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Thirty Years of Photosynthesis G.J.Kelly • E.Latzko Grahame J.Kelly • Erwin Latzko Thirty Years of Photosynthesis 1974–2004 With 61 Figures and 2 Tables 1 23 Dr.Grahame J.Kelly Queensland University ofTechnology Faculty ofScience School ofLife Sciences GPO Box 2434 Brisbane Qld 4001 Australia Prof.Dr.Erwin Latzko Kirchbergstr.21 85402 Kranzberg Germany ISBN-10 3-540-28382-X Springer Berlin Heidelberg New York ISBN-13 978-3-540-28382-9 Springer Berlin Heidelberg New York This work is subject to copyright.All rights are reserved,whether the whole or part ofthe material is concerned, specifically the rights oftranslation,reprinting,reuse ofillustrations,recitation,broadcasting,reproduction on microfilm or in any other way,and storage in data banks.Duplication ofthis publication or parts thereofis permit- ted only under the provisions ofthe German Copyright Law ofSeptember 9,1965,in its current version,and per- missions for use must always be obtained from Springer-Verlag.Violations are liable for prosecution under the German Copyright Law. Springer is a part ofSpringer Science+Business Media springeronline.com © Springer-Verlag Berlin Heidelberg 2006 Printed in Germany The use ofgeneral descriptive names,registered names,trademarks,etc.in this publication does not imply,even in the absence ofa specific statement,that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Editor:Dr.Dieter Czeschlik,Heidelberg,Germany Desk editor:Ursula Gramm,Heidelberg,Germany Cover design:design & productionGmbH,Heidelberg,Germany Production:Friedmut Kröner,Heidelberg,Germany 31/3152 YK – 5 4 3 2 1 0 – Printed on acid free paper Foreword “The path ofcarbon in photosynthesis”for Progress in Botany: 50 years ofCalvin-Bensoncycle – 30 years ofKelly-Latzkoreviews While writing this Foreword and trying to focus my thoughts on the biochem- istry of photosynthesis, a handsome slim hardcover booklet of 104 pages bound in dark blue linen is in front ofme on my desk: “The Path ofCarbon in Photosynthesis” J.A.Basshamand M.Calvin,1957 I acquired it in the month ofmy oral Ph.D.-exams,April 1960,to get prepared with the Nobel-laureate’s text. In 2004 in his last swan-song review for Progress in Botany Grahame J. Kelly celebrated “The Calvin cycle’s golden jubilee”in an overview of50 years ofcarbon flowing for the progress in botany.He had met Erwin Latzkoin 1970 in another then foremost and now historic place of the biochemistry of photosynthesis,the laboratory of Martin Gibbs at Brandeis University, Massachusetts. Four years later Latzko and Kelly (1974) published their first joint review on photosynthetic carbon metabolism,starting offa long flow ofarticles on the flow ofcarbon in the series Progress in Botany. Most faithfully they produced regular accounts of the progress in Progress in Botany every second year, and when Erwin Latzkodecided to retire after the 1996 review Grahame Kelly carried on alone. Most ofthe reviews are headed by quotations and mottos alluding to both the author’s sympathetic sense ofhumour and their deep concern for the issue of photosynthesis harvesting the sun,and in this vein the quotation in the 1992 review (Kellyand Latzko,1992) best suits as a representative example: VI Foreword “The first man I saw was of a meagre aspect,with sooty hands and face, his hair and beard long, ragged and singed in several places. His clothes, shirt and skin were all of the same colour.He had been eight years upon a project for extracting sun- beams out ofcucumbers,which were to be put into vials hermetically sealed,and let out to warm the air in raw inclement summers.He told me,he did not doubt in eight years more, that he should be able to supply the Governor’s garden with sunshine at a reasonable rate …” Jonathan Swiftin Gulliver’s Travels,ca.1727. With the 2004 review Grahame Kellynow also decided to retire.He does it at the climax ofthe golden jubilee ofthe Calvincycle,and this now certainly ends an era ofphotosynthesis reviewing.Reviews in the future will have a dif- ferent touch,in as much as progress advances into the molecular realm:“The transformation ofa pig with a spinach genehas now been described”(Saeki et al.2004;see notes added in proof to the vol.64,2002-review in Progress in Botany,in this volume). Looking forward to this book presenting the 16 reviews of30 years ofphoto- synthesis in Progress in Botanyhas a historical twist as the book demon- strates the development ofthe field over the decades.Nevertheless,it is more than looking back.It presents the reader with an up-to-date account of the state ofthe field.Hence we owe thanks to Grahame Kellyand Springer-Ver- lag for presenting the entire collection ofthe 16 reviews in this volume.It will be stimulating reading for all interested in the biochemistry ofphotosynthe- sis.Great thanks are also due to Ursula Grammfor her continuous great care over very many years in general for Progress in Botanyat Springer Verlag in Heidelberg and particularly for her care for the present book. Grahame Kelly has meticulously re-read all the reviews again to develop updating comments from the perspective of2005.These are added at the ends ofthe individual reviews compiled in this volume.It is noteworthy that aston- ishingly little needed to be said which underlines the evergreen liveliness of each individual review. I wish this book about the path and metabolism ofcarbon in photosynthesis smooth paths and a metabolic generation of new approaches, ideas and insights in the community interested in the biochemistry ofphotosynthesis. Darmstadt,in August 2005 Ulrich Lüttge Foreword VII References Bassham JA,Calvin M (1957) The path ofcarbon in photosynthesis.Prentice Hall,Inc., Englewood Cliffs,N.J. Kelly GJ,Latzko E (1992) Photosynthesis:Carbon metabolism.Twenty years offollowing carbon cycles in photosynthetic cells.Progress Bot 54:174–200 Saeki et al. (2004) Functional expression of a D12 fatty acid desaturase gene from spinach in transgenic pigs.Proc Natl Acad Sci USA 101:6361–6366 Preface My interest in photosynthesis began, I suspect, at an early age. As a child brought up in the small Australian town of Kempsey,one of my enjoyments was to create a vegetable garden behind the family house,and sell produce to my parents at 50% ofthe prevailing market value.This involved weighing the produce,and I began to wonder how my garden plants could accumulate such weight. This curiosity, combined with an excessive fear of being asked to study the French language upon entering high school (perhaps I foresaw that it was to be Germany,not France,where I was to spend six years ofmy acade- mic life),dictated that I enter the “B”class which was free offoreign languages but included “agriculture”. I continued into “Agricultural Science” at the University of Sydney where,I can still recall,John F Turner attended to my childhood query by describing the famous willow-twig experiment of Van Helmont (who obviously asked similar questions as a child) and,more impor- tantly,by outlining the Benson-Calvin cycle of photosynthetic CO fixation. 2 The biochemistry of plant growth became my passion, and subsequently coaxed me into Turner’s laboratory in Sydney,followed by Martin Gibbs’lab- oratory in Waltham and Erwin Latzko’s laboratories in Weihenstephan and Münster. The above briefpersonal history is pertinent because this entire book is,in essence,an historical account.Erwin Latzko and I embarked on the produc- tion of this chronicle in 1974,although at the time we neither planned nor anticipated that it would continue uninterrupted for three decades.But it did, thus this resultant collection is unique: it offers the opportunity to read the 30-year history of a particular topic in photosynthetic carbon metabolism (e.g.the history ofRubisco,or the history ofchloroplast starch synthesis and degradation) written “as it took place”.Nothing was written in the context of later discoveries,because these were unknown at the time ofwriting! Readers can comfortably follow a topic by jumping from one review to the next,read- ing the appropriate section in each review as they proceed. An additional bonus is that,in our contortive efforts to make subsections ofphotosynthesis crystal-clear to all plant scientists,even anatomists and taxonomists,we re- X Preface drew many metabolic pathways (some old,some new) such that all inputs and outputs were balanced.Twenty-three of these are distributed through the 16 reviews.For example,in Figure 2 of the 1980 review one can clearly see the successful photosynthetic generation ofsucrose by a leafsimultaneously pho- torespiring 37% of its fixed CO ,a situation that is close to natural for most 2 plants.Textbooks always show pathways,but seldom attend to such metabolic accountancy. The collection ofreviews acquired,along the way,a multifaceted character. Examples include:(1) the often overlooked menagerie of marine microalgae that perform close to half of Earth’s CO fixation was given prominence in 2 1984 after I was introduced to these colourful photosynthesizers by Shirley Jeffrey of the CSIRO Marine Laboratories in Hobart; (2) recognition of the emerging link between photosynthesis research and sociopolitical issues was made in 1990 after my brief visit to “Die Grünen” in Bonn; and (3) the inevitable claim that new molecular biotechnologies might be put to use to boost photosynthesis and increase humanity’s food supply was critically questioned in 1994,1998 (with inspiration from a little of the philosophy of David Walker) and 2002. This history of photosynthetic carbon metabolism is not solely a produc- tion from Erwin Latzko and me.We recognise the thousands (literally) of curious researchers who have,over the years,slowly but surely untwined the intricacies ofthe biochemistry within the great variety ofphotosynthetic cells that exist in an equal variety ofsunlit niches on Earth.This book is the story of their work.Having been drafted by us,we are then grateful to the editors (Hubert Ziegler;Ulrich Lüttge) who have polished what we have written,and to the capable staff at Springer-Verlag, most recently Dieter Czeschlik and Ursula Gramm (who,by the way,makes delicious coffee) for ensuring that it became available as printed pages for the readers.Finally,we hail the eternal bright support ofour colleagues,friends and families over the years.As writer of this Preface,I particularly express my gratitude for the endurance of my long-time co-author Erwin Latzko and his delightful wife Sylvia,and for the patience ofmy beautiful wife Chusi and three charming daughters Madeleine (born in Freising during preparation of the 1978 review),Vivienne (born in Münster during preparation ofthe 1980 review),and Genevieve (born in Wol- longong during submission of the 1984 review). Their patience has been rewarded by Springer-Verlag’s decision to publish this unusual book which, we trust, will delight the minds of those 21st-century young scientists who become struck with a passion for contemplating the biochemistry of plant growth. Grahame J Kelly Contents Photosynthesis – Carbon Metabolism(1974) . . . . . . . . . . . . . . 1 E.Latzko andG.J.Kelly 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 2 Enzymology ofthe Reductive Pentose Phosphate Cycle . . . . . . 1 3 Studies with Isolated Chloroplasts . . . . . . . . . . . . . . . . . . 3 4 Communication between Chloroplast and Cytoplasm . . . . . . . 4 5 Glycollate and Phtorespiration . . . . . . . . . . . . . . . . . . . . 6 6 C Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 4 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Photosynthesis.Biochemical and Physiological Aspects ofCarbon Metabolism(1976) . . . . . . . . . . . . . . . . . . . . . . . 14 E.Latzko andG.J.Kelly 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 2 Enzymology ofthe Reductive Pentose Phosphate Cycle . . . . . . 14 3 Studies with Isolated Chloroplasts . . . . . . . . . . . . . . . . . . 18 4 Communication between Chloroplast and Cytoplasm . . . . . . . 20 5 Starch and Sucrose Metabolism . . . . . . . . . . . . . . . . . . . . 20 6 Photorespiration and Glycollate Metabolism . . . . . . . . . . . . 23 7 C Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25 4 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27 XII Contents Phtosynthesis.Control ofCarbon Metabolism Through Enzyme Regulation and Membrane-Mediated Metabolite Transport(1978) . . 33 E.Latzko andG.J.Kelly 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 2 The Reductive Pentose Phosphate Cycle (Calvin Cycle) . . . . . . 33 3 The Chloroplast . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 4 Products ofPhotosynthesis . . . . . . . . . . . . . . . . . . . . . . 39 5 Photorespiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42 6 C Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 4 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47 Photosynthesis.Carbon Metabolism:Chloroplast Capability and the Uncertain Fate ofCO (1980) . . . . . . . . . . . . . . . . . . . 53 2 E.Latzko andG.J.Kelly 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 2 Fixation ofCO by RuBP Carboxylase . . . . . . . . . . . . . . . . 53 2 3 Products ofCO Fixation:A Consideration 2 ofChloroplast Capability . . . . . . . . . . . . . . . . . . . . . . . 57 4 Release ofCO by Photorespiration . . . . . . . . . . . . . . . . . 61 2 5 Capture and Recapture ofCO by PEP Carboxylase . . . . . . . . 65 2 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68 Photosynthesis.Carbon Metabolism:The Profound Effects ofIllumination on the Metabolism ofPhotosynthetic Cells(1982) . . 75 G.J.Kelly andE.Latzko 1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75 2 Prologue:Advances in Methodology . . . . . . . . . . . . . . . . . 76 3 The Uptake ofInorganic Carbon by Photosynthetic Cells . . . . . 77 4 The Calvin Cycle:Enzymes and Their Regulation . . . . . . . . . . 78 5 On the Light-Mediated Control ofEnzyme Activities . . . . . . . . 81 6 Transport by the Chloroplast Envelope . . . . . . . . . . . . . . . 83 7 Products ofC0 Fixation . . . . . . . . . . . . . . . . . . . . . . . . 85 2 8 C Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88 4 9 Photorespiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97

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