Table Of ContentPhotosynthetic Nitrogen Assimilation and
Associated Carbon and Respiratory Metabolism
Advances in Photosynthesis and Respiration
VOLUME 12
Series Editor:
GOVINDJEE
University of Illinois, Urabna, Illinois, U.S.A.
Consulting Editors:
Christine FOYER, Harpenden, U.K.
Elisabeth GANTT, College Park, Maryland, U.S.A.
John H. GOLBECK, University Park, Pennsylvania, U.S.A.
Susan S. GOLDEN, College Station, Texas, U.S.A.
Wolfgang JUNGE, Osnabrück, Germany
Hartmut MICHEL, Frankfurt am Main, Germany
Kirmiyuki SATOH, Okayama, Japan
James Siedow, Durham, North Carolina, U.S.A.
The scope of our series, beginning with volume 11, reflects the concept that photosynthesis
and respiration are intertwined with respect to both the protein complexes involved and to the
entire bioenergetic machinery of all life. Advances in Photosynthesis and Respiration is a book
series that provides a comprehensive and state-of-the-art account of research in photo-
synthesis and respiration. Photosynthesis is the process by which higher plants, algae, and
certain species of bacteria transform and store solar energy in the form of energy-rich organic
molecules. These compounds are in turn used as the energy source for all growth and
reproduction in these and almost all other organisms. As such, virtually all life on the planet
ultimately depends on photosynthetic energy conversion. Respiration, which occurs in
mitochondrial and bacterial membranes, utilizes energy present in organic molecules to fuel a
wide range of metabolic reactions critical for cell growth and development. In addition, many
photosynthetic organisms engage in energetically wasteful photorespiration that begins in the
chloroplast with an oxygenation reaction catalyzed by the same enzyme responsible for
capturing carbon dioxide in photosynthesis. This series of books spans topics from physics to
agronomy and medicine, from femtosecond processes to season long production, from the
photophysics of reaction centers, through the electrochemistry of intermediate electron
transfer, to the physiology of whole orgamisms, and from X-ray christallography of proteins to
the morphology or organelles and intact organisms. The goal of the series is to offer beginning
researchers, advanced undergraduate students, graduate students, and even research
specialists, a comprehensive, up-to-date picture of the remarkable advances across the full
scope of research on photosynthesis, respiration and related processes.
Photosynthetic Nitrogen
Assimilation and
Associated Carbon and
Respiratory Metabolism
Edited by
Christine H. Foyer
Crop Performance and Improvement Division,
IACR-Rothamsted, Harpenden, U.K.
and
Graham Noctor
Université Denis Diderot Paris VII,
Institut de la Biotechnologie des Plantes, Orsay, France
KLUWER ACADEMIC PUBLISHERS
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Editorial
Advance in Photosynsthesis and Respiration
It gives me great pleasure to announce the publication (8) The Photochemistry of Carotenoids (H.A.
of Volume 12, Photosynthetic Nitrogen Assimilation Frank, A.J. Young, G. Britton and R.J. Cogdell,
and Associated Carbon and Respiratory Metabolism, editors, 1999);
edited by Christine H. Foyer and Graham Noctor in (9) Photosynthesis: Physiology and Metabolism
our Series. This volume is the second one to appear (R.C. Leegood, T.D. Sharkey and S. von
under the new title of Advances in Photosynthesis Caemmerer, editors, 2000);
and Respiration. Further, a new beginning has already (10) Photosynthesis: Photobiochemistry and Photo-
been made with the appointment of new members of biophysics (B. Ke, author, 2001);
the Board of Consulting Editors. They are: Christine (11) Regulation of Photosynthesis (E-M. Aro and
Foyer, UK; Elisabeth Gantt, USA; John H. Golbeck, B. Andersson, editors, 2001).
USA; Susan Golden, USA; Wolfgang Junge,
Germany; Hartmut Michel, Germany; and Kimiyuki
Satoh, Japan. James Siedow, USA, has joined our See http://www.wkap.n1/prod/s/AIPH for further
Board to provide leadership and strength in the area information and to order these books. Please note
of ‘respiration’ in this Series. Several volumes on that the members of the International Society of
respiration (both plant and bacterial) are already in Photosynthesis Research (ISPR) (http://www.photo-
production or being contracted. synthesisresearch.org/) receive special discounts.
Photosynthetic Nitrogen Assimilation and Asso-
Published Volumes ciated Carbon and Respiratory Metabolism, edited
by Christine H. Foyer and Graham Noctor, Volume
The present volume is a sequel to the following 12 in our series, is a great book that bridges the basics
eleven volumes in the “Advances in Photosynthesis of photosynthesis and respiration with ecology and
andRespiration” (AIPH) series. agriculture. Plant growth and biomass production
require the assimilation of nitrogen into organic
(1) Molecular Biology of Cyanobacteria (D.A. compounds using energy and carbon skeletons
Bryant, editor, 1994); produced by photosynthesis and respiration. Placing
(2) Anoxygenic Photosynthetic Bacteria (R.E. nitrogen assimilation firmly at the heart of
Blankenship, M.T. Madigan and C.E. Bauer, photosynthesis, this volume provides an original and
editors, 1995); innovative appraisal of the metabolic co-operation
(3) Biophysical Techniques in Photosynthesis (J. that is required. Unique perspectives are presented in
Amesz and A.J. Hoff, editors, 1996); sixteen key areas of current research, each discussing
(4) Oxygenic Photosynthesis: The Light Reactions the latest data and critically examining the most
(D.R. Ort and C.F. Yocum, editors, 1996); important developing concepts. Key themes are the
(5) Photosynthesis and the Environment (N.R. underlying cooperation between organelles (chloro-
Baker, editor, 1996); plasts and mitochondria) and pathways (photo-
(6) Lipids in Photosynthesis: Structure, Function synthesis and respiration), as well as the extensive
and Genetics (P.-A. Siegenthaler and N. metabolic crosstalk that dictates appropriate gene
Murata, editors, 1998); expression. This book is essential reading for those
(7) The Molecular Biology of Chloroplasts and seeking to understand the details of carbon-nitrogen
Mitochondria in Chlamydomonas (J.-D. interactions and the importance of these relationships
Rochaix, M. Goldschmidt-Clermont and S. in determining photosynthetic biomass production.
Merchant, editors, 1998);
v
Future Books tection; Photosystem I; Protonation and ATP
Synthesis; Global Aspects of Photosynthesis;
The readers of the current series are encouraged to Functional Genomics; History of Photosynthesis;
watch for the publication of the forthcoming books: The Cytochromes; The Chloroplast; Laboratory
Methods for Studying Leaves and Whole Plants. In
(1) Light-harvesting Antennas in Photosynthesis view of the interdisciplinary character of research in
(Editors: B.R. Green and W.W. Parson); photosynthesis and respiration, it is my earnest hope
(2) Photosynthesis in Algae (Editors: A.W.D. that this series of books will be used in educating
Larkum, S. Douglas, and J.A. Raven); students and researchers not only in Plant Sciences,
(3) Respiration in Archaea and Bacteria,2 volumes Molecular and Cell Biology, Integrated Biology,
(Editor: D. Zannoni); Biotechnology, Agricultural Sciences, Microbiology,
(4) Biochemistry and Biophysics of Chlorophylls Biochemistry, and Biophysics, but also in Bio-
(Editors: B. Grimm, R. Porra, W. Rüdiger, and engineering, Chemistry, and Physics.
H. Scheer).
(5) Chlorophyll Fluorescence (Editors: G. Papa- I take this opportunity to thank Christine Foyer
georgiou and Govindjee); and Graham Noctor; all the authors of volume 12;
(6) Photosystem II: The Water/Plastoquinone Larry Orr; Jacco Flipsen, Lanette Setkoski; and my
Oxido-reductase in Photosynthesis (Editors: wife Rajni Govindjee for their valuable help and
T. Wydrzynski and K. Satoh); support that made the publication of Photosynthetic
Nitrogen Assimilation and Associated Carbon and
In addition to these contracted books, invitations Respiratory Metabolism possible.
are out for several books. Topics planned are: Plant Readers are requested to send their suggestions
Respiration; Protein Complexes of Photosynthesis for future volumes, authors or editors to me by E-
and Respiration; Photoinhibition and Photopro- mail ([email protected]) or fax (1-217-244-7246).
Govindjee
Series Editor
Advances in Photosynthesis and Respiration
University of Illinois at Urbana-Champaign
Departments of Biochemistry and Plant Biology
And Center of Biophysics and Computational
Biology
265 Morrill Hall, 505 South Goodwin Avenue
Urbana, IL 61801-3707, USA
URL: http://www.life.uiuc.edu/govindjee
vi
Govindjee Photomorphogenesis (Narosa Publishers, New Delhi/
Kluwer Academic Publishers, Dordrecht, 1999), (2)
The Series Editor of Advances in Photosynthesis and Molecular Biology of Photosynthesis (Kluwer
Respiration, Govindjee, uses one name only. He has Academic Publishers, Dordrecht, 1988), and (3) Light
been Professor Emeritus of Biophysics, Biochemistry Emission by Plants and Bacteria (Academic Press,
and Plant Biology, at the University of Illinois at NY, 1986). Govindjee has edited (1) Photosynthesis
Urbana-Champaign (UIUC), since 1999. He was Vol. 1: Energy Conversion by Plants and Bacteria;
born in the city of Allahabad (Uttar Pradesh, India) and Photosynthesis Vol. 2: Development, Carbon
in 1932. Govindjee graduated from the University of Metabolism, and Plant Productivity (Academic Press,
Allahabad, India in 1952 with a B.Sc. degree in NY, 1982. Russian Version, 1987), and (2) Bioener-
Chemistry, Botany and Zoology, and obtained his getics of Photosynthesis (Academic Press, NY. 1975).
M.Sc. (also from the University of Allahabad) in In collaboration with others, Govindjee’s early
Botany (specializing in Plant Physiology) under research established the participation of a short-
Professor Shri Ranjan, in 1954. He subsequently wavelength form of chlorophyll a in Photosystem II
served as a lecturer in Botany, at the same university, (PS II), that the two-light effect of Robert Emerson
from 1954-1956. Govindjee came to the United was in photosynthesis, not in respiration, and that it
States of America in 1956, to pursue his doctoral could be studied through chlorophyll fluorescence
studies at UIUC. He worked, first with Robert and delayed fluorescence. Over the years, his research,
Emerson, then with Jan B. Thomas and Eugene again with many collaborators, has focused on the
Rabinowitch, and obtained his Ph.D. in 1960, in mechanisms of PS II, including the first studies on
Biophysics. After postdoctoral research on a US its primary charge separation; the specific role of
Public Health Service Award, he was appointed as bicarbonate on the acceptor side of PS II, the
Assistant Professor of Botany at UIUC in 1961; in demonstration that excess light indeed quenches the
1965, he became an Associate Professor, and then in lifetime of PS II chlorophyll fluorescence (and thus
1969, a Professor of Biophysics and Plant Biology, at diminishes the quantum yield of fluorescence); and
the same institution. on the theory for the mechanism of thermolumin-
Govindjee is co-author of Photosynthesis (John escence in plants. Currently, however, he focuses on
Wiley and Sons, New York, 1969), and co-editor of the history of photosynthesis research, and is equally
eight volumes on photosynthesis including (1) concerned with photosynthesis education (see http:/
Concepts in Photobiology: Photosynthesis and /www.life.uiuc.edu/govindjee).
vii
Contents
Editorial v
Contents viii
Preface xiii
Color Plates CP-1
1 Photosynthetic Nitrogen Assimilation: Inter-Pathway Control
and Signaling 1–22
Christine H. Foyer and Graham Noctor
Summary 1
I. Introduction 2
II. Control of Leaf Amino Acid Contents 4
III. Integration and Control of Nitrogen and Carbon Metabolism 11
IV. The Carbon-Nitrogen Signal Transduction Network: Interactions
Between Nitrate, Sugars and Abscisic Acid 16
V. Conclusions and Perspectives 18
References 19
2 Photosynthesis and Nitrogen-Use Efficiency 23–34
P. Ananda Kumar, Martin A. J. Parry, Rowan A. C. Mitchell,
Altaf Ahmad and Yash P. Abrol
Summary 23
I. Introduction 24
II. Nitrogen in the Photosynthetic Apparatus 24
III. Optimization of Amounts of Photosynthetic Components for
Different Environments 26
IV. Role of Regulation of Rubisco Activity 29
V. Approaches to Improving Nitrogen-Use Efficiency in Crops 30
Acknowledgments 31
References 31
3 Molecular Control of Nitrate Reductase and Other Enzymes
Involved in Nitrate Assimilation 35–48
Wilbur H. Campbell
Summary 35
I. Introduction 36
II. Transcriptional Control of Nitrate Reductase and Other Nitrogen
Metabolism Genes 39
III. Post-Translational Control of Nitrogen Metabolism Enzymes 41
viii
IV. Protein Kinases and Control of Carbon and Nitrogen Metabolism 44
V. Future Prospects for the Control of Nitrogen Metabolism 45
Acknowledgment 46
References 46
4 Soluble and Plasma Membrane-bound Enzymes Involved in
Nitrate and Nitrite Metabolism 49–62
Christian Meyer and Christine Stöhr
Summary 49
I. Introduction 50
II. Nitrate Reduction at the Plasma Membrane 50
III. Nitrite Transport and Reduction 54
IV. Conclusions 59
Acknowledgments 60
References 60
5 What Limits Nitrate Reduction in Leaves? 63–70
Werner M. Kaiser, Maria Stoimenova and Hui-Min Man
Summary 63
I. Introduction 64
II. Nitrate Reduction and Nitrate Reductase Activity in Photosynthesizing
Leaves 64
III. Nitrate Reduction after Artificial Activation of Nitrate Reductase 65
IV. Is Cytosolic Nitrate Concentration Rate-Limiting? 66
V. Is Nitrate Reduction Limited by NAD(P)H? 68
VI. Conclusions 68
Acknowledgments 70
References 70
6 The Biochemistry, Molecular Biology, and Genetic Manipulation
of Primary Ammonia Assimilation 71–92
Bertrand Hirel and Peter J. Lea
Summary 71
I. Introduction: Glutamine Synthetase and Glutamate Synthase, Two
Enzymes at the Crossroads Between Carbon and Nitrogen Metabolism 72
II. Glutamine Synthetase 72
III. Glutamate Synthase 79
IV. Glutamate Dehydrogenase 85
References 86
7 Regulation of Ammonium Assimilation in Cyanobacteria 93–113
Francisco J. Florencio and José C. Reyes
Summary 93
I. Introduction 94
II. Ammonium Uptake 94
III. The Glutamine Synthetase/Glutamate Synthase Pathway 96
ix
IV. Regulation of Ammonium Assimilation 103
V. Future Perspectives 109
Acknowledgments 109
References 109
8 Photorespiratory Carbon and Nitrogen Cycling: Evidence
from Studies of Mutant and Transgenic Plants 115–134
Alfred J. Keys and Richard C. Leegood
Summary 115
I. Introduction 116
II. Entry of Carbon into the Photorespiratory Pathway 119
III. Recycling of Carbon to the Reductive Pentose Phosphate Pathway 120
IV. Recycling of Nitrogen Associated with Photorespiration 124
V. Feedback from Photorespiration on Other Processes 127
VI. Role of Photorespiration During Stress 129
Conclusions 130
References 130
9 The Regulation of Plant Phosphoenolpyruvate Carboxylase
by Reversible Phosphorylation 135–150
Jean Vidal, Nadia Bakrim and Michael Hodges
Summary 135
I. Introduction 136
II. Properties of Phosphoenolpyruvate Carboxylase 136
III. The Enzyme‘s Physiological Context 137
IV. Reversible Modulation in vivo by a Regulatory Phosphorylation Cycle 139
V. Significance of Regulatory Phosphorylation of the Photosynthetic Isoform 144
VI. Regulatory Phosphorylation of the Form: Importance in Anaplerosis 145
VII. Conclusions and Perspectives 148
References 148
10 Mitochondrial Functions in the Light and Significance to
Carbon-Nitrogen Interactions 151–172
Per Gardeström, Abir U. Igamberdiev and A. S. Raghavendra
Summary 152
I. Introduction 152
II. Export of Photosynthate from the Chloroplast 153
III. Mitochondrial Products of Photorespiration 154
IV. Products of Glycolysis in the Light 155
V. Operation of the Tricarboxylic Acid Cycle 157
VI. Electron Transport and Redox Levels in Plant Mitochondria 160
VII. Participation of Mitochondria in the Regulation of Metabolism
during Transitions between Light and Darkness 163
VIII. Mitochondrial Respiration and Photoinhibition 164
IX. The Role of Mitochondria in Photosynthesis 165
x
