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Beschreibung

Photosynthesis is one of the most important processes that affects all life on Earth, and, even now in the twenty-first century, it is still being studied and tested by scientists, chemists, and botanists.  Regardless of politics or opinion, climate change is one of the most polarizing and important, potentially dangerous, issues facing the future of our planet, and a better understanding of photosynthesis, and how it is changing with our global climate, could hold the answers to many scientific questions regarding this important phenomenon.

This edited volume, written by some of the world’s foremost authorities on photosynthesis, presents revolutionary new ideas and theories about photosynthesis, and how it can be viewed and studied at various levels within organisms. Focusing on the molecular, cellular, and organismic levels, the scientists who compiled this volume offer the student or scientist a new approach to an old subject.  Looking through this new lens, we can continue to learn more about the natural world in which we live and our place in it.

Valuable to the veteran scientist and student alike, this is a must-have volume for anyone who is researching, studying, or writing about photosynthesis. There are other volumes available that cover the subject, from textbooks to monographs, but this is the first time that a group of papers from this perspective has been gathered by an editor for publication. It is an important and enlightening work on a very important subject that is integral to life on Earth.

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Veröffentlichungsjahr: 2015

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Contents

Cover

Half Title page

Title page

Copyright page

Abstract

Preface

List of Contributors

Chapter 1: The Multiple Roles of Various Reactive Oxygen Species (ROS) in Photosynthetic Organisms1

1.1 Introduction

1.2 Generation, Decay and Deleterious Action of ROS

1.3 Non-photochemical Quenching in Plants and Cyanobacteria

1.4 Monitoring of ROS

1.5 Signaling Role of ROS

1.6 Light-Induced ROS and Cell Redox Control and Interaction with the Nuclear Gene Expression

1.7 Second Messengers and Signaling Molecules in H2O2 Signaling Chains and (Nonlinear) Networking

1.8 Concluding Remarks and Future Perspectives

Acknowledgments

Abbreviations

References

Chapter 2: Photooxidation of Mn-bicarbonate Complexes by Reaction Centers of Purple Bacteria as a Possible Stage in the Evolutionary Origin of the Water-Oxidizing Complex of Photosystem II

2.1 Introduction

2.2 Appearance of Photosynthesis

2.3 Classification of Photosynthetic Bacteria

2.4 Mechanism of Light Energy Transformation during Photosynthesis

2.5 The Water-oxidizing Complex of Photosystem II

2.6 Localization and Function of Bicarbonate in Photosystem II

2.7 Composition and Electrochemical Properties of Mn2+-bicarbonate Complexes

2.8 A Possible Role of Mn2+-bicarbonate Complexes for the Origin and Evolution of the Inorganic Core of the Water-oxidizing Complex of Photosystem II

2.9 Investigation of Redox Interaction Between Mn2+ and Type II Reaction Centers of Anoxygenic Photosynthetic Bacteria in the Presence of Bicarbonate

2.10 Influence of the Redox Potential of the P+/P Pair and Steric Accessibility of P+ on Electron Donation from Mn2+ to Type II Reaction Centers from Anoxygenic Photosynthetic Bacteria in the Presence of Bicarbonate

2.11 Conclusions

Acknowledgments

Abbreviations

References

Chapter 3: Hydrogen Metabolism in Microalgae

3.1 Introduction

3.2 Physiology of Hydrogen Metabolism

3.3 Hydrogenases

3.4 Ferredoxin

3.5 Nutrient Deprivation

3.6 Physiological Significance of Light-Dependent Hydrogen Production

3.7 Practical Importance of Hydrogen Photoproduction

3.8 Towards Practical Application of Microalgal Hydrogen Production

3.9 Conclusion

Acknowledgements

Abbreviations

References

Chapter 4: The Structure and Regulation of Chloroplast ATP Synthase

4.1 Introduction

4.2 The Structure and Functional Basics of Chloroplast ATP Synthase

4.3 The Thiol-Dependent Mechanism of Chloroplast ATP Synthase Regulation

4.4 The Nucleotide-Dependent Mechanism of Chloroplast ATP Synthase Regulation

4.5 The Properties and the Role of Chloroplast ATPase Noncatalytic Sites

4.6 Conclusion

Abbreviations

References

Chapter 5: Structural and Functional Organization of the Pigment-Protein Complexes of the Photosystems in Mutant Cells of Green Algae and Higher Plants

5.1 Introduction

5.2 The Mutants as Model Objects

5.3 The Chlorophyll-Protein Complexes

5.4 Spectral Properties of Native Chlorophyll-Protein Complexes

5.5 Functional Organization of the Photosystems

5.6 Structural Localization of the Photosystem in Chloroplast Thylakoids

5.7 Molecular Organization of the Complexes of Photosystem I and II

Abbreviations

References

Chapter 6: Photosynthetic Carbon Metabolism: Strategy of Adaptation over Evolutionary History

6.1 Introduction

6.2 Photosynthesis in Prokaryotes

6.3 Photosynthesis in Eukaryotes

6.4 About Compartmentalization and Cooperation between the Reduction and Oxidation Reactions in Photosynthetic Cells

6.5 Examples of Physiological Adaptation of Photosynthetic Carbon Metabolism to Environmental Factors at the Cellular, Tissue, and Organism Levels

6.6 General Conclusion

Acknowledgements

Abbreviations

References

Chapter 7: Adaptive Changes of Photosynthetic Apparatus to Higher CO2 Concentration

7.1 Introduction

7.2 Higher Concentration of CO2 and Its Effect on the Plants: History of the Question

7.3 Influence of the Higher CO2 Concentration on the Growth and Productivity of the Plants

7.4 Photosynthesis at Short-Term Increase of CO2 Concentration

7.5 Adaptive Changes of Photosynthetic Apparatus at Long-Term Effect of the Higher CO2 Concentration

7.6 The Role of Carbohydrate Metabolism in Regulation of the Photosynthetic Apparatus Activity at Increased CO2 Concentration

7.7 Soluble Sugars in Leaves and Other Plant Organs

7.8 Dependence of Photosynthetic Rate on Environmental Factors and its Regulation

Abbreviations

References

Chapter 8: Photosynthetic Machinery Response to Low Temperature Stress

8.1 Mechanisms of Plant Adaptation to Low Temperature

8.2 Role of Reactive Oxygen Species

8.3 Plant Cell Membranes and Their Role in Response to Low Temperature

8.4 Hormonal Response to the Temperature

8.5 Phytochrome as a Receptor of Low Temperature

8.6 Carbohydrate Function under Low Temperature

8.7 Protein Changes

8.8 Cold Stress and Photoinhibition

8.9 Molecular Mechanisms of Plants’ Response to Low Temperatures

8.10 Concluding Remarks and Future Perspectives

Acknowledgments

References

Index

Photosynthesis

New Approaches to the Molecular, Cellular, and Organismal Levelsz

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Library of Congress Cataloging-in-Publication Data:

ISBN 978-1-119-08370-2

Abstract

This book is written by Russian and international authors in the field of photosynthesis research. It is dedicated to investigations of the problems of photosynthesis at different levels of organization: molecular, cellular and organismal. The book describes the multiple roles of various reactive oxygen species in photosynthetic organisms. Further, we have presented here a discussion of the structure and function of water oxidation complex (WOC) of PS II, and a possible role of Mn-bicarbonate complex in WOC. Other important topics in this book are: the structural and functional organization of the pigment-protein complexes, the structure and regulation of chloroplast ATP-synthase, the participation of molecular hydrogen in microalgae metabolism, the current concepts on the evolution and the development of photosynthetic carbon metabolism, and the adaptive changes of photosynthesis at increased CO2 concentrations, as well as the photosynthetic machinery response to low temperature stress. The material available in this book is a unique report on the state of this trend in modern science. This book will be helpful not only for biophysicists, biochemists and experts in plant physiology, but also for a wider group of biologists; in addition, it is expected to be used in ongoing and future research work in the field. Lastly, and most importantly, it will serve to educate undergraduate, graduate and post-graduate students around the world.

Preface

Existence of life on the Earth is supported by photosynthetic organisms which provide production of organic substances and oxygen evolution. In general, photosynthesis includes primary light reactions and secondary dark reactions. Light reactions begin with absorption of photons by light harvesting photosynthetic pigments, resulting in the formation of their singlet exited states. This process is followed by excitation energy transfer from one pigment molecule to the other. Then, charge separation occurs in the photosynthetic reaction centers. Excited electrons are transferred via the photosynthetic electron transport chain (ETC), providing production of the reducing power in the form of reduced nicotinamide adenine dinucleotide phosphate (NADPH). In anoxygenic phototrophs, external hydrogen compounds are a source of the electrons, and the light is absorbed in a single photosystem. The ETC of oxygenic photosynthetics contains two photochemical systems – PS II (water-plastoquinone oxido-reductase) and PS I (plastocyanin-ferredoxin oxido-reductase) – which transfer electrons from water to NADP, using one more complex, the cytochrome-b6f-complex. The source of electrons in this case is water molecules which are decomposed by water-oxidizing complex (WOC) of the PS II. Oxygen as a “waste” product of photosynthetic water cleavage led to the present-day aerobic atmosphere. From the very first moment the interaction with oxygen generated a new condition for the existing organisms starting an evolutionary adaptation process to this new oxydizing environment. Reactive oxygen species (ROS) became a powerful selector and generated a new hierarchy of life forms from the broad range of genetic mutations represented in the biosphere. During the electron transfer from water to NADP, protons are transferred from the stroma side (the positive (p) side) to the lumen side (the negative (n) side), and when this proton gradient is dissipated through the ATP-synthase, ATP is produced.

The next stage includes biochemical processes of fixation and reduction of CO2 in photosynthetic carbon metabolism with using NADPH, and ATP. To date, the known metabolic pathways of carbon in photosynthesis can be classified into the 3-hydroxypropionat bicycle; the reductive citrate cycle, i.e., the Arnon-Buchanan cycle; C3 or the reductive pentose phosphate cycle, i.e., the Benson-Bassham-Calvin cycle; C4 or cooperative photosynthesis; Crassulacean acid metabolism (CAM); C3/C4 photosynthesis; and C4-CAM photosynthesis. Some of them, for example the 3-hydroxypropionat bicycle and the Arnon-Buchanan cycle, are specific to anoxygenic phototrophs, others, such as C4, CAM, and so on, have been in the evolution of higher plants. The most important way of carbon in photosynthesis – the Benson-Bassham-Calvin cycle – is widespread in phototrophic organisms of different taxa. Eventually, fixation and reduction of CO2 during photosynthesis leads to the formation of sugars and other organic compounds.

The present book has 8 chapters written mainly by the researchers of the Institute of Basic Biological Problems of the Russian Academy of Sciences (formerly the Institute of Photosynthesis). The each chapter describes photosynthesis at different levels of organization: molecular, cellular, and organismic. Among discussed problems in this book are: the structural and functional organization of the pigment-protein complexes; the evolutionary origin of the water-oxidizing complex of PS II; the hydrogen photoproduction coupled with photosynthesis; the structure and regulation of chloroplast ATP synthase; the formation, decay and signaling of reactive oxygen species in oxygen-evolving photosynthetic organisms during exposure to oxidative stress; the strategy of adaptation of photosynthetic carbon metabolism; the adaptive changes of photosynthesis under enhanced CO2 concentration, and the photosynthetic machinery response to low temperature stress.

The material presented here reflects, mainly, the research interests and views of the authors. We do not claim to have produced all-inclusive views of the entire field. The book is intended for a broad range of researchers and students, and all who are interested in learning the most important global process on our planet – the process of photosynthesis.

We should like to believe that this book will stimulate future researchers of photosynthesis, leading to progress in our understanding of the mechanisms of photosynthesis and in its practical use in biotechnology and human life.

We express our sincere appreciation to the 17 authors for their outstanding contribution to this book. We are extremely grateful to Academician of the Russian Academy of Sciences (RAS) V.A. Shuvalov, Academician of the Azerbaijan National Academy of Sciences J.A. Aliyev, Corresponding Member of RAS A.B. Rubin, Corresponding Member of RAS Vl.V. Kuznetsov, and Professors D.A. Los, A.M. Nosov, V.Z. Paschenko, T.E. Krendeleva, A.N. Tikhonov, V.V. Klimov, A.A. Tsygankov, Dr. I.R. Fomina, and J. Karakeyan for their permanent help and fruitful advices.

We express our deepest gratitude to Russian Science Foundation ( 14-04-00039) for their financial support.

Suleyman I. Allakhverdiev Institute of Plant Physiology, Russian Academy of Sciences; Institute of Basic Biological Problems, Russian Academy of Sciences; Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University; Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST), Daegu, Republic of Korea (e-mail: [email protected])

Suleyman I. Allakhverdiev is the head of Controlled Photobiosynthesis Laboratory at the Institute of Plant Physiology of the Russian Academy of Sciences (RAS), Moscow; Chief Research Scientist at the Institute of Basic Biological Problems RAS, Pushchino, Moscow Region; Professor at M.V. Lomonosov Moscow State University, Moscow, Russia; and Invited-Adjunct Professor at the Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST), Daegu, Republic of Korea. He is originally from Chaykend (Karagoyunly/Dilichanderesi), Armenia, and he had graduated with a B.S./M.S., in physics from the Department of Physics, Azerbaijan State University, Baku. He obtained his Dr. Sci. degree (highest/top degree in science) in plant physiology and photobiochemistry from the Institute of Plant Physiology RAS (2002, Moscow), and Ph.D. in physics and mathematics (biophysics), from the Institute of Biophysics USSR (1984, Pushchino). His Ph.D. advisors was Academician Alexander A. Krasnovsky and Dr. Sci. Vyacheslav V. Klimov. He worked for many years (1990–2007) as visiting scientist at the National Institute for Basic Biology (with Prof. Norio Murata), Okazaki, Japan, and in the Department de Chimie-Biologie, Université du Quebec à Trois Rivières (with Prof. Robert Carpentier), Quebec, Canada (1988–1990). He has been the guest editor of many (above 25) special issues in international peer-reviewed journals, as well as, currently a member of the Editorial Board of more than 15 international journals. Besides being editor-in-chief of SOAJ NanoPhotoBioSciences, associate editor of the International Journal of Hydrogen Energy, section editor of the BBA Bioenergetics, he also acts as a referee for major international journals and grant proposals. He has authored (or co-authored) more than 350 papers. He has organized several international conferences on photosynthesis. His research interests include the structure and function of photosystem II, water-oxidizing complex, artificial photosynthesis, hydrogen photoproduction, catalytic conversion of solar energy, plant under environmental stresses, and photoreceptor signaling.

List of Contributors

Azat Abdullatypov, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Suleyman I. Allakhverdiev, Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia; Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia; Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia; and Invited-Adjunct Professor at the Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST), Daegu, Republic of Korea

Karl Y. Biel, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia; and Biosphere Systems International Foundation, Tucson, Arizona, USA

Irina R. Fomina, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia; and Biosphere Systems International Foundation, Tucson, Arizona, USA

Thomas Friedrich, Technical University Berlin, Institute of Chemistry, Max-Volmer-Laboratory of Biophysical Chemistry, Berlin, Germany

Andrey A. Khorobrykh, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Vyacheslav V. Klimov, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Anatoly A. Kosobryukhov, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Vladimir D. Kreslavski, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia; and Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia

Vladimir V. Kuznetsov, Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia

Vladimir G. Ladygin, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Dmitry A. Los, Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia

Alexander N. Malyan, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Evgenia F. Markovskaya, Petrozavodsk State University, Department of Ecology and Biology, Petrozavodsk, Russia

Gernot Renger, Technical University Berlin, Institute of Chemistry, Max-Volmer-Laboratory of Biophysical Chemistry, Berlin, Germany

Franz-Josef Schmitt, Technical University Berlin, Institute of Chemistry, Max-Volmer-Laboratory of Biophysical Chemistry, Berlin, Germany

Vasily V. Terentyev, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Anatoly A. Tsygankov, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Sergey K. Zharmukhamedov, Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Chapter 1

The Multiple Roles of Various Reactive Oxygen Species (ROS) in Photosynthetic Organisms1

Franz-Josef Schmitt1, Vladimir D. Kreslavski2,3, Sergey K. Zharmukhamedov3, Thomas Friedrich1, Gernot Renger1, Dmitry A. Los2, Vladimir V. Kuznetsov2, Suleyman I. Allakhverdiev2,3,4,5,*

1Technical University Berlin, Institute of Chemistry, Max-Volmer-Laboratory of Biophysical Chemistry, Straße des 17. Juni 135, D-10623 Berlin, Germany

2Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia

3Institute of Basic Biological Problems, Russian Academy of Sciences, Institutskaya Street 2, Pushchino, Moscow Region 142290, Russia

4Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow 119991, Russia

5Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST), 333 Techno jungang-daero, Hyeonpung-myeon, Dalseong-gun, Daegu, 711-873, Republic of Korea

*Corresponding author: [email protected]

Abstract

This chapter provides an overview on recent developments and current knowledge about monitoring, generation and the functional role of reactive oxygen species (ROS) – H2O2, HO2•, HO•, OH− 1,O2 and O2−• – in both oxidative degradation and signal transduction in photosynthetic organisms including a summary of important mechanisms of nonphotochemical quenching in plants. We further describe microscopic techniques for ROS detection and controlled generation. Reaction schemes elucidating formation, decay and signaling of ROS in cyanobacteria as well as from chloroplasts to the nuclear genome in eukaryotes during exposure of oxygen-evolving photosynthetic organisms to oxidative stress are discussed that target the rapidly growing field of regulatory effects of ROS on nuclear gene expression.

Keywords: photosynthesis, plant cells, reactive oxygen species, ROS, oxidative stress, signaling systems, chloroplast, cyanobacteria, nonphotochemical quenching, chromophore-activated laser inactivation, sensors

1.1 Introduction

About 3 billion years ago the atmosphere started to transform from a reducing to an oxidizing environment as evolution developed oxygenic photosynthesis as key mechanism to efficiently generate free energy from solar radiation (Buick, 1992; Des Marais, 2000; Xiong and Bauer, 2002; Renger, 2008; Rutherford et al., 2012; Schmitt et al., 2014a). Entropy generation due to the absorption of solar radiation on the surface of the Earth was retarded by the generation of photosynthesis, and eventually a huge amount of photosynthetic and other organisms with rising complexity developed at the interface of the transformation of low entropic solar radiation to heat. The subsequent release of oxygen as a “waste” product of photosynthetic water cleavage led to the present-day aerobic atmosphere (Kasting and Siefert, 2002; Lane, 2002; Bekker et al., 2004), thus opening the road for a much more efficient exploitation of the Gibbs free energy through the aerobic respiration of heterotrophic organisms (for thermodynamic considerations, see (Nicholls and Ferguson, 2013; Renger, 1983).

From the very first moment this interaction with oxygen generated a new condition for the existing organisms starting an evolutionary adaptation process to this new oxydizing environment. Reactive oxygen species (ROS) became a powerful selector and generated a new hierarchy of life forms from the broad range of genetic mutations represented in the biosphere. We assume that this process accelerated the development of higher, mainly heterotrophic organisms in the sea and especially on the land mass remarkably.

The efficient generation of biomass and the highly selective impact of ROS lead to a broad range of options for complex organisms to be developed in the oxydizing environment. The direct, mostly deleterious impact of ROS on the biosphere is thereby just a minor facet in the broad spectrum of consequences. Important and more complex side effects are for example given by the fact that the molecular oxygen led to generation of the stratospheric ozone layer, which is the indispensable protective shield against deleterious UV-B radiation (Worrest and Caldwell, 1986). ROS led to new complex constraints for evolution that drove the biosphere into new directions – by direct oxidative pressure and by long-range effects due to environmental changes caused by the atmosphere and the biosphere themselves as energy source for all heterotrophic organisms.

For organisms that had developed before the transformation of the atmosphere the pathway of redox chemistry between water and O2 by oxygenic photosynthesis was harmful, due to the deleterious effects of ROS. O destroys the sensitive constituents (proteins, lipids) of living matter. As a consequence, the vast majority of these species was driven into extinction, while only a minority could survive by finding anaerobic ecological niches. All organisms developed suitable defense strategies, in particular the cyanobacteria, which were the first photosynthetic cells evolving oxygen (Zamaraev and Parmon, 1980).

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