by the establishment of nuclear regulatory dominance that is found at all levels ofregulation. Most conspicuous are fundamental changes of the transcription machinery in all three subgenomes, in the establishment of an elaborate posttranscriptional RNA modification system in chloroplasts that prokaryotes are largely lacking, and in sophisticated protein trafficking and assembly devices. The genetics of the photosynthetic machinery was fitted into the respective genetic programs for multicellular and terrestrial plants that developed new biochemistries including those for a spatiotemporal morphogenetic potential.

I. Introduction

Life on earth ultimately depends on energy derived from the sun. Photosynthesis is globally the only process of biological importance that can harvest this energy. It provides energy, organic matter, in its oxygenic version also oxygen, for nearly all biotic processes, and represents the only renewable energy source of our planet. The photosynthetic process is remarkably effective since it captures almost all the energy of the light it absorbs. Life would have been different, or probably even extinct, without the utilization of the external energy source through biological photosynthesis. If we can trust fossil records, this process was invented as early as >3.85 billion years ago, no more than 600-700 million years after the creation of the planet Earth. Photosynthesis has undergone crucial changes with far-reaching global consequences, notably the generation of the Photosystem II assembly which is capable to use solar energy to catalyze the breakdown of water to reducing equivalents and molecular oxygen. This caused the change from a reducing to an oxidizing environment. To date, the amount of energy stored by photosynthesis is enormous. Estimates suggest that more than 10.000 million tons of carbon are transformed annually into carbohydrate and other forms of organic matter.

In plants, photosynthesis takes place in a distinct cellular organelle, the chloroplast (rhodoplast, cy anoplast, phaeoplast etc.). Typical photoautotrophic

Abbreviations: CFo - coupling factor membrane moiety of ATP synthase; DPE - downstream promoter element; ER -endoplasmatic reticulum; EST - expressed sequence tag; FNR -ferredoxin NAD(P)H oxidoreductase; GAPDH - glyceraldehyde-3 phosphate dehydrogenase; Inr - initiator; NEP - nuclear-encoded DNA-dependent RNA polymerase in chloroplasts; PCR -polymerase chain reaction; PEP - plastid-encoded DNA-dependent RNA polymerase; RT-PCR - reverse transcriptase PCR; SRP - signal receptor particle organelles are double membrane-bound, those of secondary or tertiary endosymbiotic origin (Section II) triple- or quadruple membrane-bound entities. Their thylakoid system and stroma house the functional components required both for the light-driven and enzymatic reactions of the process. Thylakoid membranes are unique biomembranes. In oxygenic photosynthesis, they are specialized of converting inorganic substrates ( C02 and H20) with solar energy to utilizable high-energy chemical metabolites, initially in the forms of ATP and NADPH. These compounds in turn provide the necessary energy and reduction equivalents for the 'dark' reactions, i.e. the fixation of atmospheric C02 in carbohydrates. Severaldifferentmultisubunitprotein complexes are inserted in the lipid bilayers of thylakoid membranes in a vectorially oriented way (Fig. 1; reviewed in Herrmann et al., 1991; Andersson and Barber, 1994). These supramolecular protein assemblies, the Photosystems I and II, each with an ensemble of light-collecting antenna, the cytochrome bj complex, the ATP synthase, and the NAD(P)H dehydrogenase, bind and organize pigments and other non-proteinaceous cofactors. Together with mobile electron carriers in the stroma (ferredoxin, FNR), the lumen (plastocyanin), and the lipid bilayer (plasto-quinone) they cooperate in the conversion of radiant energy, and provide the link to the stromal metabolism (Fig. 1).

The photosynthetic process is anchored in the genetic system of the plant cell. Plant cells and their genomes are beyond doubt the result of endocyto-bioses (Fig. 2; Woese, 1987; Woese et al., 1990). Chloroplasts, as mitochondria, are descendants of endosymbiotic cells and have preserved remnants of the ancestral genomes which is a second fundamental feature ofphotoautotrophic organelles. They contain not only DNA, but also the mechanisms to maintain this information and to convert it into function.

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