Advances in Plant Biology Volume Series Editor John J Harada Davis, USA Advances in Plant Biology provides summaries and updates of topical areas of plant biology This series focuses largely on mechanisms that underlie the growth, development, and response of plants to their environment Each volume contains primarily on information at the molecular, cellular, biochemical, genetic and genomic level, although they will focused on information obtained using other approaches More information about this series at http://www.springer.com/series/8047 Steven M Theg • Francis-André Wollman Editors Plastid Biology 1 3 Editors Steven M Theg Department of Plant Biology Univeristy of California-Davis Davis California USA Francis-André Wollman Physiologie Membranaire et Moléculaire du Chloroplaste Institut de Biologie Physico-Chimique Paris France ISBN 978-1-4939-1135-6 ISBN 978-1-4939-1136-3 (eBook) DOI 10.1007/978-1-4939-1136-3 Springer New York Heidelberg Dordrecht London Library of Congress Control Number: 2014947238 © Springer Science+Business Media New York 2014 This work is subject to copyright All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher’s location, in its current version, and permission for use must always be obtained from Springer Permissions for use may be obtained through RightsLink at the Copyright Clearance Center Violations are liable to prosecution under the respective Copyright Law The use of general descriptive names, registered names, trademarks, service marks, etc in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made The publisher makes no warranty, express or implied, with respect to the material contained herein Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) Preface Photosynthesis is the process through which the energy inherent in sunlight is captured in the chemical bonds of reduced carbon compounds, thereby providing the food upon which almost all life depends In addition, the production of oxygen as a result of the utilization of water as the ultimate electron donor to the photosynthetic electron transport chain has transformed our atmosphere, allowing for the emergence of oxygenic respiration, without which there would be no human life on Earth Photosynthesis is carried out in plants and algae in chloroplasts Given their central role in energy transduction in the biosphere, chloroplasts have been the focus of attention for generations of scientists This volume brings together many aspects of modern research into plastids relating to their biogenesis, functioning in photosynthesis and utility for biotechnology Plastids had their origins in free living photosynthetic bacteria and took up residence in the primitive eukaryotic cells through endosymbiosis While they have lost most of their DNA to the nucleus, they retain a functioning genome and are capable of a limited but critical amount of semi-autonomous protein synthesis Accordingly, we start this volume with a series of three chapters devoted to the handling of the genetic information contained within the plastid genome and crosstalk between the chloroplast and nucleus as the information encoded in both locations is decoded Following this are five chapters that examine the biogenesis and differentiation of the plastid itself and the sub-structures found at the plastid surface and within the internal thylakoid system Also included here is a treatment of the unusual nonphotosynthetic plastids found within the Apicoplexa, a group of parasitic protists responsible for a number of important human diseases Despite having their own genomes, the vast majority of plastid proteins are synthesized in the cytosol and taken up into and subsequently distributed within the organelle The next six chapters of the volume describe these processes, as well as the roles of molecular chaperones and proteases in protein homeostasis This is followed by three chapters dedicated to critical aspects of chloroplast physiology relating to dissipation of excess light energy, control of electron transport and ion homeostasis Finally, the book ends with two chapters discussing the emerging roles of plastids in biotechnology, one as a platform for synthesis of useful proteins, made v vi Preface desirable because of the superior containment of transgenes within this organelle than when inserted in nuclear genomes, and the other as a source of hydrogen production to be used as biofuel Each of the chapters has been written by leading authorities in their respective research areas Many chapters are the result of collaborations between experts in different laboratories, giving a broader than usual perspective on a given topic In each case, readers will find well-crafted chapters containing information and insights for both novices and experts alike We are grateful to our many friends and scholars who contributed these outstanding chapters The breadth of their knowledge and clarity of their writing have made for a unique and readable volume bringing together many disparate but interconnected topics relating to plastid biology We are also indebted to those at Springer, especially Kenneth Teng and Brian Halm, who oversaw this project in its final stages of production Davis, CA, USA Paris, France Steven M Theg Francis-André Wollman Contents Part I Genetic Material and its Expression Chloroplast Gene Expression—RNA Synthesis and Processing���������� 3 1 Thomas Börner, Petya Zhelyazkova, Julia Legen and Christian Schmitz-Linneweber Chloroplast Gene Expression—Translation������������������������������������������ 49 2 Jörg Nickelsen, Alexandra-Viola Bohne and Peter Westhoff 3 The Chloroplast Genome and Nucleo-Cytosolic Crosstalk������������������ 79 Jean-David Rochaix and Silvia Ramundo Part II Plastid Differentiation An 4 Overview of Chloroplast Biogenesis and Development������������������ 115 Barry J Pogson and Veronica Albrecht-Borth 5 Dynamic Architecture of Plant Photosynthetic Membranes���������������� 129 Helmut Kirchhoff 6 Plastid Division����������������������������������������������������������������������������������������� 155 Jodi Maple-Grødem and Cécile Raynaud 7 Stromules�������������������������������������������������������������������������������������������������� 189 Amutha Sampath Kumar, Savithramma P Dinesh-Kumar and Jeffrey L. Caplan 8 The Apicoplast: A Parasite’s Symbiont�������������������������������������������������� 209 Lilach Sheiner and Boris Striepen vii viii Contents Part III Biogenesis of Chloroplast Proteins Mechanisms of Chloroplast Protein Import in Plants������������������������ 241 9 Paul Jarvis and Felix Kessler Protein Routing Processes in the Thylakoid���������������������������������������� 271 10 Carole Dabney-Smith and Amanda Storm 11 Protein Transport into Plastids of Secondarily Evolved Organisms�������������������������������������������������������������������������������� 291 Franziska Hempel, Kathrin Bolte, Andreas Klingl, Stefan Zauner and Uwe-G Maier Processing and Degradation of Chloroplast Extension Peptides������� 305 12 Kentaro Inoue and Elzbieta Glaser Molecular Chaperone Functions in Plastids���������������������������������������� 325 13 Raphael Trösch, Michael Schroda and Felix Willmund 14 Plastid Proteases������������������������������������������������������������������������������������� 359 Zach Adam and Wataru Sakamoto Part IV Chloroplast Photophysiology Photoprotective Mechanisms: Carotenoids����������������������������������������� 393 15 Luca Dall’Osto, Roberto Bassi and Alexander Ruban Regulation of Electron Transport in Photosynthesis�������������������������� 437 16 Giles N Johnson, Pierre Cardol, Jun Minagawa and Giovanni Finazzi Ion 17 homeostasis in the Chloroplast������������������������������������������������������ 465 Marc Hanikenne, Marík Bernal and Eugen-Ioan Urzica Part V Chloroplast Biotechnology Synthesis of Recombinant Products in the Chloroplast��������������������� 517 18 Ghislaine Tissot-Lecuelle, Saul Purton, Manuel Dubald and Michel Goldschmidt-Clermont Hydrogen and Biofuel Production in the Chloroplast������������������������ 559 19 Yonghua Li-Beisson, Gilles Peltier, Philipp Knörzer, Thomas Happe and Anja Hemschemeier Index . 587 Contributors Zach Adam The Robert H Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University, Rehovot, Israel Veronica Albrecht-Borth Australian National University, Canberra, Australia Roberto Bassi Dipartimento di Biotecnologie, Università di Verona, Verona, Italy María Bernal Plant Nutrition Department, Estación Experimental De Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), Zaragoza, Spain Department of Plant Physiology, Ruhr University Bochum, Bochum, Germany Alexandra-Viola Bohne Molekulare Pflanzenwissenschaften, Biozentrum LMU München, Planegg-Martinsried, Germany Kathrin Bolte Laboratory for Cell Biology, Philipps University of Marburg, Marburg, Germany Thomas Börner Institute of Biology, Humboldt University Berlin, Berlin, Germany Jeffrey L Caplan Department of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, DE, USA Pierre Cardol Laboratoire de Génétique des Microorganismes, Institut de Botanique, Université de Liège, Liège, Belgium Carole Dabney-Smith Department of Chemistry and Biochemistry, Miami University, Oxford, OH, USA Luca Dall’Osto Dipartimento di Biotecnologie, Università di Verona, Verona, Italy Savithramma P Dinesh-Kumar Department of Plant Biology and The Genome Center, College of Biological Sciences, University of California, Davis, CA, USA Manuel Dubald Bayer CropScience, Morrisville, NC, USA ix 574 Y Li-Beisson et al Fig 19.3 Pathways of fatty acid synthesis and lipid assembly as targets for genetic engineering studies The scheme of the subcellular organization of lipid metabolic pathways is based on that of plants, unless specific experimental evidence is provided for algal species Names of enzymes are in italic, and those enzymes described in this chapter are highlighted in red Lipid-X means that the exact substrate for this enzyme is unknown ACCase acetyl-CoA carboxylase, ACP acyl carrier protein, CoA coenzyme A, DAG diacylglycerol, DGAT diacylglycerol acyltransferase, FAS fatty acid synthase, ER endoplasmic reticulum, FAT fatty acyl-ACP thioesterase, G3P glycerol3-phosphate, GPAT glycerol-3-phosphate acyltransferase, LACS long chain acyl-CoA synthetase, LPA lysophosphatidic acid, LPAT lysophosphatidic acid acyltransferase, MLDP major lipid droplet protein, PA phosphatidic acid, PDAT phospholipid:diacylglycerol acyltransferase, PAP phosphatidic acid phosphatase, TAG triacylglycerol 19.4.4 Triacylglycerol Biosynthesis The best known TAG biosynthetic pathway involves the sequential acylation of sn-glycerol-3-phosphate (G3P) with three acyl-CoAs catalyzed by three distinct a cyltransferases (Fig. 19.3) It is initiated by G3P acyltransferase (GPAT) to produce lysophosphatidic acid (LPA), which is then further acylated by LPA acyltransferase (LPAT) to form phosphatidic acid (PA) Phosphatidic acid phosphatase (PAP) catalyzes the removal of the phosphate group from PA to generate sn-1,2-diacylglycerol (DAG), the central intermediate of all glycerolipids The last and committed step to oil synthesis is catalyzed by acyl-CoA:diacylglycerol acyltransferase (DGAT) This enzyme has been subjected to intensive studies, including overexpression, directed evolution and quantitative trait loci mapping [18, 139, 172] In Chlamydomonas, homology searches identified five type-2 DGATs (encoded by DGTT1–5) and one type-1 DGAT (DGAT1) DGTT1 exhibits increased transcript abundance in N-starvation conditions, and it has been demonstrated to be able to complement a yeast quadruple mutant deficient for i TAG synthesis [14] Engineering strategies nvolving overexpression of DGTT1 alone or in combination with other enzymes might be a possible way to increase oil content 19 Hydrogen and Biofuel Production in the Chloroplast 575 An alternative reaction important for oil synthesis is catalyzed by phos pholipid:diacylglycerol acyltransferase (PDAT) contributing to TAG synthesis using phosphatidylcholine as an acyl donor and sn-1,2-diacylglycerol as an acyl acceptor [28, 171] Contrary to all three acyltransferases described above, PDAT does not require acyl-CoA as donor Therefore, its reaction is often termed acyl-CoA independent pathway PDAT has been well characterized in both plants and yeast [28, 171] A homolog of this enzyme is present in Chlamydomonas and has lately been shown to be important for TAG accumulation as insertional null mutants ( pdat1–1 and pdat1–2) accumulate 25 % less TAG compared to the parent strain [14] This evidence for a trans-acylation pathway in TAG synthesis in Chlamydomonas was corroborated by the observation that cell lines carrying PDAT-directed amiRNA silencing constructs accumulate up to 30 % less TAG compared to the wild-type strain [168] However, as pdat mutants exhibit reduced, but not abolished TAG accumulation, DGTT1 must also contribute to oil synthesis [14] The same overlapping function of PDAT and DGAT has been demonstrated in the model plant Arabidopsis thaliana [171] in which minor reductions in oil content could be observed in either of the single mutants, whereas the double mutation is embryo-lethal As well as their acylation to glycerol, fatty acyl chains are modified by fatty acidmodifying enzymes including desaturases, epoxidases, elongases, and hydroxylases Desaturases catalyze the reduction of a C-C bond to form a C=C bond in an existing acyl chain [135] The number of double bonds in a fatty acid molecule plays a determinant role in its final utility For example, biodiesel containing a too high proportion of saturated fatty acids turns to gel even at ambient temperatures On the other hand, when too many unsaturated fatty acids are present, the biodiesel will have a good cold flow but will be prone to oxidation Desaturases have long been used as targets to engineer fatty acid compositions in higher plants [79, 95, 135] Four desaturases have been characterized in Chlamydomonas [23, 82, 128, 169] and many more have been identified based on sequence homology searches Molecular manipulation of these desaturases constitutes a promising way to engineer fatty acid composition in Chlamydomonas 19.4.5 Accumulation of Oil Bodies After a certain amount of TAGs has accumulated in specific domains of the ER or the plastid, oil bodies or lipid droplets bud off and form distinct subcellular organelles Oil bodies are spherical organelles consisting of a neutral lipid core enclosed by a membrane lipid monolayer coated with proteins [74] Oil body biogenesis and its associated proteins have been well studied in yeast [26, 27], as well as in plant oilseeds [73] Only recently, compositions of lipid body-associated proteins 200 proteins have been identified have been analyzed in Chlamydomonas and > 28 kDa is the most abundant of these and was thus [107, 113] One protein of ~ named major lipid droplet protein (MLDP) MLDP has been postulated to play a similar structural role as oleosin in oilseeds Besides MLDP, numerous metabolic a enzymes ( cyltransferases, lipases) or trafficking proteins are also present, indicating the dynamic nature of Chlamydomonas oil bodies The knowledge about oil 576 Y Li-Beisson et al body-associated proteins provided by these studies represents a rich source for the exploration of oil accumulation mechanisms in general, and also elucidates biotechnological targets For example, either N- or C- terminal fusion of a desired protein to MLDP could potentially direct it to oil bodies, as has been demonstrated for oleosins [10] One unique feature of Chlamydomonas oil bodies is that they are not only present in the ER (as is true for most organisms studied), but also in the plastid [40, 55] This has been shown by Transmission Electron Microscope (TEM) and is further supported by the strong enrichment in C16 fatty acids at the sn-2 position in both TAGs and chloroplast membrane lipids (but not in extra-plastidial lipids) This finding has implications for our overall understanding of the subcellular organization of glycerolipid metabolism and of the specificities of key lipid metabolic enzymes involved A plastid TAG synthesis pathway could provide additional advantages because engineering of lipid metabolic pathways could be achieved via a synthetic biology approach based on manipulation of the plastid genome Unlike the still-problematic transgene expression in the C reinhardtii nuclear genome [131], it is a well-established technique in the plastid genome and transgene expression can reach very high levels (over 70 % of total protein) [114] Transgenes can be delivered to the plastid genome via biolistic bombardment and they are integrated by homologous recombination [31, 105] Successful introduction of a 50 kb DNA fragment into the plastid genome of tobacco has been reported [1] This opened up the possibility of introducing several genes simultaneously in the plastid genome using a synthetic biology approach 19.4.6 Transcriptional Regulation of TAG Biosynthesis WRINKLED1 (WRI1), belonging to the APETALA2-ethylene responsive elementbinding protein (AP2-EREBP), family is the only transcription factor identified in regulation of fatty acid synthesis in Arabidopsis [7, 21] and maize [137] It has also been implicated in regulating oil synthesis in other species such as oil palm [13] Overexpression of WRI1 leads to a large increase in seed oil content in maize [137] and in tubers [69] No WRI1 homolog could be identified in the genome of Chlamydomonas, but comparative transcriptomic studies have led to identification of two regulatory proteins, NRR1–1 (nitrogen responsive regulator) [14] and an stressinduced lipid trigger [167] Overexpression or silencing of the genes encoding these proteins led to altered cellular oil content, but the exact mechanism and downstream target(s) of these proteins remain to be tested 19.5 Closing Remarks Plastids are the power house of all photosynthetic cells Photosynthesis converts the abundant energy of the sun into high-energy electrons and chemical energy equiva lents Accordingly, chloroplasts of microalgae are sources of valuable compounds 19 Hydrogen and Biofuel Production in the Chloroplast 577 such as molecular hydrogen, starch and lipids Recent studies of H2 and lipid m etabolic pathways in microalgal models have led to significant advances in our understanding of the molecular and biochemical mechanisms [66, 94, 104] Currently, the vast majority of studies on microalgal biofuel are focused on understanding and boosting the generation of H2 and the accumulation of TAGs [20, 66, 83, 84] In our view, generation of oil is only the first step toward the engineering of algal cell factories Production of value-added fatty acid-derived molecules such as alkanes, free fatty acids, wax esters and fatty alcohols will constitute the next major step At the moment, significant effort has been put on analyzing the H2 and lipid metabolism of the model microalga C reinhardtii However, the genomes of around ten microalgal species have been sequenced so far, and many more are currently being sequenced Intensive efforts are underway to develop molecular genetic tools for Chlamydomonas and other algae For example, the occurrence of homologous recombination in Nannochloropsis sp has been reported [85] This development, together with our knowledge gained through examining model systems, should aid in the master design of an ideal algal cell factory for the production of industrially desirable molecules References Adachi T, Takase H, Tomizawa KI (2007) Introduction of a 50 kbp DNA fragment into the plastid genome Biosci Biotechnol Biochem 71:2266–2273 Antal TK, Krendeleva TE, Laurinavichene TV, Makarova VV, Ghirardi ML, Rubin AB, Tsygankov AA, Seibert M (2003) The dependence of algal H2 production on Photosystem II and O2 consumption activities in sulfur-deprived Chlamydomonas reinhardtii cells Biochim Biophys Acta 1607:153–160 Antonkine ML et al (2007) Chemical rescue of a site-modified ligand to a [4Fe-4S] cluster in PsaC, a bacterial-like dicluster ferredoxin bound to Photosystem I Biochim Biophys Acta 1767:712–724 Arnon DI, Losada M, Nozaki M, Tagawa K (1961) Photoproduction of hydrogen, photofixation of nitrogen and a unified concept of photosynthesis Nature 190:601–606 Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria J Biol Chem 281:9909–9918 Atteia A, van Lis R, Tielens AG, Martin WF (2013) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes Biochim Biophys Acta 1827:210–223 Baud S, Santos-Mendoza M, To A, Harscoet E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis Plant J 50:825–838 Beer LL, Boyd ES, Peters JW, Posewitz MC (2009) Engineering algae for biohydrogen and biofuel production Curr Opin Biotechnol 20:264–271 Benemann JR, Berenson JA, Kaplan NO, Kamen MD (1973) Hydrogen evolution by a chloroplast-ferredoxin-hydrogenase system Proc Natl Acad Sci USA 70:2317–2320 10 Bhatla SC, Kaushik V, Yadav MK (2010) Use of oil bodies and oleosins in recombinant protein production and other biotechnological applications Biotechnol Adv 28:293–300 11 Blankenship RE et al (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement Science 332:805–809 12 Boudreau E, Nickelsen J, Lemaire SD, Ossenbuhl F, Rochaix JD (2000) The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability EMBO J 19:3366–3376 578 Y Li-Beisson et al 13 Bourgis F, Kilaru A, Cao X, Ngando-Ebongue GF, Drira N, Ohlrogge JB, Arondel V (2011) Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning Proc Natl Acad Sci U S A 108:12527–12532 14 Boyle NR et al (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas J Biol Chem 287:15811–15825 15 Browse J, McCourt P, Somerville C (1986) A mutant of Arabidopsis deficient in C18–3 and C16–3 leaf lipids Plant Physiol 81:859–864 16 Browse J, Warwick N, Somerville CR, Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid-synthesis in the 16–3 plant Arabidopsis-thaliana Biochem J 235:25–31 17 Bruska MK, Stiebritz MT, Reiher M (2011) Regioselectivity of H cluster oxidation J Am Chem Soc 133:20588–20603 18 Burgal J, Shockey J, Lu CF, Dyer J, Larson T, Graham I, Browse J (2008) Metabolic engineering of hydroxy fatty acid production in plants: RcDGAT2 drives dramatic increases in ricinoleate levels in seed oil Plant Biotechnol J 6:819–831 19 Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B (2005) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation J Mol Microbiol Biotechnol 10:181–196 20 Burgess SJ, Tamburic B, Zemichael F, Hellgardt K, Nixon PJ (2011) Solar-driven hydrogen production in green algae Adv Appl Microbiol 75:71–110 21 Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis Plant J 40:575–585 22 Chen HC, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii Photosynthesis Res 84:289–296 23 Chi XY, Zhang XW, Guan XY, Ding L, Li YX, Wang MQ, Lin HZ, Qin S (2008) Fatty acid biosynthesis in eukaryotic photosynthetic microalgae: identification of a microsomal delta 12 desaturase in Chlamydomonas reinhardtii J Microbiol 46:189–201 24 Chochois V, Dauvillee D, Beyly A, Tolleter D, Cuine S, Timpano H, Ball S, Cournac L, Peltier G (2009) Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism Plant Physiol 151:631–640 25 Cinco RM, MacInnis JM, Greenbaum E (1993) The role of carbon dioxide in light-activated hydrogen production by Chlamydomonas reinhardtii Photosynthesis Res 38:27–33 26 Coleman RA, Lee DP (2004) Enzymes of triacylglycerol synthesis and their regulation Prog Lipid Res 43:134–176 27 Czabany T, Wagner A, Zweytick D, Lohner K, Leitner E, Ingolic E, Daum G (2008) Structural and biochemical properties of lipid particles from the yeast Saccharomyces cerevisiae J Biol Chem 283:17065–17074 28 Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne H (2000) Phospholipid: diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants Proc Natl Acad Sci U S A 97:6487–6492 29 Dau H, Zaharieva I (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation Acc Chem Res 42:1861–1870 30 Davies JP, Yildiz FH, Grossman A (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation EMBO J 15:2150–2159 31 Day A, Goldschmidt-Clermont M (2011) The chloroplast transformation toolbox: selectable markers and marker removal Plant Biotechnol J 9:540–553 32 Dehesh K, Jones A, Knutzon DS, Voelker TA (1996) Production of high levels of 8:0 and 10:0 fatty acids in transgenic canola by overexpression of Ch FatB2, a thioesterase cDNA from Cuphea hookeriana Plant J 9:167–172 33 Delosme R, Olive J, Wollman F-A (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii Biochim Biophys Acta (BBA)-Bioenerg 1273:150–158 19 Hydrogen and Biofuel Production in the Chloroplast 579 34 Delrue F, Setier PA, Sahut C, Cournac L, Roubaud A, Peltier G, Froment AK (2012) An economic, sustainability, and energetic model of biodiesel production from microalgae Bioresour Technol 111:191–200 35 Desplats C, Mus F, Cuine S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts J Biol Chem 284:4148–4157 36 Doebbe A, Keck M, La Russa M, Mussgnug JH, Hankamer B, Tekce E, Niehaus K, Kruse O (2010) The interplay of proton, electron, and metabolite supply for photosynthetic H2 production in Chlamydomonas reinhardtii J Biol Chem 285:30247–30260 37 Dunahay TG, Jarvis EE, Dais SS, Roessler PG (1996) Manipulation of microalgal lipid production using genetic engineering Appl Biochem Biotechnol 57–58:223–231 38 Durrett TP, Benning C, Ohlrogge J (2008) Plant triacylglycerols as feedstocks for the production of biofuels Plant J 54:593–607 39 Falkowski PG (2006) Evolution Tracing oxygen’s imprint on earth’s metabolic evolution Science 311:1724–1725 40 Fan JL, Andre C, Xu CC (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii FEBS Lett 585:1985–1991 41 Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii Biochim Biophys Acta 1413:117–129 42 Florin L, Tsokoglou A, Happe T (2001) A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain J Biol Chem 276:6125–6132 43 Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases Chem Rev 107:4273–4303 44 Forestier M, King P, Zhang LP, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions Eur J Biochem 270:2750–2758 45 Fouchard S, Hemschemeier A, Caruana A, Pruvost K, Legrand J, Happe T, Peltier G, Cournac L (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells Appl Environ Microbiol 71:6199–6205 46 Gaffron H (1939) Reduction of carbon dioxide with molecular hydrogen in green algae Nature 143:204–205 47 Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae J Gen Physiol 26:219–240 48 Gfeller RP, Gibbs M (1984) Fermentative metabolism of Chlamydomonas reinhardtii: I Analysis of fermentative products from starch in dark and light Plant Physiol 75:212–218 49 Gfeller RP, Gibbs M (1985) Fermentative metabolism of Chlamydomonas reinhardtii: II Role of plastoquinone Plant Physiol 77:509–511 50 Ghirardi ML, Togasaki RK, Seibert M (1997) Oxygen sensitivity of algal H2-production Appl Biochem Biotechnol 63–65:141–151 51 Giannelli L, Scoma A, Torzillo G (2009) Interplay between light intensity, chlorophyll concentration and culture mixing on the hydrogen production in sulfur-deprived Chlamydomonas reinhardtii cultures grown in laboratory photobioreactors Biotechnol Bioeng 104:76–90 52 Giroud C, Eichenberger W (1988) Fatty acids of Chlamydomonas reinhardtii-structure, positional distribution and biosynthesis Biol Chem Hoppe Seyler 369:18–19 53 Giroud C, Gerber A, Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii-analysis of molecular species and intracellular sites(s) of biosynthesis Plant Cell Physiol 29:587–595 54 Goldet G, Brandmayr C, Stripp ST, Happe T, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009) Electrochemical kinetic investigations of the reactions of [FeFe]-hydrogenases with carbon monoxide and oxygen: comparing the importance of gas tunnels and active-site electronic/redox effects J Am Chem Soc 131:14979–14989 55 Goodson C, Roth R, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost Eukaryot Cell 10:1592–1606 580 Y Li-Beisson et al 56 Grimme RA, Lubner CE, Bryant DA, Golbeck JH (2008) Photosystem I/molecular wire/ metal nanoparticle bioconjugates for the photocatalytic production of H2 J Am Chem Soc 130:6308 57 Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment Protist 151:201–224 58 Grossman AR, Catalanotti C, Yang W, Dubini A, Magneschi L, Subramanian V, Posewitz MC, Seibert M (2011) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii New Phytol 190:279–288 59 Hackstein JH, Akhmanova A, Boxma B, Harhangi HR, Voncken FG (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments Trends Microbiol 7:441–447 60 Halliwell B (2006) Reactive species and antioxidants Redox biology is a fundamental theme of aerobic life Plant Physiol 141:312–322 61 Happe T, Kaminski A (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii Eur J Biochem 269:1022–1032 62 Happe T, Naber JD (1993) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii Eur J Biochem 214:475–481 63 Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii Eur J Biochem 222:769–774 64 Harwood JL, Guschina IA (2009) The versatility of algae and their lipid metabolism Biochimie 91:679–684 65 Hedges SB, Blair JE, Venturi ML, Shoe JL (2004) A molecular timescale of eukaryote evolution and the rise of complex multicellular life BMC Evol Biol 4:2 66 Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii Biochim Biophys Acta 1807:919–926 67 Hemschemeier A, Fouchard S, Cournac L, Peltier G, Happe T (2008) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks Planta 227:397–407 68 Hemschemeier A, Jacobs J, Happe T (2008) Biochemical and physiological characterization of the pyruvate formate-lyase Pfl1 of Chlamydomonas reinhardtii, a typically bacterial enzyme in a eukaryotic alga Eukaryot Cell 7:518–526 69 Hofvander P, Carlsson AS, A.S F (2011) Arabidopsis WRL1 induces a large increase of TAG accumulation in potato microtubers 5th European symposium on plant lipids: 88 70 Hong G, Pachter R (2012) Inhibition of biocatalysis in [Fe-Fe] hydrogenase by oxygen: molecular dynamics and density functional theory calculations ACS Chem Biol 7:1268–1275 71 Hoshino T, Johnson DJ, Cuello JL (2012) Design of new strategy for green algal photohydrogen production: spectral-selective photosystem I activation and photosystem II deactivation Bioresour Technol 120:233–240 72 Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances Plant J 54:621–639 73 Huang AHC (1992) Oil bodies and oleosins in seeds Annu Rev Plant Physiol Plant Mol Biol 43:177–200 74 Huang AHC (1994) Structure of plant seed oil bodies Curr Opin Struct Biol 4:493–498 75 Ihara M, Nakamoto H, Kamachi T, Okura I, Maeda M (2006) Photoinduced hydrogen production by direct electron transfer from photosystem I cross-linked with cytochrome c3 to [NiFe]-hydrogenase Photochem Photobiol 82:1677–1685 76 Ihara M et al (2006) Light-driven hydrogen production by a hybrid complex of a [NiFe]hydrogenase and the cyanobacterial photosystem I Photochem Photobiol 82:676–682 77 Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii FEBS Lett 583:325–329 78 Jans F et al (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas Proc Natl Acad Sci U S A 105:20546–20551 19 Hydrogen and Biofuel Production in the Chloroplast 581 79 Jaworski J, Cahoon EB (2003) Industrial oils from transgenic plants Curr Opin Plant Biol 6:178–184 80 Jensen PE, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller HV (2007) Structure, function and regulation of plant photosystem I Biochim Biophys Acta Bioenerg 1767:335–352 81 Kaczmarzyk D, Fulda M (2010) Fatty acid activation in cyanobacteria mediated by acyl-acyl carrier protein synthetase enables fatty acid recycling Plant Physiol 152:1598–1610 82 Kajikawa M, Yamato KT, Kohzu Y, Shoji S, Matsui K, Tanaka Y, Sakai Y, Fukuzawa H (2006) A front-end desaturase from Chlamydomonas reinhardtii produces pinolenic and coniferonic acids by omega13 desaturation in methylotrophic yeast and tobacco Plant Cell Physiol 47:64–73 83 Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification Biochimie 93:91–100 84 Khozin-Goldberg I, Iskandarov U, Cohen Z (2011) LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology Appl Microbiol Biotechnol 91:905–915 85 Kilian O, Benemann CSE, Niyogi KK, Vick B (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp Proc Natl Acad Sci U S A 108:21265–21269 86 Knaff DB (2004) Ferredoxin and ferredoxin-dependent enzymes oxygenic photosynthesis: the light reactions (Ort DR, Yocum CF, Heichel IF (eds)) Springer, Netherlands, pp 333–361 87 Krasnovsky AA, Van Ni C, Nikandrov VV, Brin GP (1980) Efficiency of hydrogen photoproduction by chloroplast-bacterial hydrogenase systems Plant Physiol 66:925–930 88 Kreuzberg K (1984) Starch fermentation via a formate producing pathway in Chlamydomonas reinhardii, Chlorogonium elongatum and Chlorella fusca Physiologia Plantarum 61:87–94 89 Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H2 production in engineered green algal cells J Biol Chem 280:34170–34177 90 Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxinencoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor Eukaryot Cell 9:1747–1754 91 Lambertz C, Leidel N, Havelius KG, Noth J, Chernev P, Winkler M, Happe T, Haumann M (2011) O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase J Biol Chem 286:40614–40623 92 Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol Metab Eng 12:387–391 93 Li-Beisson Y SB, Beisson F, Andersson M, Arondel V, Bates P, Baud S, Bird D, DeBono A, Durrett T, Franke R, Graham I, Katayama K, Kelly A, Larson T, Markham J, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid K, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2010) Acyl lipid metabolism in the Arabidopsis book Last R (ed) American Society of Plant Biologists Rockville, MD 94 Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself Curr Opin Biotechnol 24:300–309 95 Lu CF, Napier JA, Clemente TE, Cahoon EB (2011) New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications Curr Opin Biotechnol 22:252–259 96 Lubner CE, Knörzer P, Silva PJN, Vincent KA, Happe T, Bryant DA, Golbeck JH (2010) Wiring an [Fe-Fe]-hydrogenase with photosystem I for light-induced hydrogen production Biochemistry 49:10264–10266 97 Lubner CE, Applegate AM, Knörzer P, Ganago A, Bryant DA, Happe T, Golbeck JH (2011) Solar hydrogen-producing bionanodevice outperforms natural photosynthesis Proc Natl Acad Sci U S A 108:20988–20991 582 Y Li-Beisson et al 98 Madoka Y, Tomizawa KI, Mizoi J, Nishida I, Nagano Y, Sasaki Y (2002) Chloroplast transformation with modified accD operon increases acetyl-CoA carboxylase and causes extension of leaf longevity and increase in seed yield in tobacco Plant Cell Physiol 43:1518–1525 99 Matias PM, Soares CM, Saraiva LM, Coelho R, Morais J, Le Gall J, Carrondo MA (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 A and modelling studies of its interaction with the tetrahaem cytochrome c3 J Biol Inorg Chem 6:63–81 100 McTavish H (1998) Hydrogen evolution by direct electron transfer from photosystem I to hydrogenases J Biochem 123:644–649 101 Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii Plant Physiol 122:127–136 102 Merchant S, Sawaya MR (2005) The light reactions: a guide to recent acquisitions for the picture gallery Plant Cell 17:648–663 103 Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas Biochim Biophys Acta 1763:578–594 104 Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2012) TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation Curr Opin Biotechnol 23:352–363 105 Michelet L, Lefebvre-Legendre L, Burr SE, Rochaix JD, Goldschmidt-Clermont M (2011) Enhanced chloroplast transgene expression in a nuclear mutant of Chlamydomonas Plant Biotechnol J 9:565–574 106 Mignolet E, Lecler R, Ghysels B, Remacle C, Franck F (2012) Function of the chloroplastic NAD(P)H dehydrogenase Nda2 for H2 photoproduction in sulphur-deprived Chlamydomonas reinhardtii J Biotechnol 162:81–88 107 Moellering ER, Benning C (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii Eukaryot Cell 9:97–106 108 Mongrand S, Bessoule J-J, Cabantous F, Cassagne C (1998) The C16:3\C18:3 fatty acid balance in photosynthetic tissues from 468 plant species Phytochemistry 49:1049–1064 109 Moore TS, Du Z, Chen Z (2001) Membrane lipid biosynthesis in Chlamydomonas reinhardtii In vitro biosynthesis of diacylglyceryltrimethylhomoserine Plant Physiol 125:423–429 110 Morweiser M, Kruse O, Hankamer B, Posten C (2010) Developments and perspectives of photobioreactors for biofuel production Appl Microbiol Biotechnol 87:1291–1301 111 Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on nonphotochemical plastoquinone reduction and H2 photoproduction in Chlamydomonas reinhardtii Biochim Biophys Acta 1708:322–332 112 Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways J Biol Chem 282:25475–25486 113 Nguyen HM et al (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: With focus on proteins involved in lipid metabolism Proteomics 11:4266–4273 114 Oey M, Lohse M, Kreikemeyer B, Bock R (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic Plant J 57:436–445 115 Ohlrogge J, Pollard M, Bao X, Focke M, Girke T, Ruuska S, Mekhedov S, Benning C (2000) Fatty acid synthesis: from CO2 to functional genomics Biochem Soc Trans 28:567–574 116 Pape M, Lambertz C, Happe T, Hemschemeier A (2012) Differential expression of the Chlamydomonas [FeFe]-hydrogenase-encoding HYDA1 gene is regulated by the copper response regulator1 Plant Physiol 159:1700–1712 117 Philipps G, Krawietz D, Hemschemeier A, Happe T (2011) A pyruvate formate lyase-deficient Chlamydomonas reinhardtii strain provides evidence for a link between fermentation and hydrogen production in green algae Plant J 66:330–340 19 Hydrogen and Biofuel Production in the Chloroplast 583 118 Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii Planta 235:729–745 119 Radakovits R, Eduafo PM, Posewitz MC (2011) Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum Metab Eng 13:89–95 120 Rawsthorne S (2002) Carbon flux and fatty acid synthesis in plants Prog Lipid Res 41:182–196 121 Raymond J, Blankenship RE (2004) Biosynthetic pathways, gene replacement and the antiquity of life Geobiology 2:199–203 122 Raymond J, Segre D (2006) The effect of oxygen on biochemical networks and the evolution of complex life Science 311:1764–1767 123 Riekhof WR, Sears BB, Benning C (2005) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase B TA1Cr Eukaryot Cell 4:242–252 124 Roessler PG, Lien S (1984) Purification of hydrogenase from Chlamydomonas reinhardtii Plant Physiol 75:705–709 125 Roessler PG, Ohlrogge JB (1993) Cloning and characterization of the gene that encodes acetyl-coenzyme-A carboxylase in the alga Cyclotella cryptica J Biol Chem 268:19254–19259 126 Rühle T, Hemschemeier A, Melis A, Happe T (2008) A novel screening protocol for the isolation of hydrogen producing Chlamydomonas reinhardtii strains BMC Plant Biol 8:107 127 Ruuska SA, Girke T, Benning C, Ohlrogge JB (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling Plant Cell 14:1191–1206 128 Sato N, Fujiwara S, Kawaguchi A, Tsuzuki M (1997) Cloning of a gene for chloroplast omega6 desaturase of a green alga, Chlamydomonas reinhardtii J Biochem 122:1224–1232 129 Sawers RG (2005) Formate and its role in hydrogen production in Escherichia coli Biochem Soc Trans 33:42–46 130 Scharnewski M, Pongdontri P, Mora G, Hoppert M, Fulda M (2008) Mutants of Saccharomyces cerevisiae deficient in acyl-CoA synthetases secrete fatty acids due to interrupted fatty acid recycling FEBS J 275:2765–2778 131 Schroda M (2006) RNA silencing in Chlamydomonas: mechanisms and tools Curr Genet 49:69–84 132 Schwarze A, Kopczak MJ, Rogner M, Lenz O (2010) Requirements for construction of a functional hybrid complex of photosystem I and [NiFe]-hydrogenase Appl Environ Microbiol 76:2641–2651 133 Scoma A, Krawietz D, Faraloni C, Giannelli L, Happe T, Torzillo G (2012) Sustained H2 production in a Chlamydomonas reinhardtii D1 protein mutant J Biotechnol 157: 613–619 134 Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, Smith AG (2010) Biodiesel from algae: challenges and prospects Curr Opin Biotechnol 21:277–286 135 Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids Annu Rev Plant Physiol Plant Mol Biol 49:611–641 136 Sheehan J, Dunahay T, Benemann J, Roessler PG A look back at the US Department of Energy’s aquatic species program—biodiesel from algae, 1998, US Department of Energy’s Office of Fuels Development: Golden, CO: National Renewable Energy Laboratory 137 Shen B, Allen WB, Zheng PZ, Li CJ, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize Plant Physiol 153:980–987 138 Shima S, Thauer RK (2007) A third type of hydrogenase catalyzing H2 activation Chem Rec 7:37–46 139 Shockey JM, Gidda SK, Chapital DC, Kuan JC, Dhanoa PK, Bland JM, Rothstein SJ, M ullen RT, Dyer JM (2006) Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum Plant Cell 18:2294–2313 140 Siaut M et al (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves BMC Biotechnol 11:7 584 Y Li-Beisson et al 141 Skjånes K, Knutsen G, Källqvist T, Lindblad P (2008) H2 production from marine and freshwater species of green algae during sulfur deprivation and considerations for bioreactor design Int J Hydrogen Energy 33:511–521 142 Stiebritz MT, Reiher M (2012) Hydrogenases and oxygen Chem Sci 3:1739–1751 143 Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, Armstrong FA, Happe T (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms Proc Natl Acad Sci U S A 106:17331–17336 144 Stuart TS, Gaffron H (1972) The mechanism of hydrogen photoproduction by several algae Planta 106:101–112 145 Suorsa M, Sirpio S, Aro EM (2009) Towards characterization of the chloroplast NAD(P)H dehydrogenase complex Mol Plant 2:1127–1140 146 Surzycki R, Cournac L, Peltier G, Rochaix JD (2007) Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas Proc Natl Acad Sci U S A 104:17548–17553 147 Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics Mol Cell Proteomics 9:1514–1532 148 Terauchi AM et al (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii J Biol Chem 284:25867–25878 149 Thannickal VJ (2009) Oxygen in the evolution of complex life and the price we pay Am J Respir Cell Mol Biol 40:507–510 150 Timmins M, Thomas-Hall SR, Darling A, Zhang E, Hankamer B, Marx UC, Schenk PM (2009) Phylogenetic and molecular analysis of hydrogen-producing green algae J Exp Bot 60:1691–1702 151 Timmins M et al (2009) The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion J Biol Chem 284:35996 152 Tolleter D et al (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii Plant Cell 23:2619–2630 153 Vieler A, Wilhelm C, Goss R, Sub R, Schiller J (2007) The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF MS and TLC Chem Phys Lipids 150:143–155 154 Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview Chem Rev 107:4206–4272 155 Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases FEMS Microbiol Rev 25:455–501 156 Vincent KA, Parkin A, Lenz O, Albracht SP, Fontecilla-Camps JC, Cammack R, Friedrich B, Armstrong FA (2005) Electrochemical definitions of O2 sensitivity and oxidative inactivation in hydrogenases J Am Chem Soc 127: 18179–18189 157 Vincent KA, Parkin A, Armstrong FA (2007) Investigating and exploiting the electrocatalytic properties of hydrogenases Chem Rev 107:4366–4413 158 Voelker T, Worrell A, Anderson L, Bleibaum J, Fan C, Hawkins D, Radke S, Davies H (1992) Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants Science 257:72–74 159 Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii Eukaryot Cell 8:1856–1868 160 Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels Science 329:796–799 161 Winkler M, Heil B, Heil B, Happe T (2002) Isolation and molecular characterization of the [Fe]-hydrogenase from the unicellular green alga Chlorella fusca Biochim Biophys Acta 1576:330–334 162 Winkler M, Kuhlgert S, Hippler M, Happe T (2009) Characterization of the key step for light-driven hydrogen evolution in green algae J Biol Chem 284:36620–36627 163 Winkler M, Hemschemeier A, Jacobs J, Stripp S, Happe T (2010) Multiple ferredoxin isoforms in Chlamydomonas reinhardtii - their role under stress conditions and biotechnological implications Eur J Cell Biol 89:998–1004 19 Hydrogen and Biofuel Production in the Chloroplast 585 164 Winkler M, Kawelke S, Happe T (2011) Light driven hydrogen production in protein based semi-artificial systems Bioresour Technol 102:8493–8500 165 Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii Plant Physiol 117:129–139 166 Yacoby I, Pochekailov S, Toporik H, Ghirardi ML, King PW, Zhang S (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxin:NADP+-oxidoreductase (FNR) enzymes in vitro Proc Natl Acad Sci U S A 108:9396–9401 167 Yohn C MM, Behnke C, Brand A (2011) Stress-induced lipid trigger US Patent 168 Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii Plant Cell 24:3708–3724 169 Zauner S, Jochum W, Bigorowski T, Benning C (2012) A cytochrome b5-containing plastidlocated fatty acid desaturase from Chlamydomonas reinhardtii Eukaryot Cell 11:856–863 170 Zhang LP, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga) Planta 214:552–561 171 Zhang M, Fan J, Taylor DC, Ohlrogge JB (2009) DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development Plant Cell 21:3885–3901 172 Zheng P et al (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize Nat Genet 40:367–372 Index 3’ untranslated region (3’UTR), 532 5´ untranslated regions (5’UTRs), 532 5′ untranslated regions (5′UTRs), 52 A Abiotic stress responses, 197, 198 Actin, 196 Alzheimer’s disease (AD), 312 Aminoglycoside adenyl transferase (aadA), 52, 536, 537, 539, 543 Aminoglycoside phosphotransferase (aphA-6), 537, 539 Anion, 467, 486 Apicoplast, 211, 213–217, 219–221, 224–228, 295 B Biofuels, 450, 546, 560, 570 Biolistic transformation, 525 Biotic stress responses, 198, 199 C Carotenoids, 118, 122, 200, 228, 403, 405, 407, 415, 418, 488 xanthophyll cycle, 419–421 Cation, 250, 298, 467 Chaperones, 94, 102, 121, 124, 251, 253, 326, 327, 330, 340, 342, 344, 367 Chaperonin, 166, 330, 334 isoforms and complex compositions, 327–329 Chlamydomonas, 4, 7, 10, 15, 18, 28, 30, 102, 451–453, 456, 475, 480–483, 485 Chloramphenicol acetyl transferase (cat), 537 Chloroplast biogenesis, 8, 19, 25, 71, 102, 116–120, 123–125, 344, 368, 370, 476 Chloroplast editing, 24 Chloroplast envelope, 19, 93, 96, 124, 160, 168, 195, 245, 257, 276, 307, 476–479, 486, 493, 523 Chloroplast genome, 13, 24, 52, 54, 80, 120, 242, 250, 307, 535, 541 Chloroplast nucleases, 26 Chloroplast promoter, Chloroplast protein import, 242, 243, 245, 248, 249, 252, 253, 255, 259, 338, 345, 474 Chloroplast RNA, degradation, 29 polymerase, 19, 100 processing, 29 Chloroplast RNA-binding proteins, 4, 5, 23, 62 Chloroplast Sec, 257, 272, 274, 278 Chloroplast splicing, 15, 18, 19 Chloroplast SRP, 274 Chloroplast Tat (cp Tat), 278, 280 Chloroplast transcription, 5, 83, 84, 101, 125, 524 Chloroplast translation, 26, 27, 50–52, 58, 60, 62, 68, 95 regulatory principles of, 62, 64 spatial organization of, 70, 71 Chloroplast translational apparatus, constituents of, 54 Chromalveolates, 214, 456 Co-chaperone, 164, 166, 167, 252 Complex plastids, 218, 258, 293, 295, 298, 299 evolution of, 292 D Degradation, 4, 24, 26, 28, 92, 120, 122, 139, 141, 306, 314, 326, 360, 368, 376–378, 487 RNA cleavage and, 25 S.M Theg, F.-A Wollman (eds.), Plastid Biology, Advances in Plant Biology 5, DOI 10.1007/978-1-4939-1136-3, © Springer Science+Business Media New York 2014 587 588 Development, 7, 10, 12, 52, 95, 103, 117, 178, 202, 224, 311, 469, 484, 489 plastid, 338 Disaggregation, 331, 342–344 E Endosymbiosis, 54, 211, 219, 332 F Fatty Acid Synthase I (FASI), 223, 224 Filamenting temperature-sensitive mutant Z (FtsZ), 124, 157–159, 162, 163, 166, 172, 173, 175, 179 Fluorescent proteins, 195, 198, 201 Folding, 19, 121, 298, 329, 416 general protien, 334 Functional genomics, carotenoids, 415, 416 G Gene gun, 93 Grana thylakoid, 130–132, 135, 137, 139, 142, 143, 146 Green Fluorescent Protein (GFP), 310 H Heat shock proteins (HSPs), 198, 255, 309, 326 Helical repeat proteins, 62, 71 Heme, 92–94, 222, 487, 495 biosynthesis, 225, 226, 469 Herbicide tolerance, 537, 543 Heteroplasmic, 521, 531, 539 Homologous recombination, 520, 521, 543, 576 Homoplasmic, 521, 525, 537, 539 Human PreP homologue (hPreP), 312 Hydrogen, 482, 560 Hypoxia, 491 I Import, 118, 121, 125, 215, 247 stages of, 243 Inducible expression, 341, 535 Inter-organelle communication, 200 Isoprenoid precursors, 99 L Lipids, 118, 223, 415, 440, 570, 577 M Macromolecular crowding, 142–144, 146 Macronutrients, calcium, 474–476 chloride, 486, 487 Index magnesium, 469, 473, 474 nitrogen, 484–486 phosphorus, 479–481 potassium, 476–478 sodium, 478, 479 sulphur, 482, 483 Malaria, 210, 227, 541 Maternal inheritance, 520, 544 Metabolic engineering, 536, 542, 546 Metal, 226, 455, 467 Microalgae, 51, 440, 450, 451, 454, 455, 457, 545, 546, 563, 570, 576 Micronutrients, 467 copper, 490–493 iron, 487–490 manganese, 493 zinc, 494 Microtubule, 124 Min, 158, 159, 162, 179 Mineral nutrition, 179 Molecular chaperone, 165, 251, 326, 327, 335, 342, 378 N Neomycin phosphotransferase (nptII), 537 Non-photochemical quenching (NPQ), 397, 408, 442, 449 Nutrient starvation, 452 O Oral vaccines, 518 Organellar peptidasome, 310 P Photoinhibition, 336, 371, 374–376, 410, 421, 456, 488 Pitrilysin, 311 Plant development, 68, 166, 179, 251, 255, 311, 315, 337 Plastid, dividing rings, 168 Plastid biogenesis, 123, 124, 219 Plastid division ring, 156 Plastid(s), 4, 5, 8, 11, 56, 82 Plastome, 10, 12, 519, 521, 531, 539 target loci in, 531, 532 Polycistronic unit, 520, 531, 536, 542 PPR proteins, 20, 23, 24, 28, 62, 87, 120 Presequence Protease, PreP, 310 Promoter, NEP, 9–12 PEP, 7, Proteases, 139, 168, 312, 335, 342, 360, 361, 374, 376, 380 deg, 369 Protein arrays, 144, 145, 147 Index Protein import, 121, 167, 214, 217, 220, 250, 253, 310, 313, 365 in plastids, 337, 338 Protein routing in chloroplasts, 272, 274–280, 282–284 Protein synthesis, 50, 53, 56, 58, 59, 62, 70, 118, 211, 213, 257, 368, 482, 518 Protein targeting, 121, 257, 344 Protein translocation, 195, 219, 279, 293, 297 Protein transport, 217, 284, 292, 297, 313 non-canonical, 258, 259 R Redox control, 65, 97, 253, 441, 443 Regulatory processes, 62, 326, 441 Repressible chloroplast gene expression, in Chlamydomonas, 99–102 Retrograde signaling, 80, 91, 93, 95, 96, 99, 102, 103, 377, 469, 472 RNA polymerase, 4, 5, 7, 8, 10, 12, 82, 97, 520 S Secondary endosymbiosis, 214, 292, 293, 295 Selectable marker, 251, 531, 532, 537, 543 Senescence, 346, 372, 376 Shine-Dalgarno sequences, 56, 58, 533 Signaling, 80, 86, 178, 202, 472, 481, 484 Stress response, 98, 99 Stromule, 190–193, 197 589 Supramolecular level, 142, 148 Sustainable energy, 570 T Targeting sequences, 371, 521 Thylakoid membrane (TM), 9, 56, 57, 66, 70, 102, 121, 130–134 Thylakoid protein translocation \t See Chloroplast protein import, 122 Thylakoids, 70, 121, 133, 136, 141, 148, 254, 297, 313, 407, 418 TOC/TIC machinery, 298, 307 Toxoplasma, 210, 213, 217, 221, 224, 225, 228 Transcription, 4–6, 8–10 nuclear, 119, 120 Transformation, 519, 521, 525, 537, 539, 542 Translation factors, 57, 533, 534 Translocon, 121, 216, 219, 253, 259, 297, 298 Transport, 118, 121, 122, 130, 137, 198, 200, 202, 283 of metabolites, 228, 229 T-zones, 30, 66, 70 U Uniparental inheritance, 524, 544 V Virus, 191, 198 ... rps12 int.1, ycf3 int.1, clpP int.1 psbH petB int atpF int., trnK int., trnA int., trnI int., trnV int., rpl2 int., rps12 int.2 ycf3 int.2 rps12 int.1 trnG-UCC int psaA int1 and int2 Albino, pale... ycf3 int.2, clpP int1, petD, ndhA, ndhB pet Dint., trnG int., rps16 int., rpl16 int., ycf3 int.1, clpP int.1, rpoC1 int., ndhA int rps12 int.1; petB int., ndhB int., ndhA int., ycf3 int.1 trnL int.,... binding domains, including the CRM domain found in ribosome-assembly factors [16], the abundant RRM domain [ 257 ], the mTERF domain [92], and the organelle-specific PPR domain [19, 52 , 55 , 1 35] In