Lipids in plant and algae development

Subcellular Biochemistry 86 Yuki Nakamura Yonghua Li-Beisson Editors Lipids in Plant and Algae Development Tai Lieu Chat Luong Subcellular Biochemistry Volume 86 Series editor J Robin Harris University of Mainz, Mainz, Germany The book series SUBCELLULAR BIOCHEMISTRY is a renowned and well recognized forum for disseminating advances of emerging topics in Cell Biology and related subjects All volumes are edited by established scientists and the individual chapters are written by experts on the relevant topic The individual chapters of each volume are fully citable and indexed in Medline/Pubmed to ensure maximum visibility of the work Series Editor J Robin Harris, University of Mainz, Mainz, Germany International Advisory Editorial Board T Balla, National Institutes of Health, NICHD, Bethesda, USA R Bittman, Queens College, City University of New York, New York, USA Tapas K Kundu, JNCASR, Bangalore, India A Holzenburg, Texas A&M University, College Station, USA S Rottem, The Hebrew University, Jerusalem, Israel X Wang, Jiangnan University,Wuxi, China More information about this series at http://www.springer.com/series/6515 Yuki Nakamura • Yonghua Li-Beisson Editors Lipids in Plant and Algae Development Editors Yuki Nakamura Institute of Plant and Microbial Biology Academia Sinica Taipei, Taiwan Yonghua Li-Beisson Institut de Biologie Environnementale et Biotechnologie UMR 7265 CEA - CNRS - Université Aix Marseille, CEA Cadarache Saint-Paul-lez-Durance, France ISSN 0306-0225 Subcellular Biochemistry ISBN 978-3-319-25977-2 ISBN 978-3-319-25979-6 DOI 10.1007/978-3-319-25979-6 (eBook) Library of Congress Control Number: 2016930683 Springer Cham Heidelberg New York Dordrecht London © Springer International Publishing Switzerland 2016 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 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 The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made Printed on acid-free paper Springer International Publishing AG Switzerland is part of Springer Science+Business Media (www springer.com) Preface This book titled Lipids in Plant and Algae Development aims at summarizing recent advances in function of lipids in plant and algal development As a primary biomolecule, lipids have structural as well as diverse physiological functions such as essential constituents of biological membranes, sustainable carbon energy storage, and active signal transducer in cellular processes In the past few decades, plant and algal lipids have gone through an established biochemistry, enzymology, and analytical chemistry, which revealed distinct functions of specific lipid classes based on their physical and biochemical properties Upon entry into the postgenomic era, gene knockout studies on the lipid-related genes rapidly uncover functional aspects of lipids Owing to a pile of recent publications that discuss how lipids modulate critical biological processes in plants and algae, a new axis is being developed which classifies global lipidome on a physiological basis Our conceptual novelty in this book is to summarize our recent understanding of lipids from the viewpoint of developmental context Furthermore, we put together the discussion of algal and plant lipids so as to contrast the lipid function and underlying evolutionary context in photosynthetic unicellular and multicellular organisms The first chapter gives a general overview on lipids, including their structures, metabolism, and analytical tools The subsequent chapters can be grouped into three major parts: part I, lipids in photosynthesis (Chaps 2, 3, 4, 5, 6, and 7); part II, lipids in development and signaling (Chaps 8, 9, 10, 11, 12, 13, 14, 15, 16, and 17); and part III, lipids in industrial applications (Chaps 18, 19, and 20) The subjects of each chapter cover the fast-moving topics in the field of plant and algal lipids, inviting contribution by the internationally recognized expert groups, so that the book provides refreshing viewpoint in addition to the solid discussion by established authority Given the current fascination of plants and algae in carbon fixation and their potential as an alternative source for production of energies or novel chemical molecules, this book would also encompass what plants or algae can in the field of industrial applications This book would not have been published without valuable contributions by many of our friends and colleagues First of all, we are grateful to the authors of the individual chapters who kindly agreed to devote their time and effort to provide this v vi Preface book with the highest degree of expertise Thanks are also due to the scientists in the relevant research fields who have contributed tremendous original articles and form the intellectual basis of this book We thank Thijs van Vlijmen, Sara Germans, and other editorial staffs of Springer for their professional support to make the publication of this book possible Taipei, Taiwan Saint-Paul-lez-Durance, France 22 July 2015 Yuki Nakamura Yonghua Li-Beisson Contents Lipids: From Chemical Structures, Biosynthesis, and Analyses to Industrial Applications Yonghua Li-Beisson, Yuki Nakamura, and John Harwood Part I Lipids in Photosynthesis Roles of Lipids in Photosynthesis Koichi Kobayashi, Kaichiro Endo, and Hajime Wada 21 DGDG and Glycolipids in Plants and Algae Barbara Kalisch, Peter Dörmann, and Georg Hölzl 51 Thylakoid Development and Galactolipid Synthesis in Cyanobacteria Koichiro Awai 85 Role of Lipids in Chloroplast Biogenesis 103 Koichi Kobayashi and Hajime Wada Role of MGDG and Non-bilayer Lipid Phases in the Structure and Dynamics of Chloroplast Thylakoid Membranes 127 Győző Garab, Bettina Ughy, and Reimund Goss Chemical Genetics in Dissecting Membrane Glycerolipid Functions 159 Florian Chevalier, Laura Cuyàs Carrera, Laurent Nussaume, and Eric Maréchal Part II Lipids in Development and Signaling Triacylglycerol Accumulation in Photosynthetic Cells in Plants and Algae 179 Zhi-Yan Du and Christoph Benning vii viii Contents Cellular Organization of Triacylglycerol Biosynthesis in Microalgae 207 Changcheng Xu, Carl Andre, Jilian Fan, and John Shanklin 10 High-Throughput Genetics Strategies for Identifying New Components of Lipid Metabolism in the Green Alga Chlamydomonas reinhardtii 223 Xiaobo Li and Martin C Jonikas 11 Plant Sphingolipid Metabolism and Function 249 Kyle D Luttgeharm, Athen N Kimberlin, and Edgar B Cahoon 12 Plant Surface Lipids and Epidermis Development 287 Camille Delude, Steven Moussu, Jérôme Joubès, Gwyneth Ingram, and Frédéric Domergue 13 Role of Lipid Metabolism in Plant Pollen Exine Development 315 Dabing Zhang, Jianxin Shi, and Xijia Yang 14 Long-Distance Lipid Signaling and its Role in Plant Development and Stress Response 339 Allison M Barbaglia and Susanne Hoffmann-Benning 15 Acyl-CoA-Binding Proteins (ACBPs) in Plant Development 363 Shiu-Cheung Lung and Mee-Len Chye 16 The Rise and Fall of Jasmonate Biological Activities 405 Thierry Heitz, Ekaterina Smirnova, Emilie Widemann, Yann Aubert, Franck Pinot, and Rozenn Ménard 17 Green Leaf Volatiles in Plant Signaling and Response 427 Kenji Matsui and Takao Koeduka Part III Lipids in Industrial Application 18 Omics in Chlamydomonas for Biofuel Production 447 Hanna R Aucoin, Joseph Gardner, and Nanette R Boyle 19 Microalgae as a Source for VLC-PUFA Production 471 Inna Khozin-Goldberg, Stefan Leu, and Sammy Boussiba 20 Understanding Sugar Catabolism in Unicellular Cyanobacteria Toward the Application in Biofuel and Biomaterial Production 511 Takashi Osanai, Hiroko Iijima, and Masami Yokota Hirai Index 525 Chapter Lipids: From Chemical Structures, Biosynthesis, and Analyses to Industrial Applications Yonghua Li-Beisson, Yuki Nakamura, and John Harwood Abstract Lipids are one of the major subcellular components, and play numerous essential functions As well as their physiological roles, oils stored in biomass are useful commodities for a variety of biotechnological applications including food, chemical feedstocks, and fuel Due to their agronomic as well as economic and societal importance, lipids have historically been subjected to intensive studies Major current efforts are to increase the energy density of cell biomass, and/or create designer oils suitable for specific applications This chapter covers some basic aspects of what one needs to know about lipids: definition, structure, function, metabolism and focus is also given on the development of modern lipid analytical tools and major current engineering approaches for biotechnological applications This introductory chapter is intended to serve as a primer for all subsequent chapters in this book outlining current development in specific areas of lipids and their metabolism Keywords Fatty acids • Lipid biotechnology • Lipid metabolism • Lipid analysis • Algae • Plants Y Li-Beisson (*) Institut de Biologie Environnementale et Biotechnologie, UMR 7265 CEA - CNRS Université Aix Marseille, CEA Cadarache, Saint-Paul-lez-Durance 13108, France e-mail: yonghua.li@cea.fr Y Nakamura Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan e-mail: nakamura@gate.sinica.edu.tw J Harwood School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK e-mail: harwood@cardiff.ac.uk © Springer International Publishing Switzerland 2016 Y Nakamura, Y Li-Beisson (eds.), Lipids in Plant and Algae Development, Subcellular Biochemistry 86, DOI 10.1007/978-3-319-25979-6_1 518 T Osanai et al overexpression widely altered primary metabolism; particularly a decrease in sugar phosphates and an increase in several amino acids (Osanai et al 2014c) In Synechococcus, RpaA is a cognate response regulator of SasA (Takai et al 2006) The cognate response regulator of Hik8 in Synechocystis 6803 remains to be determined The Synechocystis 6803 genome contains a gene encoding the histidine kinase Hik31 (sll0790) in the chromosome, and the homolog of Hik31 (slr6041), which is 95.7 % identical to Hik31 (sll0790) at the amino acid level, is encoded by the plasmid in Synechocystis 6803 (Kahlon et al 2006) The hik31 knockout mutant could not grow under mixotrophic conditions (in the presence of mM glucose), and the G6PD activity was increased to more than twice that of the wild-type strain (Kahlon et al 2006) Importantly, the authors claimed the instability of phenotypes of the hik31 mutant (Kahlon et al 2006), a fact consistent with our transcriptome analysis; among all histidine kinases in Synechocystis 6803, only hik31 exhibited a large value of standard deviations (Osanai et al 2006) The deletion mutant of the plasmid operon of the hik31 ortholog (slr6039-slr6041) lost its viability under dark conditions, and the expression levels of glgP and zwf were decreased, the expression of glgC, fbaI, fbaII (encoding fructose-1,6-bisphosphate aldolases), gap2 (encoding glyceraldehyde-3-phosphate dehydrogenase), and pdh (encoding pyruvate dehydrogenase) were increased (Nagarajan et al 2014) Cell division and copper resistance were abolished by the deletion of the hik31 operon (Giner-Lamia et al 2012; Nagarajan et al 2012), suggesting that Hik31 plays multiple roles in primary and secondary metabolism and cell proliferation Hik31 is localized to both the plasma and thylakoid membranes (Giner-Lamia et al 2012) and Rre34/CopR, whose gene is included in the hik31 operon, is a probable cognate response regulator of Hik31 in Synechocystis 6803 Engineering of Sugar Catabolism in Synechocystis 6803 for Bioplastics and Hydrogen Production Metabolic engineering involves the alteration of cellular metabolisms by genetic modification to increase products of interest, and has a long history of studies Overexpressing and/or increasing the activities of metabolic enzymes are straightforward methods of metabolic engineering; however, researchers often encounter only marginal increases in productivity Since multiple genes should be modified simultaneously to alter metabolism and increase the products of interest, Alper and Stephanopoulos (2007) put forward global transcription machinery engineering (gTME), which alters transcription factors and sigma factors rather than metabolic enzymes As mentioned in section “Transcriptional regulators controlling sugar catabolism in Synechocystis 6803”, several transcriptional regulators that control the expression of genes of sugar catabolism have been identified in Synechocystis 6803, and therefore, our group tried to use these factors for metabolic engineering To generate the sigE-overexpressing strain, a sigE open reading frame was fused with 20 Understanding Sugar Catabolism in Unicellular Cyanobacteria Toward… 519 the psbAII promoter and integrated into a neutral site of the Synechocystis 6803 genome The sigE-overexpressing strain exhibited an increased expression of enzymes of glycogen catabolism and the OPP pathway, and decreased glycogen levels under photoautotrophic conditions (Osanai et al 2011) Metabolome analysis revealed that acetyl-CoA, citrate, and isocitrate levels were increased by sigEoverexpression, indicating enhanced sugar catabolism by sigE overexpression (Osanai et al 2011) Synechocystis 6803 accumulates PHB, one of the biodegradable polyesters grouped in polyhydroxyalkanoates (PHAs), during nitrogen starvation (Hein et al 1998) PHB is synthesized from acetyl-CoA by three reactions: acetoacetyl-CoA synthesized from acetyl-CoA by ketothiolase (encoded by phaA), 3-hydroxybutylyl-CoA synthesized from acetoacetyl-CoA by acetoacetyl-CoA reductase (encoded by phaB), and PHB synthesized from 3-hydroxybutylyl-CoA by PHA synthase (encoded by phaC and phaE) (Hein et al 1998) Microarray analysis suggested that the expression of phaC and phaE was up-regulated by sigE overexpression (Osanai et al 2011) The levels of PHB in the sigE-overexpressing strain after nitrogen deprivation were 2.5 times that in the wild-type strain (Osanai et al 2013b) Another microarray analysis indicated that the transcripts of phaA and phaB were increased by rre37 overexpression, and the PHB levels were doubled in the rre37-overexpresing strain compared with the wild-type strain (Osanai et al 2014a) PHB was additively increased by the double overexpression of sigE and rre37, suggesting that SigE and Rre37 activate the PHB biosynthetic pathway in parallel (Osanai et al 2014a) (Fig 20.3) Thus, overexpression of the transcriptional regulators increased the PHB levels in Synechocystis 6803, demonstrating that gTME is also an effective method for metabolic engineering in cyanobacteria Microarray analysis also suggested that the expression of hoxEFUYH was upregulated by sigE overexpression, which was confirmed by quantitative realtime PCR (Osanai et al 2011, 2013a) Hydrogen is accumulated during anaerobic Fig 20.3 Schematic model of activation of sugar catabolism and polyhydroxybutyrate biosynthesis by SigE and Rre37 (red arrows indicate the transcriptional activation by SigE and Rre37) 520 T Osanai et al conditions, and it was found that the levels of accumulated hydrogen were higher in the sigE-overexpressing strain than in the wild-type strain under both light and dark conditions (Osanai et al 2013a) Thus, SigE regulates the genes related to sugar catabolism, PHB biosynthesis, and hydrogen production As mentioned in section “Two transcription factors belonging to the AbrB-family”, AbrB transcription factors regulates the expression of enzymes related to primary metabolism and hydrogen production, suggesting the close relationship among carbon, nitrogen, and hydrogen metabolism in Synechocystis 6803, although its physiological meaning is unclear at present Conclusion In this review, we have summarized the recent progress of studies on the primary metabolism of unicellular cyanobacteria by focusing on Synechocystis 6803 sugar catabolism and transcriptional regulators Several transcriptional regulators of sugar metabolism in Synechocystis 6803 have been identified and molecular mechanisms of the signal transduction of light/dark, day/night, and nutrient status have been elucidated In addition to basic science, there are examples of which mutants of transcriptional regulators of sugar catabolism increased high-value products, opening up the novel strategy of the metabolic engineering of Synechocystis 6803 The advances in the applied sciences of cyanobacteria will contribute to generations of renewable energy and alternative materials, and the basic knowledge about cyanobacterial transcription and metabolism will be indispensable for the sustainable development of human society Acknowledgments This work was supported by the Ministry of Education, Culture, Sports, Science, and Technology, Japan; by a grant to T.O by funds from ALCA (Project name “Production of cyanobacterial succinate by the genetic engineering of transcriptional regulators and circadian clocks”) from the Japan Science and Technology Agency, and CREST from the Japan Science and Technology Agency The authors have no conflict of interest to declare References Allen MMM, Smith AJ (1969) Nitrogen chlorosis in blue-green algae Arch Microbiol 69:114–120 Alper H, Stephanopoulos G (2007) Global transcription machinery engineering: a new approach for improving cellular phenotype Metab Eng 9:258–267 Aquirre von Wobeser E, Ibelings BW et al (2011) Concerted changes in gene expression and cell physiology of the cyanobacterium Synechocystis sp strain PCC 6803 during transitions between nitrogen and light-limited growth Plant Physiol 155:1445–1457 Azuma M, Osanai T, Hirai MY et al (2011) A response regulator Rre37 and an RNA polymerase sigma factor SigE represent two parallel pathways to activate sugar catabolism in a cyanobacterium Synechocystis sp PCC 6803 Plant Cell Physiol 52:404–412 20 Understanding Sugar Catabolism in Unicellular Cyanobacteria Toward… 521 Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution J Exp Bot 54:609–622 Dutheil J, Saenkham P, Sakr S et al (2012) The AbrB2 autorepressor, expressed from an atypical promoter, represses the hydrogenase operon to regulate hydrogen production in Synechocystis strain PCC6803 J Bacteriol 194:5423–5433 Forchhammer K (2004) Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets FEMS Microbiol Rev 28:319–333 Garcia-Dominguez M, Reyes JC, Florencio FJ (1999) Glutamine synthetase inactivation by protein-protein interaction Proc Natl Acad Sci U S A 96:7161–7166 Giner-Lamia J, Lopez-Maury L, Reyes JC, Florencio FJ (2012) The CopRS two-component system is responsible for resistance to copper in the cyanobacterium Synechocystis sp PCC 6803 Plant Physiol 159:1806–1818 Goto-Seki A, Shirokane M, Masuda S et al (1999) Specificity crosstalk among group and group sigma factors in the cyanobacterium Synechococcus sp PCC7942: in vitro specificity and a phylogenetic analysis Mol Microbiol 34:473–484 Hein S, Tran H, Steinbuchel A (1998) Synechocystis sp PCC6803 possesses a two-component polyhydroxyalkanoic acid synthase similar to that of anoxygenic purple sulfur bacteria Arch Microbiol 170:162–170 Iijima H, Watanabe A, Takanobu J et al (2014) rre37 overexpression alters gene expression related to the tricarboxylic acid cycle and pyruvate metabolism in Synechocystis sp PCC 6803 Sci World J 2014, 921976 Ishii A, Hihara Y (2008) An AbrB-like transcriptional regulator, Sll0822, is essential for the activation of nitrogen-regulated genes in Synechocystis sp PCC 6803 Plant Physiol 148:660–670 Ishiura M, Kutsuna S, Aoki S et al (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria Science 281:1519–1523 Iwasaki H, Williams SB, Kitayama Y et al (2000) A kaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria Cell 101:223–233 Kahlon S, Beeri K, Ohkawa H et al (2006) A putative sensor kinase, Hik31, is involved in the response of Synechocystis sp strain PCC 6803 to the presence of glucose Microbiology 152:647–655 Klein W, Marahiel MA (2002) Structure-function relationship and regulation of two Bacillus subtilis DNA-binding proteins, HBsu and AbrB J Mol Microbiol Biotechnol 4:323–329 Kucho K, Okamoto K, Tsuchiya Y et al (2005) Global analysis of circadian expression in the cyanobacterium Synechocystis sp strain PCC 6803 J Bacteriol 187:2190–2199 Lieman-Hurwitz J, Haimovich M, Shalev-Malul G et al (2009) A cyanobacterial AbrB-like protein affects the apparent photosynthetic affinity for CO2 by modulating low-CO2-induced gene expression Environ Microbiol 11:927–936 Liu D, Yang C (2014) The nitrogen-regulated response regulator NrrA controls cyanophycin synthesis and glycogen catabolism in the cyanobacterium Synechocystis sp PCC 6803 J Biol Chem 289:2055–2071 Merida A, Candau P, Florencio FJ (1991) Regulation of glutamine synthetase activity in the unicellular cyanobacterium Synechocystis sp strain PCC 6803 by the nitrogen source: effect of ammonium J Bacteriol 173:4095–4100 Muro-Pastor AM, Herrero A, Flores E (2001a) Nitrogen-regulated group sigma factor from Synechocystis sp strain PCC 6803 involved in survival under nitrogen stress J Bacteriol 183:1090–1095 Muro-Pastor MI, Reyes JC, Florencio FJ (2001b) Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels J Biol Chem 276:38320–38328 Muro-Pastor MI, Reyes JC, Florencio FJ (2005) Ammonium assimilation in cyanobacteria Photosynth Res 83:135–150 Nagarajan S, Sherman DM, Shaw I, Sherman LA (2012) Functions of the duplicated hik31 operons in central metabolism and responses to light, dark, and carbon sources in Synechocystis sp strain PCC 6803 J Bacteriol 194:448–459 522 T Osanai et al Nagarajan S, Srivastava S, Sherman LA (2014) Essential role of the plasmid hik31 operon in regulating central metabolism in the dark in Synechocystis sp PCC 6803 Mol Microbiol 91:79–97 Nakajima T, Kajihata S, Yoshikawa K et al (2014) Integrated metabolic flux and omics analysis of Synechocystis sp PCC 6803 under mixotrophic and photoheterotrophic conditions Plant Cell Physiol 55:1605–1612 Nakaya Y, Iijima H, Takanobu J et al (2015) One day of nitrogen starvation reveals the effect of sigE and rre37 overexpression on the expression of genes related to carbon and nitrogen metabolism in Synechocystis sp PCC 6803 J Biosci Bioeng 120(2):128–1234 Oliveira P, Lindblad P (2008) An AbrB-like protein regulates the expression of the bidirectional hydrogenase in Synechocystis sp strain PCC 6803 J Bacteriol 190:1011–1019 Osanai T, Kanesaki Y, Nakano T et al (2005) Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp PCC 6803 by the group sigma factor SigE J Biol Chem 280:30653–30659 Osanai T, Imamura S, Asayama M et al (2006) Nitrogen induction of sugar catabolic gene expression in Synechocystis sp PCC 6803 DNA Res 13:185–195 Osanai T, Azuma M, Tanaka K (2007) Sugar catabolism regulated by light- and nitrogen-status in the cyanobacterium Synechocystis sp PCC 6803 Photochem Photobiol Sci 6:508–514 Osanai T, Imashimizu M, Seki A et al (2009) ChlH, the H subunit of the Mg-chelatase, is an antisigma factor for SigE in Synechocystis sp PCC 6803 Proc Natl Acad Sci U S A 106:6860–6865 Osanai T, Oikawa A, Azuma M et al (2011) Genetic engineering of group sigma factor SigE widely activates expressions of sugar catabolic genes in Synechocystis species PCC 6803 J Biol Chem 286:30962–30971 Osanai T, Kuwahara A, Iijima H et al (2013a) Pleiotropic effect of sigE over-expression on cell morphology, photosynthesis and hydrogen production in Synechocystis sp PCC 6803 Plant J 76:456–465 Osanai T, Numata K, Oikawa A et al (2013b) Increased bioplastics production with an RNA polymerase sigma factor SigE during nitrogen starvation in Synechocystis species PCC 6803 DNA Res 20:525–535 Osanai T, Oikawa A, Numata K et al (2014a) Pathway-level acceleration of glycogen catabolism by a response regulator in the cyanobacterium Synechocystis species PCC 6803 Plant Physiol 164:1831–1841 Osanai T, Oikawa A, Shirai T et al (2014b) Capillary electrophoresis-mass spectrometry reveals the distribution of carbon metabolites during nitrogen starvation in Synechocystis sp PCC 6803 Environ Microbiol 16:512–524 Osanai T, Shirai T, Iijima H et al (2014c) Alteration of cyanobacterial sugar and amino acid metabolism by overexpression hik8, encoding a KaiC-associated histidine kinase Environ Microbiol doi:10.1111/1462-2920.12715 Singh AK, Sherman LA (2005) Pleiotropic effect of a histidine kinase on carbohydrate metabolism in Synechocystis sp strain PCC 6803 and its requirement for heterotrophic growth J Bacteriol 187:2368–2376 Tabei Y, Okada K, Tsuzuki M (2007) Sll1330 controls the expression of glycolytic genes in Synechocystis sp PCC 6803 Biochem Biophys Res Commun 355:1045–1050 Takahashi H, Uchimiya H, Hihara Y (2008) Difference in metabolite levels between photoautotrophic and photomixotrophic cultures of Synechocystis sp PCC 6803 examined by capillary electrophoresis electrospray ionization mass spectrometry J Exp Bot 59:3009–3018 Takai N, Nakajima M, Oyama T et al (2006) A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria Proc Natl Acad Sci U S A 103:12109–12114 Tomita J, Nakajima M, Kondo T, Iwasaki H (2005) No transcription-translation feedback in circadian rhythm of KaiC phosphorylation Science 307:251–254 Yamauchi Y, Kaniya Y, Kaneko Y, Hihara Y (2011) Physiological roles of the cyAbrB transcriptional regulator pair Sll0822 and Sll0359 in Synechocystis sp strain PCC 6803 J Bacteriol 193:3702–3709 20 Understanding Sugar Catabolism in Unicellular Cyanobacteria Toward… 523 Yang C, Hua Q, Shimizu K (2002) Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose Metab Eng 4:202–216 Yoshikawa K, Hirasawa T, Ogawa T et al (2013) Integrated transcriptomic and metabolomic analysis of the central metabolism of Synechocystis sp PCC 6803 under different trophic conditions Biotechnol J 8:571–580 Index A Aborted microspore (AMS), 328 AbrB-family, 517 Abscisic acid (ABA), 342 Abscisic acid insensitive4 (ABI4), 182 Acetyl-CoA carboxylase (ACCase) subunits, 8, 9, 458 Acetyl-CoA synthetase (ACS), Acyl-CoA-binding proteins (ACBPs) AtACBPs (see AtACBP) in eukaryotes (see Eukaryotes) OsACBP6, peroxisomal fatty acid β-oxidation, 384–385 in seed oil biosynthesis, 377–384 in systemic transport, 392 Allene oxide synthase (AOS), 408 Annexin, 347 Applied Biosystems SOLiD Sequencing, 452 Arabidopsides, 412 Arabidopsis mgd1-1 mutant, 28 AtACBP in cuticle formation, 388–389 in embryo development, 387–388 in leaf senescence, 391 in pollen development, 389–390 seed germination and development, 385–386 AtMYB103, 329 AUGUSTUS, 452 Auxins, 342 Azelaic acid (AzA), 343 Azelaic acid induced (AZI1), 344 B Basic helix-loop-helix (bHLH) transcription factors, 321 Biomolecular fluorescence complementation (BiFC), 371 Blue native polyacrylamide gel electrophoresis (BN-PAGE) analysis, 31 Botrytis cinerea, 412 Bryonia, 410 C Calvin-Benson cycle, 457 Calvin cycle, 461 Chain termination method, 452 Chemical genetics advantages, 160 direct phosphate, 170 PTN, 171 screening strategies, 169–170 disadvantages, 161 reverse acyl profile, 166, 167 fatty acid biosynthesis, 162–164 galvestine-1, 166–168 gavestine-1 (Ki), 166 lyso-PA and PA, 164–166 phosphatidylcholine (PC), 168 piperidinyl-benzimidazolidinone scaffold, 168 screening strategies, 161–162 © Springer International Publishing Switzerland 2016 Y Nakamura, Y Li-Beisson (eds.), Lipids in Plant and Algae Development, Subcellular Biochemistry 86, DOI 10.1007/978-3-319-25979-6 525 526 Chlamydomonas classic hypothesis, 190 DCMU, 191 endogenous genes, 193 factors, 192 global transcript analysis, 192 insertional mutagenesis, 189 lipid droplet formation, 192 mechanism, 189 nitrogen deprivation, 189, 190 PDAT, 190 peripheral distribution, 191 PGD1, 190, 191 photosynthesis/flagella biogenesis, 189 reverse genetic screening, 189 SQD2 promoter, 193 SQUAMOSA promoter-binding-proteindomain, 193 TBARS, 191 Chlamydomonas reinhardtii biohydrogen production, 460 anoxic conditions, 461, 462 sulfur deplete conditions, 462–464 high energy carbon storage molecules C reinhardtii strains, 456 glycolysis/gluconeogenesis enzymes, 456 heat stress conditions, 460 lipid synthesis, 456 nitrogen metabolism, 456 nitrogen starvation, 455, 457 phosphorus and sulfur, 458, 459 photosynthetic activity, 457 protein synthesis, 456 TAG synthesis, 454, 457, 458 model organism knock out libraries, 450 nutrient stress, 451 Chl fluorescence analysis, 29 Chloroplast biogenesis galactolipid biosynthesis, 116–117 regulation of, 111–113 photosynthesis, 107–108 thylakoid lipid biogenesis, 106–107 thylakoid lipid biosynthesis, 117–118 thylakoid lipid synthesis alternative galactolipid pathway, 114 DLA2, 116 MGDG biosynthesis, 114 P deficiency, 116 pgp1-2 mutant, 114 photoprotection machinery, 113 photosynthesis-associated genes, 116 plastid nucleoids, 114 thylakoid membrane lipids, 108–110 Index Chloroplast galactolipids CrΔ4FAD, 483, 484 EhDES15 expression, 483 eukaryotic pathway, 481 extraplastidial membranes, 483 fatty-acid synthesis and modifications, 480 glycerolipid synthesis, 481 heterokonts and rhodophytes, 481 MGDG, 481 ω-3 desaturase, 483 Phaeodactylum tricornutum, 482 plastidial desaturation pathway, 482 prokaryotic pathway, 481 tertiary endosymbiosis, 482 Circium arvense, 412 Cis-jasmone (CJ), 412, 413 Cis-oxo-phytodienoic acid (OPDA), 410–412 Cold stress signaling, 276–277 Crystallography analysis, 33 CURVATURE THYLAKOID (CURT1), 89, 134 Cuticular waxes, 289 Cutin, 289 Cyanobacterial circadian clock, 517 CYP94 enzymes, 417, 418 Cyt b6/f, 26, 27 Cytochrome P450 family, 324 D Defective in cuticular ridges (DCR), 293 Defective in induced resistance (DIR1), 344, 347 Defective pollen wall (DPW), 323 Deficient in Cutin Ferulate (DCF), 293 Dehydroabietinal (DA), 343 Delayed tapetum degeneration (DTD), 328 Desorption electrospray ionization (DESI), 14 DGD1, 59 Diacylglycerol (DAG) acetyl-CoA carboxylase, 208 biosynthesis, 208 Chlamydomonas chloroplast lipid biosynthesis, 209 eukaryotic pathway, 209 fatty acid synthase, 208 origin of, 211–212 PA dephosphorylation reactions, 209 phospholipid, 209 prokaryotic pathway, 208 sequential G-3-P acylation, 209 synthesize extraplastidic membrane lipids, 209 Diacylglyceryl-trimethylhomoserine (DGTS), 52 527 Index 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), 191 Digalactosyldiacylglycerol (DGDG) cyanobacteria BN-PAGE analysis, 33 crystallography analysis, 33 in vitro PSII activity, 32 oxygen-evolving complex, 33 photodamage, 32 repair process, 32, 33 Synechocystis dgdA mutant, 33 in plants BN-PAGE analysis, 31 complementation analysis, 31 deficiency, 32 DGD1 and DGD2 genes, 30 dgd1 mutation, 31 fluorometric analysis, 31 in vitro protein analysis, 31 LHCII levels, 31 photoinhibition, 31 PSI, structure and function of, 31 thermostability, 32 transgenic expression, 30 Direct RNA sequencing, 452 DNA-binding with one finger (DOF) box, 374 E Embryo Cuticle Functionality (ECF) pathway, 304 Epidermal cells clonal analyses, 303 cuticle mutants fatty elongation complex, 295–298 knock-out mutations, 298 pleiotropic defects, 298–300 cuticular barrier ABC transporters and LTPs, 294 alcohol forming pathway, 291 alkane-forming pathway, 292 composition, 288 depolymerization reactions, 292 fatty acid elongase complex, 289–291 fluorescent fusion proteins, 293 lcr and att1 mutants, 293 dermatogen stage, 303 double gso1 gso2 mutant, 304 ECF pathway, 304, 306 epidermal specification pathway, 306 juxtaposed cuticles, 303 LACS2, FDH, and BDG1 pathway, 303 mathematical modeling, 306 molecular and cellular mechanisms, 304 molecular and genetic analysis, 306 non-cell autonomous component, 304 pavement cells, 288 in restricting plant growth, 288 syncytial endosperm, 303 transcriptional regulation, 300–302 Ethylene response factor (ERF), 371 Eukaryotes Arabidopsis amino acid determinants, 371 AtACBP2-AtEBP interaction, 371 detoxification, 372 differential subcellular localization and ligand specificities, 371 DOF box and GT-1 motif, 374 ERF, 371 GFP tagged proteins, 370 HAB1, regulation of, 373 hypoxia, heavy metal and oxidative stresses, 373 hypoxia-responsive gene expression, 372 in vitro binding, 372 Northern blot analysis, 372 RNA gel blot analysis, 374 sequence alignment, 370 six paralogs, 370 stress-responsiveness, 374 subcellular fractionation experiments, 370 transgenic expression, 374 combination techniques, 366 prototype form, 365 rice, 374–376 F Fatty acid methyl esters (FAMEs), 12 Fatty-acid desaturases (FAD), 479–480 Fatty acid synthase (FAS), Fish oil components, Flexible surface model (FSM), 146 FT signals, 347 Fucoxanthin chlorophyll protein (FCP) complexes, 136 G Galactolipid biosynthesis, 92–94 localization, 95 substrate specificity, 94–95 528 GAMYB, 329 Gas chromatography (GC), 12–13, 453 Gas chromatography-flame ionization detector (GC-FID) analysis, 230 Glucosylgalactosyldiacylglycerol (GlcGalDG), 30 Glutamate synthase (GOGAT), 514 Glycerol-3-phosphate-derivative, 343 Glycolipids algae, lipid composition, 52 Δ9-acyl-ACP desaturase, 53 in eukaryotic algae, 70 chlorophyta, 65–68 complex plastid, 64 glaucophyta, 65 Paulinella, 74 phosphate, 75 plastidial glycolipid metabolism, 65 primary endosymbiosis, 64 primary plastids, 64 rhodophyta, 69–70 secondary endosymbiosis, 65 (see also Secondary endosymbiosis) in plants 6-acyl-MGDG, 63 angiosperms, 54 DGDG synthases, 53, 54, 59 chloroplast development and morphology, 61 “18:3”-plants, 53 lipid composition, 52 lipid trafficking, 63–64 mgd1 mutant deficient, 61 MGDG synthase, 53, 54 MGD2/MGD3/DGD2 pathway, 62 oxylipins, 62 pgp1 mutant, 62 phosphate, 62 Picea abies, 54 Pinus sylvestris, 54 Pleurozium schreberi and Ceratodon purpureus (Bryophyta), 54 Polypodium vulgare/Pteridium aquilinum, 54 16\:3-plants, 53 Sphagnum fimbriatum, 54 sqd2 mutant, 61, 62 SQDG synthesis, 53, 54, 59 MGlcDG, 53 plastidial lipids (prokaryotic pathway), 53 prokaryotic/eukaryotic pathways, 53 Glycosylglycerides, Green fluorescence protein (GFP), 429 Green leaf volatiles (GLVs) Index biosynthesis ‘burst’ of GLV formation, 431 fatty acids, 429, 430 GUS activity, 430 heat stress, 431 HPL and AOS pathways, 429 gene evolution, 432, 433 sensing by plants Arabidopsis, 433, 434 on insect behavior, 433 interactions with membranes, 437, 438 metabolism, 438–440 perception as toxic xenobiotics, 435–437 physiological effects on mammals, 433 stressed plants, 433 volatiles, 434, 435 structure, in plants, 428 GS-GOGAT cycle, 514 H Henry’s law constants, 439 High-throughput genetics strategies chlamydomonas, 223–224 growth conditions, 226 mutation and mutant phenotype genetic complementation, 241 genetic linkage analysis, 240–241 locus, 240 multiple alleles, 240 primary screen flow cytometry, 229–230 fluorescent dye, 228 GC-FID analysis, 230 lipid bio-markers, 230 permeabilizing cells, 228–229 plate reader, 229–230 SCRS, 231 quantitative analysis and microscopy, 233 electron microscopy, 232 GC-FID, 232 insertional mutagenesis (see Insertional mutagenesis) mapped insertional mutant library, 238–240 MS, 232 point mutations, 233 TAG metabolism, 225–226 Histidine kinases (Hik8 and Hik31), 517, 518 Hydrophobic/amphipathic small molecules, Hydroxylated fatty acids, 324 Hypersensitive response (HR), 276 Hypersensitive to ABA1 (HAB1), 373 Index I Insertional mutagenesis Agrobacterium tumefaciens, 235 antibiotic resistance markers, 234 auxotrophy markers, 234 biolistic particle delivery, 235 drug-selectable markers, 234 electroporation, 235 glass beads, 235 insertion site, 237 number of insertions per mutant, 235 plasmid rescue/PCR-based methods, 235–237 promoter, 234 Isocitrate lyase (ICL), 461 In vitro protein analysis, 31 J JA-amino acid conjugates, 414 Jasmonate metabolic grid, 419, 420 Jasmonic acid (JA) anti-cancer properties of, 415 arabidopsides, 412 biosynthesis, 408 biosynthetic pathways/biological activities, 409, 410 cis-jasmone, 412, 413 diversity, structures and biological activities, 407 glucosylated/sulfated derivatives, 414 herbivores attacks, 406 jasmonoyl-isoleucine catabolism, 414, 415 amido-hydrolases, 418 CYP94 enzymes, 417, 418 Jasmonate metabolic grid, 419, 420 JA-triggered plant immunity, 406 and methyl jasmonate (MJ), 413 OPDA, 410, 411 in reproduction, 406 signaling pathway, 409 tuberonic acid, 414 unifying signaling model, 406 Jasmonoyl-isoleucine (JA-Ile), 414, 415 K 3-ketosphinganine reductase (KSR), 260–261 L Leaf closing factor (LCF), 414 LEAFY COTYLEDON1 (LEC1), 182 529 Light-harvesting complex of photosystem II (LHCII), 27 Lipid biosynthesis, transcriptional regulation, 300–302 Lipids algae and higher plants compositions, 6–7 structure of, 3–5 analyses GC, 12, 13 lipidomics, 13 MSI, 14 TLC, 11 biosynthesis carbon source and two-carbon, 8–9 cellular functions, 9–10 glycerolipid assembly, biotechnological applications, 14, 15 classes of, definition, membrane structures, signaling molecules, storage lipids, surface coverings, Lipid signaling conductive system, 340 lipophilic compounds JA, 344–345 oxylipins, 344–345 phosphatidyl inositol and phosphates, 349–351 (phospho-)glycerolipids, 345–348 phospholipases, 349 plant hormones, 342 PtdOH, 351–353 SAR, 342–344 small lipophilic metabolites, 342–344 in long-distance signaling, 340 pressure flow hypothesis, 340 signaling compounds, 340 Lipid transfer protein (LTP), 347 Long-chain bases (LCB) biosynthesis KSR, 260 serine palmitoyltransferase complex, 252–259 ceramides phosphorylation/ dephosphorylation, 269 modifications C-4 hydroxylation, 261 Δ4 desaturation, 262 Δ8 unsaturation, 261 hydroxylation and desaturation, 262–263 530 Long-distance developmental signals, 346 Lyso-phosphatidic (lyso-PA), 164–166 M Major lipid droplet protein (MLDP), 230, 457 MALE STERILITY (MS1), 327 MALE STERILITY2 (MS2), 323 Mass spectrometry imaging (MSI), 14 Mass spectroscopy (MS), 232 Matrix-assisted laser desorption/ionization (MALDI), 14, 453 Maxam-Gilbert sequencing, 452 Metabolomics, 453 Methyl jasmonate (MJ), 413 Microalgae active growth recovery, 492 ALA, 484 C16 PUFA and C20 PUFA, 493 cellular localization and compartmentalization betaine lipids, 490 chloroplast lipids, 489 cytoplasm, 489 EPA-CoA, 491 genomic survey, 488 L incisa, 490 ω-3 desaturation, 490 phospholipids, 490 Porphyridium cruentum, 489 PtdCho, 489 TAG, 489, 490 Chlamydomonas reinhardtii, 492 chloroplast-membrane glycerolipids, 492 ∆4 desaturases, 487 ∆6 and ∆5 desaturases, 486, 487 DGDG, 493 DHA, 473, 485 diversity C16 PUFA, 479 Chlorarachniophyceae, 479 chromalveolates, 476 core green lineage, 477 diatoms, 478 freshwater ecosystems, 475 glimpse, 475 green algal lineage, 475 green lineage, 477, 478 Lobosphaera incisa, 478 non-monophyletic evolution, 478 octadecapentaenoic acid, 479 primary endosymbiosis, 475 primary plastid, 475 red algal lineage, 477 Index secondary endosymbiosis, 475 secondary plastid, 477 Stramenopiles clade, 476 VLC-PUFA biosynthesis, 475 double-bond location, 472 EPA, 473 eukaryotic microalgae, 471 FAD, 479–480 fish-oil contamination, 474 “front-end” desaturases, 485 genetic engineering acyl-CoA pool, 497 genomes and transcriptomes, 496 lipid droplets, 497 lipidomics analysis, 497 Nannochloropsis, 496, 498 NoD12 expression, 498 oilseed plants, 496 polar lipid classes, 497 TAG, 497 lipid-biosynthesis pathways, 474 low-temperature-sensitive mutant, 492 ω-3 desaturases, 487 ω-6 VLC-PUFA AA, 473 photosynthetic organism, 487 photosynthetic planktonic microalgae, 472 plastidic desaturation (see Chloroplast galactolipids) polar diatoms and chlorophytes, 493 PUFA elongation, 487–488 putative desaturase, 486 Thraustochytriaceae, 485 unsaturation level, 491 VLC-PUFA production, 472 heterotrophic production, 495 L incisa, 495 marine photosynthetic diatom, 495 mass cultivation, 493 micrographs, 494 photoautotrophic diatoms, 494 primary and secondary plastids, 495 Yarrowia lipolytica, 474 Microspore mother cells (MMCs), 320 Monogalactosyldiacylglycerol (MGDG), 53 CURT1, 134 cyanobacteria, 29 in plants amiR-MGD1, 29 Arabidopsis mgd1-1 mutant, 28 Chl fluorescence analysis, 29 isoform, 28 photoprotective mechanism, 28 synthase genes, 28 thylakoid membrane biogenesis, 28 Index EPR measurements, 134 extended ordered protein arrays, 134 membrane fusions, 135 protein complexes cytochrome b6f, 139 in LHCII structures, 135–136 light-harvesting complexes, 136–137 PSI, structure and function, 139 PSII, structure and function, 137–139 xanthophyll cycle localization and operation, 143–144 non-bilayer phases, 142, 143 pigments, 141–142 solubilisation capacity, 142, 143 MYB transcription factors, 321 N NINJA, co-repressors, 409 Non-bilayer lipids, 134 flexible surface model, 146 fluid mosaic membrane model, 146 hypotheses, 148 lateral pressure bilayer membrane model, 146 MGDG (see Monogalactosyldiacylglycerol (MGDG)) phases, 147 refined model, 147 VDE and lipocalin proteins, 149 Nuclear magnetic resonance (NMR), 454 O -Omics approaches, 458 Chlamydomonas reinhardtii (see Chlamydomonas reinhardtii) genomics and transcriptomics, 451–453 metabolomics, 453, 454 proteomics, 453 Oxylipins, 62, 344–345 P Pavement cells, 288 Peptide “fingerprints”, 453 Phaseolus, 410 PHD-finger proteins, 321 Phloem-localized lipid-associated protein (PLAFP), 348 Phosphatidic acid (PA), 164–166, 208, 351–353 Phosphatidylglycerol (PG), cyanobacteria, 35–39 531 in plants, 34–35 Phosphoinositides, 350 Photosynthesis core photosynthetic protein–cofactor complexes, 22 DGDG cyanobacteria, 32–33 in plants, 30–32 MGDG cyanobacteria, 29 in plants, 27–29 PG cyanobacteria, 35–39 in plants, 34–35 photosynthetic protein–cofactor complexes Cyt b6/f, 26 Cyt f, 27 LHCII, 27 PSI, 25 PSII, 25, 26 SQDG cyanobacteria, 40 in plants, 39–40 thylakoid glycerolipids, 22 Photosystem (PS) I, 25 Photosystem (PS) II, 25, 26 Physcomitrella patens, 411 Phytooxylipins, 406 Phytozome Genome Browser, 452 Plant pollen exine development angiosperms, life cycle, 315 biological processes, 317 chemical staining experiments, 318 colonization, 329 development stages, 319 exine biosynthesis de novo FAS, 323–324 fatty acid synthesis, 323 phenolic compounds, 324 functions and enzymatic activities, 330 inner intine, 316 morphological analysis, 317 morphological features, 320 outer exine, 316, 317 phylogenetic studies, 330 pollen coat, 316 regulation network AMS, 328 AtMYB103, 329 GAMYB, 329 MS1, 327 TAZ1, 328 TDR/bHLH5, 328 reverse genetic analysis, 330 532 Plant pollen exine development (cont.) SAPs, 318 sporopollenin precursors, 317 ABC transporters, 326 lipid transfer proteins, 326–327 tapetal cells, 319 tapetum, 320–321 Plastidial fatty acid biosynthesis, Plastidial lipids (prokaryotic pathway), 53 Processing-Associated Tetratricopeptide Repeat protein (PratA), 90 Programmed cell death (PCD), 274–276 Proteomics, 453 Pyrosequencing, 452 Pyruvate dehydrogenase (PDH), Q Quantitative real-time PCR (qRT-PCR), 372 R Reactive electrophile species (RES), 411, 436 Reactive oxygen species (ROS), 436 Relief of repression model, 409 Response regulator Rre37 (SyNrrA), 516 S Salicylic acid (SA), 342, 343 Sanger sequencing, 452 Secondary endosymbiosis with chlorophyta, 70 with rhodophyta in alveolata, 73–74 haptophyte, 71 in heterokonts (Strameopiles), 71–73 Secondary ion MS (SIMS), 14 Sequencing by synthesis (Illumina), 452 Serine palmitoyltransferase (SPT) activity, 275 sigE-overexpression, 518–520 Sigma factor (SigE), 516 Single-cell Raman spectroscopy (SCRS), 231 Sphingolipids acid, 271 alkaline ceramidases, 271 ceramide synthesis, 265–266 endomembrane trafficking, 273 fatty acid synthesis and structural modifications, 263–264 glucosylceramide synthesis, 267 inositolphosphoceramide synthesis, 267–268 Index LCB (see Long-chain bases (LCB)) membrane function, 271–273 net content and composition, 270 neutral, 271 physiological mediators ABA-dependent guard cell closure, 274 cold stress signaling, 276–277 pathogen resistance, 276 PCD, 274–276 structure, 250–252 Sphingosine-analog mycotoxins (SAMs), 275 Sporopollenin acceptor particles (SAPs), 318 Sugar catabolism bioplastics, 519 hydrogen production, 519 light/dark and day/night conditions, 512, 513 metabolic engineering, 518 metabolic map, 513 nitrogen-starved conditions, 515 glutamine synthetase, 514 microarray analysis, 514 2-OG levels, 514 protein levels, OPP pathway, 514 PHB biosynthesis, 519 sigE-overexpression, 519, 520 transcriptional regulators AbrB-family, 517 histidine kinases (Hik8 and Hik31), 517, 518 response regulator, Rre37 (SyNrrA), 516 RNA polymerase SigE, 516 Sulfoquinovose transferase (SQD1), 59 Sulfoquinovosyldiacylglycerol (SQDG), 458 cyanobacteria, 40 in plants, 39–40 Sulphoquinovosyldiacylglycerol (SQD2), 193 Syncytial endosperm, 303 Synechocystis 6803, 512–514, (see also Sugar catabolism) T Tapetum degeneration retardation (TDR), 328 TAPETUM DEVELOPMENT ZINC FINGER PROTEIN1 (TAZ1), 328 Thin layer chromatography (TLC), 11–12 Thiobarbituric acid reactive substances (TBARS), 191 Thylakoid membranes biogenesis, 88–90 533 Index of cyanobacteria, 90–92 de novo biogenesis, 96–97 diatom, 131 galactolipid MGDG, 130 lipid composition, 129 negatively charged PG, 130 non-bilayer propensity, 130 phase behaviour, 131–134 photosystem I, mutant of, 96 proteoliposome experiments, 131 SQDG, 130 structure of, 86–88 ultrastructure, 86–88 Time-of-flight (TOF) spectrometry, 453 TOPLESS, co-repressors, 409 Triacylglycerols (TAGs) environmental stresses, 183–185 microalgae, 189–193 acyl chains, 186 acyl-CoA-dependent and independent pathways, 210–211 acyl remodeling, 213–215 bioethanol production, 186 biofuel products vs crops, 186 Brefeldin A, 188 chemical/non-chemical, 188 chlamydomonas (see Chlamydomonas) cost effective, 187 culture aging/senescence, 189 culture and aging, 188 DAG, 208–212 glycerolipid synthesis, 208–210 lipid droplets, 215–217 nitrogen deficiency, 188 non-chemical based stresses, 188 phosphorus starvation, 188 Nannochloropsis, 193–196 non-seed plant tissues genetic engineering, 181–183 plant oils, 181 Trigalactosyldiacylglycerol (TGDG), 91 Tuberonic acid (TA), 413 U UDP-glucose pyrophsophorylase (UGP3), 59 UDP-sulfoquinovose synthase (SQD1), 59 V Very long chain polyunsaturated fatty acids (VLCPUFAs), 53 Very long-chain omega-3 and omega-6 polyunsaturated fatty acids (VLC-PUFA) See Microalgae Vesicle-inducing protein in plastids (VIPP1), 63, 88 W Western blot analysis, 370 Wintermans enzyme or galactolipid:galactolipid galactosyltransferase, 92 WRINKLED1 (WRI1), 182 X Xanthophyll cycle (XC), 134 higher plants and algae, 140–141 localization and operation of, 143–144 non-bilayer phase, 142 non-bilayer phases, 143 pigments, 141–142 solubilisation, 143 solubilisation capacity, 142 Y Yeast 2-hybrid (Y2H) assays, 371