Tansley Review No. 112 Oxygen processing in photosynthesis: regulation and signalling

Abstract

I. INTRODUCTION 360

II. PHOTOINHIBITION AND ACTIVE OXYGEN 360

III. OXYGEN AS AN ELECTRON ACCEPTOR 362

1. Oxygen ‘poises’ electron transport and carbon assimilation 362

2. The role of oxygen in ATP synthesis 364

3. How fast is O₂reduction at PSI? 364

4. Chloroplastic processing of H₂O₂ 366

IV. REDOX REGULATION OF PHOTOSYNTHETIC METABOLISM 368

1. The thioredoxin system 368

2. Manipulating the expression of thiol-regulated enzymes 369

3. Modifying sensitivity to thiol regulation 369

V. PHOTORESPIRATION 369

1. The pathway and its genetic manipulation 369

2. Engineering plants that photorespire less? 371

3. Is photorespiration important in energy dissipation? 372

4. Production and processing of photorespiratory H₂O₂ 373

5. Catalase and foliar H₂O₂levels 374

6. Catalase and non-photorespiratory H₂O₂generation 375

VI. RESPIRATION 376

1. ‘Photosynthetic’ respiration 376

2. AOS in the mitochondrion 376

3. AOX: regulation and significance to photosynthesis 377

VII. PHOTOSYNTHESIS AND REDOX SIGNAL TRANSDUCTION 378

1. The need for sensors, signals and transducers 378

2. Signal transduction at the local level 378

3. Remote signalling and responses leading to acclimation of photosynthesis? 379

4. Interactions between AOS, NO^., and antioxidants 380

VIII. CONCLUSIONS 380

Acknowledgements 381

References 381

The gradual but huge increase in atmospheric O₂ concentration that followed the evolution of oxygenic photosynthesis is one consequence that marks this event as one of the most significant in the earth's history. The high redox potential of the O₂/water couple makes it an extremely powerful electron sink that enables energy to be transduced in respiration. In addition to the tetravalent interconversion of O₂ and water, there exist a plethora of reactions that involve the partial reduction of O₂ or photodynamic energy transfer to produce active oxygen species (AOS). All these redox reactions have become integrated during evolution into the aerobic photosynthetic cell. This review considers photosynthesis as a whole-cell process, in which O₂ and AOS are involved in reactions at both photosystems, enzyme regulation in the chloroplast stroma, photorespiration, and mitochondrial electron transport in the light. In addition, oxidants and antioxidants are discussed as metabolic indicators of redox status, acting as sensors and signal molecules leading to acclimatory responses. Our aim throughout is to assess the insights gained from the application of mutagenesis and transformation techniques to studies of the role of O₂ and related redox components in the integrated regulation of photosynthesis.