Regulation of Chloroplast Biogenesis

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Volume 226-Regulation of Chloroplast Biogenesis edited by Joan H_ Argyroudi-Akoyunoglou

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Regulation of Chloroplast Biogenesis Edited by

Joan H. Argyroudi-Akoyunoglou Institute of Biology National Centre for Scientific Research "Demokritos" Athens, Greece

Springer Science+ Business Media, LLC

Proceedings of a NATD Advanced Research Workshop on Regulation of Chloroplast Biogenesis, held July 28-August 3,1991, in Crete, Greece

Llbrary of Congress Cataloglng-In-Publlcation Data

Regulation of chloroplast biogenesis I eOited by Joan H. Argyroudi -Akoyunoglou.

p. cm. -- (NATD ASI series. Series A, Life sciences ; v. 226)

"Proceedings of a NATD Advanced Research Workshop an Regulation of Chloroplast Biogenesis, held July 28-August 3, 1991, in Crete, Greece"--T.p. versa.

'Published in cooperat ion with NATD Scientific Affairs Division." Includes bibliographical references and index. ISBN 978-1-4613-6485-6 ISBN 978-1-4615-3366-5 (eBook) DOI 10.1007/978-1-4615-3366-5 1. Chloroplasts--For.ation--Regulation--~ongresses. 1. Argyroudi

-Akoyunoglou, J. H. II. NATD Advanced Research Warkshop on Regulation of Chloroplast Biogenesis (1991 , Crote, Greece) III. North Atlantic Treaty Organization. Scientific Affairs Division. IV. Series. OK725.R517 1992 581.87' 33--dc20 92-2952

ISBN 978-1-4613-6485-6

© 1992 Springer Science+Business Media New York Driginally published by Plenum Press, New York in 1992

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This book is dedicated to the memory of George Akoyunoglou

George Akoyunoglou 1927-1986

It is most appropriate to open this conference on "Regulation of Chloroplast Biogenesis" with words of remembrance and honour of our late colleague and my personal friend George Akoyunoglou.

without going into details, a few stepstones of the scientific career of George Akoyunoglou shall be mentioned . He obtained his ph.D. with a study on the carboxydismutase reactions under the guidance of Melvin calvin. He was called back to his home country to become Head of the Photobiology Laboratory and one of the pioneers of the Nuclear Research Center "Demokritos" in Athens. He acted as Head of the Biology Department for many years.

He has spent longer research visits in the laboratories of C. Siron­val in Liege, Bill siegelman in Brookhaven, Itzhak Ohad in Jerusalem and ours in Marburg. George ' s scientific work is marked by the fortunate and successful collaboration with his wife Joan. He represented the unique combination of a Biologist and a Biochemist.

During the 25 years of his scientific work George in collaboration with his wife Joan has set landmarks for the understanding of chloroplast biogenesis. During the transition of etioplasts to chloroplasts they investigated the chlorophyll synthesis, the formation of PS II and PS I and contributed significantly to the understanding of the development of the photosynthetic mechanism. They introduced the intermittent illumina­tion of developing plants for suppressing the formation of the light­harvesting chI alb complex, a technique used worldwide to study the relation between LHC and RC. They elaborated the technique of gel elec­trophoreses of pigment protein complexes and disclosed the sequential binding of chlorophylls to the various integral polypeptides of the thylakoid membrane. Always taking into consideration the biology of the plants they studied, George and Joan Akoyunoglou's work emphasizes the close correlation between the developmental stage of the plant from which the chloroplasts derived and the post-translational regulation of the chloroplast biogenesis.

But even to those who had no intimate knowledge of his scientific work, George Akoyunoglou is known as the outstanding organizer of several most memorable meetings. I mention the "International symposium on

VII

Chloroplast Development" at spetsai (1978), the "5th International Photosynthesis congress" at Halkidike (1980), the "symposium on the Autonomy and Biogenesis of Mitochondria and chloroplasts" at Delphi (1982) and the "International Meeting on the Regulation of chloroplast Differentiation" at Rhodos (1985). Those of us having had the privilege to participate in these meetings experienced George as the perfect organizer. He was everywhere where help was needed, but he never placed himself into the foreground. Perfect organization, the warm and friendly atmosphere and the combination of a program of highest scientific stan­dards with relaxing social events and inspiring cultural excursions became a trade mark of those meetings. During all these meetings George could count on the help of his family and we appreciated their cheerful help during the meetings. George, his family and his coworker Mr. Pastel­lacos appeared as an admirable entity during the past meetings.

As products of the meetings George has edited with various coeditors a number of valuable books. Among them the volumes of the proceedings of the 5th International Photosynthesis Congress still the most comprehen­sive work in photosynthesis literature.

George Akoyunoglou has served in many national and international committees. He took considerable part in the promotion of biology and biochemistry of his own country. He was a founding member of the Hellenic Biochemical and Biophysical society. Last but not least he inspired the foundation of the "International society of Chloroplast Development" for which he was elected as first chairman.

My first personal encounter with George Akoyunoglou was, when he was my chairman at the 3rd International Photosynthese congress in Rehovot (1974). Thereafter we met at various meetings and discussed our mutual research interest. Impressed by his scientific accomplishments and by his personality, I could persuade him to accept a one year guest professor­ship at our university. During this time we became friends. My co-workers and students could not only experience him as an inspiring, stimulating scientist and skillful experimentor but also as a cheerful and charming person who loved to exchange and laugh with them. But he could also be a serious and witty counterpart in long discussions about science, philos­ophy and Greek mythology.

I had the privilege to help George in organizing the last meeting in Rhodes. When most participants were gone, we sat in the lobby of the capsis Hotel and did the last accounting. After we finished, George said to me: Horst, that meeting was fun, let's do it again, and he already planned ahead for this meeting.

We have to be most thankful to George's wife Joan that she fulfilled the plan of George and took all the trouble of organizing this Interna­tional Meeting on the "Regulation of chloroplast Biogenesis".

We dedicate this meeting to the memory of George Akoyunoglou and I am sure it will be held in his sense to serve the scientific progress and friendship in good spirits.

viii

Horst senger president, International society for Chloroplast Development

PREFACE

From July 28 to August 3, 1991, an International Meeting on the REGULATION OF CHLOROPLAST BIOGENESIS was held at the capsis Beach Hotel in Aghia Pelaghia, on the island of crete, Greece. The Meeting (Advanced Research Workshop-Lecture Course) was co-sponsored by NATO, FEBS and IUB, and was held under the auspices of the International society for Chloro­plast Development, the Greek Ministry of Industry, Research and Technol­ogy, and the National Center for Scientific Research "Demokritos".

The Meeting focused on recent advances in the field of chloroplast biogenesis and the regulatory mechanisms underlined, and brought together over 120 experts and students of the field from 22 countries. The subject of chloroplast biogenesis has experienced great progress in recent years mainly thanks to the application of Molecular Biology techniques and methodology. New findings that emerge gradually unravel the regulatory mechanisms involved in the assembly, stabilization and growth of the photosynthetic units in thylakoids, the signal transduction chain leading from photoreception to gene expression, the transport of nuclear-coded proteins into stroma-soluble supramolecular enzyme complexes as well as thylakoid-bound supramolecular complexes, involved in light-energy transduction.

It was the aim of this meeting to bring together experts and students coming from diverse disciplines (ranging from Botany and plant physiology to Molecular Biology, Biophysics and Biotechnology), to discuss the recent advances in the field so that thorough exchange of ideas and working hypotheses would be achieved.

The current volume contains near to 90 papers given as lectures or poster presentations in the areas of:

I. Regulation of gene expression

II. Import of nuclear-coded proteins into chloroplasts and mecha­nisms of chloroplast protein translocation

III. Biosynthesis and origin of chloroplast pigments

IV. Regulation of pigment-protein complex formation and assembly into photosynthetic units

V. organization and interactions of photosynthetic units

VI. Adaptation mechanisms in plants and algae-shade adaptation-state transition

VII. Genetic manipulation as a means to monitor assembly and function

ix

I want to express my thanks to all who contributed to the Meeting and to this volume. My sincere thanks are also due to members of the Interna­tional Organizing committee, and especially to Prof. Dr. Horst senger, for their help, to my collaborators in "Demokritos", and especially to Mr. Leonidas Pastelakos and Ms Mitsy Akoyunoglou for their efficient and never expiring assistance.

August 1991 Athens, Greece

x

Joan Argyroudi-Akoyunoglou

CONTENTS

REGULATION OF GENE EXPRESSION

Structure and organization of Plastidal Genes and the Features of their Expression • • . . . . •

R. Hagemann

Chloroplast Gene Expression and Reverse Genetics in Chlamydomonas reinhardtii . . • . . .

J.D. Rochaix, M. Goldschmidt-clermont, Y. Choquet, Y. Takahashi, M. Kuchka, J. Girard-Bascou and P. Bennoun

Transcriptional and post-Transcriptional Determinants of Chloroplast Biogenesis .

J. Nickelsen, K. Tiller, C. Fiebig, A. Eisermann and G. Link

Regulation of Expression of the Pea Plastocyanin Gene J.C. Gray, K.-H. pwee, R.E. slatter and P. Dupree

Regulation of Genes Encoding Plastid Proteins during chloroplast Biogenesis in Euglena

D.E. Buetow, L.S.H. Yi and G. Erdos

cellular Differentiation Processes during Chloroplast Development in Euglena gracilis

st. Reinbothe

plastid Gene Expression during chloroplast Development by Two Alternative Pathways in Barley seedlings .

K. Krupinska, A. schmidt and J. Falk

cis-Regulatory Elements Responsible for the Tissue­specific Expression of the Wheat CAB-1 Gene

M. szell, M. Szekeres, E. Adam, E. Fejes and F. Nagy

Characterization of c-DNAs which Encode Enzymes Involved in chromoplast Differentiation and Carotenoid Biosynthesis in capsicum annuum

S. Romer, A. saint-Guily, F. Montrichard, M.L. Schantz, J.H. weil, R. schantz, M. Kuntz and B. Camara

1

· 9

· 17

· 23

· 31

• 43

· 51

57

63

xi

Photoreceptors and their Action on Chloroplast Development . . . .. 71 (Photoregulated Gene Expression)

G. Richter

Regulation of Gene Expression in Plastidogenesis by Light, Nitrate and Plastidic Factor • • • • • • • . • . • •

H. Mohr

Action spectrum of LHC-II Precursor Apoprotein Transcription

77

and coordinated Translation • • • • • . . • . • •• .... 85 K. Triantaphyllopoulos and J.H. Argyroudi-Akoyunoglou

Heat-Induced "photo" Morphogenesis in Dark-Grown plants and Circadian Rhythmicity - Is there a Connection? . • • •

K. Kloppstech, B. otto and J. Beator

Circadian control of Gene Expression and Morphogenesis by Heat shock in Barley . . • . . . . . .

J. Beator and K. Kloppstech

coordination in LHC-II mRNA Transcription, Translation and capacity for chlorophyll synthesis: circadian Rhythm

91

101

in all Processes • . • . . . . . . . . . . • . . . . . . . . . 107 T. A. Bei-paraskevopoulou and J.H. Argyroudi-Akoyunoglou

Induction of the Early Light-Inducible Protein Mature Pea plants during photo inhibition

(ELIP) in

I. Adamska, I. Ohad and K. Kloppstech

Regulation by phytochrome and oxygen Radicals of Ascorbate specific Peroxidase and Glutathione Reductase . . . .

H. Drumm-Herrel, B. Thomsen and H. Mohr

IMPORT OF NUCLEAR-CODED PROTEINS INTO CHLOROPLASTS AND MECHANISM OF CHLOROPLAST PROTEIN TRANSLOCATION

Chloroplast-specific Import and Routing of Proteins . . • • • P. weisbeek and D. de Boer

Targeting of Proteins into and across the chloroplastic Envelope . • . . . .. . ......•.

K. Keegstra, H.-m. Li, J. Marshall, J. ostrom and s. Perry

Import and processing of the Major Light-Harvesting Chlorophyll alb Binding Protein of PSII • . . . . . . . . . . .

G. Lamppa, M. Abad, s. Clark and J. Oblong

processing of the Light-Harvesting chlorophyll alb Protein II Precursor - possible Intermediate steps Examined by Using Truncated Precursors . . • . . • • . • • • • .

A. sommer, E. Ne'eman and E. Harel

Protein Targeting to the Thylakoid Lumen R.M. Mould and C. Robinson

BIOSYNTHESIS AND ORIGIN OF CHLOROPLAST PIGMENTS

pigments of the plastid Envelope Membranes J. Joyard, M.A. Block, B. Pineau and R. Douce

xii

113

119

125

135

143

151

159

165

New Aspects of the Intermediates, catalytic Components and the Regulation of the c5-pathway to chlorophyll ........ 175

D. Dornemann

Last steps in chlorophyll Biosynthesis: Esterification and Insertion into the Membrane • . • . • • . • • • • • • . • . • • 183

W. Rudiger

control of Carotenoid synthesis and Assembly of PS-II by Light in Mutant C-6D of scenedesmus • . • . ••... 191

K. Humbeck and s. Romer

Purification and characterization of two Glutamyl-tRNA Ligase Fractions from the unicellular Green Alga Scenedesmus obliguus Mutant C-2A' . • . . . . • . • • • . . . . 199

u. Vothknecht, D. Dornemann and H. Senger

The Photoreduction of protochlorophyll(ide) in scenedesmus and Barley (Hordeum vulgare) ••..••••••

R. Knaust, B. seyfried, K. Kotzabasis and H. senger

The Regulation of protochlorophyll synthesis and its

• •.•. 205

Physiological Role . .. . . . . . . • . . • • . • . . . . • . • 211 K. Kotzabasis, K. Humbeck and H. senger

Pigment-protein complexes of chlorophyll Precursors ....•.... 217 M. Ryberg, N. Artus, B. Boddi, A. Lindsten,

B. wiktorsson and c. Sundqvist

cross-linking of NADPH-protochlorophyllide oxidoreductase in Isolated Prolamellar Bodies . . . . • . • .

c. sundqvist, B. wiktorsson, Z. Lin Bang, B. Boddi and M. Ryberg

225

IEF of solubilized Active Protochlorophyllide Reductase . . . . . . . 231 B. wiktorsson, M. Ryberg and c. Sundqvist

Effect of Phosphonic Acid Esters on photoconversion of Protochlorophyllide in Barley Etioplasts . . . . . • . 235

F. Franck, o. Gornicka and K. strzalka

On the Formation of chlorophyllide after phototransformation of protochlorophyllide in 2-day Old Bean Leaves: comparison with Etiolated Leaves

B. Schoefs, M. Bertrand and F. Franck

chlorophyll Synthesis and Degradation in Germinating Barley seedlings . . . • . • . . . . . . . . . . . . . . . .

J. Walmsley and H. Adamson

susceptibility of Dark Chlorophyll Synthesis in Barley and Pine seedlings to Inhibition by Gabaculine

K.-L. ou, J. Walmsley and H. Adamson

Chlorophyll Biosynthesis: spectrofluorometric Estimation of protoporphyrin IX, Mg-protoporphyrin and Protochlorophyllide . . . . . • . . . . • .

P. Hukmani and B.C. Tripathy

. . • . 241

. . . 247

253

259

xiii

PHOTOSYNTHETIC UNIT ASSEMBLY AND ITS DYNAMIC REGULATION

In vitro synthesis of chlorophyll A Regulates Translation of chlorophyll A-Apoproteins in Barley Etioplasts

L.A. Eichacker

In vitro synthesis and Membrane Integration of the chloroplast

· 265

Encoded D-2 Protein of Photosystem II 271 A. Friemann, H.J. Schwarz and W. Hachtel

characterization of the Sequential Light-Regulated Assembly of photosystem I Core complex . 277

o. Lotan, Y. cohen, s. Yalovsky, D. Michaeli and R. Nechushtai

Biogenesis of Photosystem I: Subunit PsaE is Important for the stability of PS I complex 285

P.R. chitnis and N. Nelson

Assembly of the Photosystem I Multiprotein Complex and the oligomeric Form of the Major Light-Harvesting Chlorophyll alb Protein in Pea seedlings Grown in Flashed Light Followed by continuous Illumination . 291

J.T. Jaing, B.A. welty, D.T. Morishige and J.P. Thornber

PSII Inhibitor Binding, QB-Mediated Electron Flow and Rapid Degradation are Separable properties of the D1 Reaction Centre Protein . . . . .

M.A.K. Jansen, A.R.J. Driesenaar, H. Kless, S. Malkin, A.K. Mattoo and M. Edelman

Regulation of Photosynthetic unit Assembly: Regulation of Light-Harvesting Apoprotein Transcription, Translation and Stabilization in Thylakoids .

J. Argyroudi-Akoyunoglou, T. Bei-Paraskevopoulou, K. Triantaphyllopoulos and R. Anastassiou

Role of the Chloroplast Envelope in Thylakoid Biogenesis J.K. Hoober, D.B. Marks, J.L. Gabriel and L.G. Paavola

Thylakoid-bound Protease Activity as Monitored by Azo-Dye Release from Azocoll Substrate is Affected by Thylakoid Development and chlorophyll synthesis Inhibitors . . ....

R. Anastassiou and J.H. Argyroudi-Akoyunoglou

proteolytic Digestion of Apoproteins of Light-Harvesting Chlorophyll alb-protein Complexes in Barley Leaves

T. Honda, H. Ito, Y. Tanaka, A. Tanaka and H. Tsuji

Reconstitution of LHCp-pigment Complexes with Mutant LHCP and Chlorophyll Analogs

H. paulsen, S. Hobe and c. Eisen

Biogenesis of chloroplasts and Pigment-Protein Complexes in Barley Seedlings with Blocked Biosynthesis of

xiv

Carotenoids . . . . N.V. Karapetyan, M.G. Rakhimberdieva, Y.V. Bolychevtseva,

A.A. Moskalenko, N. YU. Kuznetsova and V.I. Popov

· 303

· 313

323

331

· 337

343

349

Development of proplastids and Accumulation of LHCP II Apoprotein in Golgi and Thylakoids of Dark-Grown Wax-Rich Cells of Euglena gracilis at Low Light Intensities Seen by Immunoelectron Microscopy

T. Osafune, S. Sumida, T. Ehara, J.A. schiff and E. Hase

Low-intensity Light-Induced Development of Thylakoids in proplastids of Dark-Grown wax-Rich cells of Euglena gracilis • . • . • • • • . • • .

T. Osafune, S. sumida and E. Hase

••.• 355

.. 361

ORGANIZATION AND INTERACTIONS OF PHOTOSYNTHETIC UNITS

Reconstitution of the photo system I Complex with Genetically Modified PsaC and PsaD Polypeptides Expressed in Escherichia coli

J.H. Golbeck

Organization of the photo system II Reaction center K. satoh

Extrinsic Polypeptides and the Inorganic cofactors of Photosystem II • • . . • • .

D.F. Ghanotakis, A. Bakou and K. Kavelaki

Glycine Betaine, sucrose, or Chloride Ions Protect Isolated photo system 2 Particles from Denaturation and Inactivation • . . . • . . . . • . • . . . . . . . . .

K. Kalosaka and G.C. Papageorgiou

Assembly of the Auxiliary chlorophyll alb Light-Harvesting Antenna of Photosystem-II in chloroplasts • . . • . .

M.A. Harrison, J.A. Nemson and A. Melis

Organization of the Photosystem II Antenna system of Maize plants Grown under Intermittent Light condition

J. Marquardt and R. Bassi

Structure of the Cyanobacterial photo system II:

367

• • • 375

383

391

• • . 397

405

An Indication of Different Functions of CP47 and CP43 • . • . . 411 J. Komenda, J. MasoJidek and E. ~etllkova

Glycolipids are Prosthetic Groups of polypeptides of the Reaction Center complex of Photosystem II

R. vo~, A. Radunz and G.H. schmid

The Fo and O-J-I-P Fluorescence Rise in Higher plants and Algae .••..•••.•.....•.•...

R.J. Strasser and Govindjee

characterization of the Oxygen Evolving complex of Prochlorothrix hollandica •...•.••

T.S. Mor, A.F. Post and I. Ohad

Prochlorothrix hollandica Is More Sensitive to Photoinhibition than chlamydomonas reinhardtii

T.S. Mor, A.F. Post and I. Ohad

.. 417

. •.. 423

427

433

XV

comparison of the 02-Evolving Complexes of oscillatoria chalybea with that of Different Greening stages of Higher plant chloroplasts: An Arnperometric and Mass Spectrometric study 439

K.P. Bader, F. Franck and G.H. schmid

The Effect of Temperature and Radical Protection on the photo­inhibition of spinach Thylakoids

A. wild, M. Richter and B. Bothin

The Effect of Heat Treatment on the Capacity of the Electron Transport: Interaction of Light and structural Organization . . . . .

K. Van Loven and R. valcke

Does a Heat-shock Treatment Affect photosynthesis in Nicotiana tabacum? . . . . .

R. valcke and K. Van Loven

Irnrnunogold-Localization of Tubulin-Like Protein in the Intra­skeletal structure of Pea chloroplasts

N. valkov and A.G. Ivanov

A Platelet Activating Factor-Like compound Isolated from Higher plants

C. Vakirtzi-Lemonias, v. Tsaoussis and J.H. Argyroudi­Akoyunoglou

ADAPTATION MECHANISMS IN PLANTS AND ALGAE

A Regulatory Feedback Mechanism for Light Acclimation of the Photosynthetic Apparatus: Are Photosystems II and I self-Regulatory Light Sensors?

J.M. Anderson and w.s. chow

Dynamic Light Acclimation of the Photosynthetic Apparatus of Higher plants

J.M. Anderson, w.s. Chow, H. Adamson and A. Melis

Modification of Chloroplast Development by Irradiance A. Melis

Regulation of the Photosynthetic Adaptation in scenedesmus obliguus Depending on Blue and Red Light .

D. Hermsmeier, E. Mala, R. Schulz, J. Thielmann, P. Galland and H. senger

Light-quality and Irradiance Level Interaction in control of Chloroplast Development .

K. Eskins

Reorganization of Thylakoid Membrane Lateral Heterogeneity Following state-I state II Transition

R. Bassi and P. Dainese

LHC II Kinase Activation during Greening Correlates with the Assembly of cytochrome b 6 /f Complex and Grana Formation .

Y. soroka, A. Gal and I. Ohad

xvi

· 445

. . 451

457

· 463

469

· 475

483

· 491

499

505

511

521

Phosphorylation of D1 and D2 Proteins of photosystem IIc Induces Heterogeneity of QB-site Activity .

M.T. Giardi, F. Rigoni, G.M. Giacometti and R. Barbato

Redox-Regulated Protein Phosphorylation and Photosystem II Function

T.D. Elich, M. Edelman and A.K. Mattoo

Thylakoid Protein Phosphorylation Leads to organization of the oligomeric Forms of pigment-protein Complexes in Pea Grana and stroma Lamellae

J. Georgakopoulos and J.H. Argyroudi-Akoyunoglou

Development of Shade-type Appearance - Light Intensity Adaptation-

527

533

539

and Regulation of the D1 Protein in synechococcus 545 F. Koenig

What Do We Know About the Biogenesis and the Development of Secondary Thylakoids (Grana Formation) in Higher plant systems?

J.A. De Greef

GENETIC MANIPULATION AS A MEANS TO MONITOR ASSEMBLY AND FUNCTION

site Directed Mutagenesis of a chloroplast Encoded Protein . E. Przibilla and R. Yamamoto

site Directed Mutagenesis to Probe the Role of the D2 Protein in Photosystem II. ....

B. Eggers and w. Vermaas

Photosystem I in the Nitrogen-Fixing cyanobacterium Anabaena variabilis ATCC 29413: Subunit composition and Directed Mutagenesis of cofactor Binding Proteins

H.B. pakrasi, K.J. Nyhus, R. Mannar Mannan and H.C.P.J. Matthijs

Towards Protein Engineering of Chlamydomonas reinhardtii chloroplast ATP synthase .

S. Leu, J. Schlesinger, R. Motzery, N. shavit and A. Michaels

Accelerated Rate of Turnover of the D1 subunit of Photosystem II is correlated with Inhibition of Electron Transfer from QA to QB in Cyanobacterial Mutants

N. Ohad, Y. Inoue and J. Hirschberg

Mutations in the QB-Binding Niche in the D1 subunit of Photosystem II Impair Electron Transport from QA to QB .

o. pra~il, N. Ohad and J. Hirschberg

Isolation and General characterization of chlorophyll Q Deficient Mutants and their Developmental Phenotypes from the Green Alga Scenedesmus obliguus

N.I. Bishop and s. Maggard

contributors

Index

551

561

. 567

575

583

. 589

597

603

611

613

xvii