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Glycerolipid Biosynthesis and Chloroplast Biogenesis

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Plastid Development in Leaves during Growth and Senescence

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

Chloroplast membranes are enriched with galactoglycerolipids, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG). These galactolipids do not contain phosphorus and chloroplast membranes are therefore very poor in phospholipids, primarily represented as a special trans Δ3-hexadecenoic acid-containing phosphatidylglycerol (PG), a finely compartmentalized amount of phosphatidylcholine (PC) and a very low and transitory level of phosphatidic acid (PA). The biogenesis of chloroplasts requires a highly efficient glycerolipid-synthesis system for the development and functioning of both the chloroplast envelope and the thylakoids. Photosynthesis notably relies on the presence of galactolipids and PG. In this chapter, we review the properties of these glycerolipids, their role in photosynthesis and the characteristics of their synthetic pathways. We focus on the role of MGDG synthase in chloroplast biogenesis, the enzyme functioning in the chloroplast envelope membrane, and different mechanisms involved in its regulation. The regulation of MGDG synthase by the phospholipids, PG and PA, is discussed in terms of membrane homeostasis and plant cell biology.

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Abbreviations

ACP –:

Acyl carrier protein;

C16:0 –:

Palmitic acid;

C16:3 –:

Hexadecatrienoic acid;

C18:0 –:

Stearic acid;

C18:1 –:

Oleic acid;

C18:2 –:

Linoleic acid;

DAG –:

Diacylglycerol;

DGDG –:

Digalactosyldiacylglycerol;

ER –:

Endoplasmic reticulum;

G3P –:

Glycerol-3-Phosphate;

MGDG –:

Monogalactosyldiacylglycerol;

PA –:

Phosphatidic acid;

PAP –:

Phosphatidic acid phosphatase;

PC –:

Phosphatidylcholine;

PE –:

Phosphatidylethanolamine;

PG –:

Phosphatidylglycerol;

PGP –:

Phosphatidylglycerol phosphate;

PI –:

Phosphatidylinositol;

PLC –:

Phospholipase C;

PLD –:

Phospholipase D;

PS –:

Phosphatidylserine;

PS II –:

Photosystem II;

SQDG –:

Sulfoquinovosyldiacylglycerol;

TAG –:

Triacylgly­cerol;

TetraGDG –:

Tetragalactosyldiacylglycerol;

TriGDG –:

Trigalactosyldiacylglycerol;

References

  • Andersson MX, Sandelius AS (2004) A chloroplast-localized vesicular transport system: a bio-informatics approach. BMC Genomics 5:40

    Article  PubMed  CAS  Google Scholar 

  • Andersson MX, Kjellberg JM, Sandelius AS (2001) Chloroplast biogenesis. Regulation of lipid transport to the thylakoid in chloroplasts isolated from expanding and fully expanded leaves of pea. Plant Physiol 127:184–193

    Article  PubMed  CAS  Google Scholar 

  • Andersson MX, Kjellberg JM, Sandelius AS (2004) The involvement of cytosolic lipases in converting phosphatidyl choline to substrate for galactolipid synthesis in the chloroplast envelope. Biochim Biophys Acta 1684:46–53

    Article  PubMed  CAS  Google Scholar 

  • Andersson MX, Goksor M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282:1170–1174

    Article  PubMed  CAS  Google Scholar 

  • Andrews J, Mudd JB (1985) Phosphatidylglycerol synthesis in pea chloroplasts: pathway and localization. Plant Physiol 79:259–265

    Article  PubMed  CAS  Google Scholar 

  • Andrews J, Ohlrogge JB, Keegstra K (1985) Final step of phosphatidic acid synthesis in pea chloroplasts occurs in the inner envelope membrane. Plant Physiol 78:459–465

    Article  PubMed  CAS  Google Scholar 

  • Andrews J, Schmidt H, Heinz E (1989) Interference of electron inhibitors with desaturation of monogalactosyldiacylglycerol in intact chloroplasts. Arch Biochem Biophys 270:611–622

    Article  PubMed  CAS  Google Scholar 

  • Apostolova EL, Domonkos I, Dobrikova AG, Sallai A, Bogos B, Wada H, Gombos Z, Taneva SG (2008) Effect of phosphatidylglycerol depletion on the surface electric properties and the fluorescence emission of thylakoid membranes. J Photochem Photobiol B 91:51–57

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Schottler MA, Kelly AA, Sundqvist C, Dormann P, Karim S, Jarvis P (2008) Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol 148:580–592

    Article  PubMed  CAS  Google Scholar 

  • Aseeva E, Ossenbuhl F, Sippel C, Cho WK, Stein B, Eichacker LA, Meurer J, Wanner G, Westhoff P, Sol J, Vothknecht UC (2007) Vipp 1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol Biochem 45:119–128

    Article  PubMed  CAS  Google Scholar 

  • Awai K, Maréchal E, Block MA, Brun D, Masuda T, Shimada H, Takamiya K, Ohta H, Joyard J (2001) Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:10960–10965

    Article  PubMed  CAS  Google Scholar 

  • Awai K, Xu C, Lu B, Benning C (2006) Lipid trafficking between the endoplasmic reticulum and the chloroplast. Biochem Soc Trans 34:395–398

    Article  PubMed  CAS  Google Scholar 

  • Babiychuk E, Muller F, Eubel H, Braun HP, Frentzen M, Kushnir S (2003) Arabidopsis phosphatidylgly­cerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33:899–909

    Article  PubMed  CAS  Google Scholar 

  • Benning C (1998) Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49:53–75

    Article  PubMed  CAS  Google Scholar 

  • Benning C (2007) Questions remaining in sulfolipid biosynthesis: a historical perspective. Photosynth Res 92:199–203

    Article  PubMed  CAS  Google Scholar 

  • Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25:71–91

    Article  PubMed  CAS  Google Scholar 

  • Bessoule JJ, Testet E, Cassagne C (1995) Synthesis of phosphatidylcholine in the chloroplast envelope after import of lysophosphatidylcholine from endoplasmic reticulum membranes. Eur J Biochem 228:490–497

    Article  PubMed  CAS  Google Scholar 

  • Billecocq A (1975) Structure des membranes biologiques: localisation du sulfoquinovosyldiglycéride dans les diverses membranes des chloroplastes au moyen des anticorps spécifiques. Annales d’Immunologie (Institut Pasteur) 126C:337–352

    CAS  Google Scholar 

  • Billecocq A, Douce R, Faure M (1972) Structures des membranes biologiques: localisation des galactosyldiglycérides dans les chloroplastes au moyen des anticorps spécifiques. CR Académie des Sciences Paris 275:1135–1137

    CAS  Google Scholar 

  • Block MA, Dorne A-J, Joyard J, Douce R (1983a) The phosphatidic acid phosphatase of the chloroplast envelope is located on the inner envelope membrane. FEBS Lett 164:111–115

    Article  CAS  Google Scholar 

  • Block MA, Dorne AJ, Joyard J, Douce R (1983b) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J Biol Chem 258:13281–13286

    PubMed  CAS  Google Scholar 

  • Block MA, Maréchal E, Joyard J (2001) Role of the plastid envelope in the biogenesis of chloroplast lipids. In: Aro EM, Andersson B (eds) Regulation of photosynthesis, vol 11. Kluwer, Dordrecht, pp 195–218

    Chapter  Google Scholar 

  • Botté C, Jeanneau C, Snajdrova L, Bastien O, Imberty A, Breton C, Maréchal E (2005) Molecular modeling and site-directed mutagenesis of plant chloroplast monogalactosyldiacylglycerol synthase reveal critical residues for activity. J Biol Chem 280:34691–34701

    Article  PubMed  CAS  Google Scholar 

  • Botté CY, Deligny M, Roccia A, Bonneau A-L, Saïdani N, Hardré H, Aci S, Yamaryo-Botté Y, Jouhet J, Dubots E, Loizeau K, Bastien O, Bréhélin L, Joyard J, Cintrat J-C, Falconet D, Block MA, Rousseau B, Lopez R, Maréchal E (2011) Chemical inhibitors of monogalactosyldiacylglycerol synthases in Arabidopsis thaliana. Nat Chem Biol 7:834–842

    Article  PubMed  CAS  Google Scholar 

  • Carde J, Joyard J, Douce R (1982) Electron microscopic studies of envelope membranes from spinach plastids. Biol Cell 44:315–324

    Google Scholar 

  • Cline K, Keegstra K (1983) Galactosyltransferases involved in galactolipid biosynthesis are located in the outer membrane of pea chloroplast envelopes. Plant Physiol 71:366–372

    Article  PubMed  CAS  Google Scholar 

  • Coves J, Joyard J, Douce R (1988) Lipid requirement and kinetic studies of solubilized UDP-galactose:diacyl­glycerol galactosyltransferase activity from spinach chloroplast envelope membranes. Proc Natl Acad Sci USA 85:4966–4970

    Article  PubMed  CAS  Google Scholar 

  • Cruz-Ramirez A, Oropeza-Aburto A, Razo-Hernandez F, Ramirez-Chavez E, Herrera-Estrella L (2006) Phospholipase Dζ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103:6765–6770

    Article  PubMed  CAS  Google Scholar 

  • Domonkos I, Laczko Dobos H, Gombos Z (2008) Lipid-assisted protein-protein interactions that support photosynthetic and other cellular activities. Prog Lipid Res 47:422–435

    Article  PubMed  CAS  Google Scholar 

  • Dörmann P, Hoffmann-Benning S, Balbo I, Benning C (1995) Isolation and characterization of an arabidopsis mutant deficient in the thylakoid lipid digalactosyldiacylglycerol. Plant Cell 7:1801–1810

    PubMed  Google Scholar 

  • Dörmann P, Balbo I, Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284:2181–2184

    Article  PubMed  Google Scholar 

  • Dorne AJ, Block MA, Joyard J, Douce R (1982) The galactolipid: galactolipid galactosyltransferase is located on the outer surface of the outer chloroplast envelope. FEBS Lett 145:30–34

    Article  CAS  Google Scholar 

  • Dorne AJ, Joyard J, Block MA, Douce R (1985) Localization of phosphatidylcholine in outer envelope membrane of spinach chloroplasts. J Cell Biol 100:1690–1697

    Article  PubMed  CAS  Google Scholar 

  • Douce R (1974) Site of galactolipid synthesis in spinach chloroplasts. Science 183:852–853

    Article  PubMed  CAS  Google Scholar 

  • Douce R, Joyard J (1990) Biochemistry and function of the plastid envelope. Annu Rev Cell Biol 6:173–216

    Article  PubMed  CAS  Google Scholar 

  • Dubacq JP, Trémolières A (1983) Occurence and function of phosphatidyl glycerol containing d-3-tran-hexadecenoic acid in photosynthetic lamellae. Physiologie Végétale 2:293–312

    Google Scholar 

  • Dubertret G, Mirshahi A, Mirshahi M, Gerard-Hirne C, Tremolieres A (1994) Evidence from in vivo manipulations of lipid composition in mutants that the delta 3-trans-hexadecenoic acid-containing phosphatidylglycerol is involved in the biogenesis of the light-harvesting chlorophyll a/b-protein complex of Chlamydomonas reinhardtii. Eur J Biochem 226:473–482

    Article  PubMed  CAS  Google Scholar 

  • Dubots E, Audry M, Yamaryo Y, Bastien O, Ohta H, Breton C, Maréchal E, Block MA (2010) Activation of the chloroplast monogalactosyldiacylglycerol synthase MGD1 by phosphatidic acid and phosphatidylglycerol. J Biol Chem 285:6003–6011

    Article  PubMed  CAS  Google Scholar 

  • Dubots E, Botté C, Boudière L, Yamaryo-Botté Y, Jouhet J, Maréchal E, Block MA (2012) Role of phosphatidic acid in plant galactolipid synthesis. Biochimie 94(1):86–93

    Article  PubMed  CAS  Google Scholar 

  • Eastmond PJ, Quettier AL, Kroon JT, Craddock C, Adams N, Slabas AR (2010) Phosphatidic acid phosphohydrolase 1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell 22:2796–2811

    Article  PubMed  CAS  Google Scholar 

  • Essigmann B, Hespenheide BM, Kuhn LA, Benning C (1999) Prediction of the active-site structure and NAD(+) binding in SQD1, a protein essential for sulfolipid biosynthesis in Arabidopsis. Arch Biochem Biophys 369:30–41

    Article  PubMed  CAS  Google Scholar 

  • Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345

    PubMed  CAS  Google Scholar 

  • Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7:270–276

    Article  PubMed  CAS  Google Scholar 

  • Frentzen M, Heinz E, McKeon TA, Stumpf PK (1983) Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. Eur J Biochem 129:629–636

    Article  PubMed  CAS  Google Scholar 

  • Frentzen M, Neuburger M, Joyard J, Douce R (1990) Intraorganelle localization and substrate specificities of the mitochondrial acyl-CoA: sn-glycerol-3-phosphate O-acyltransferase and acyl-CoA: 1-acyl-sn-glycerol-3-phosphate O-acyltransferase from potato tubers and pea leaves. Eur J Biochem 187:395–402

    Article  PubMed  CAS  Google Scholar 

  • Fritz M, Lokstein H, Hackenberg D, Welti R, Roth M, Zahringer U, Fulda M, Hellmeyer W, Ott C, Wolter FP, Heinz E (2007) Channeling of eukaryotic diacylglycerol into the biosynthesis of plastidial phosphatidylglycerol. J Biol Chem 282:4613–4625

    Article  PubMed  CAS  Google Scholar 

  • Froehlich JE, Benning C, Dormann P (2001) The digalactosyldiacylglycerol (DGDG) synthase DGD1 is inserted into the outer envelope membrane of chloroplasts in a manner independent of the general import pathway and does not depend on direct interaction with monogalactosyldiacylglycerol syn­thase for DGDG biosynthesis. J Biol Chem 276:31806–31812

    Article  PubMed  CAS  Google Scholar 

  • Gad M, Awai K, Shimojima M, Yamaryo Y, Shimada H, Masuda T, Takamiya K, Ikai A, Ohta H (2001) Accumulation of plant galactolipid affects cell morphology of Escherichia coli. Biochem Biophys Res Commun 286:114–118

    Article  PubMed  CAS  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    Article  PubMed  CAS  Google Scholar 

  • Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256

    Article  PubMed  CAS  Google Scholar 

  • Heinz E, Harwood JL (1977) Incorporation of carbon dioxide, acetate and sulphate into the glycerolipids of Vicia faba leaves. Z Physiol Chem 358:897–908

    Article  CAS  Google Scholar 

  • Heinz E, Roughan PG (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72:273–279

    Article  PubMed  CAS  Google Scholar 

  • Holzl G, Witt S, Gaude N, Melzer M, Schottler MA, Dormann P (2009) The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol 150:1147–1159

    Article  PubMed  CAS  Google Scholar 

  • Hugueney P, Bouvier F, Badillo A, d’Harlingue A, Kuntz M, Camara B (1995) Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci USA 92:5630–5634

    Article  PubMed  CAS  Google Scholar 

  • Jager-Vottero P, Dorne AJ, Jordanov J, Douce R, Joyard J (1997) Redox chains in chloroplast envelope membranes: spectroscopic evidence for the presence of electron carriers, including iron-sulfur centers. Proc Natl Acad Sci USA 94:1597–1602

    Article  PubMed  CAS  Google Scholar 

  • Jarvis P, Dormann P, Peto CA, Lutes J, Benning C, Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97:8175–8179

    Article  PubMed  CAS  Google Scholar 

  • Jouhet J, Marechal E, Bligny R, Joyard J, Block MA (2003) Transient increase of phosphatidylcholine in plant cells in response to phosphate deprivation. FEBS Lett 544:63–68

    Article  PubMed  CAS  Google Scholar 

  • Jouhet J, Marechal E, Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Prog Lipid Res 46:37–55

    Article  PubMed  CAS  Google Scholar 

  • Joyard J, Douce R (1977) Site of synthesis of phosphatidic acid and diacyglycerol in spinach chloroplasts. Biochim Biophys Acta 486:273–285

    Article  PubMed  CAS  Google Scholar 

  • Joyard J, Douce R (1979) Characterization of phosphatidate phosphohydrolase activity associated with chloroplast envelope membranes. FEBS Lett 102:147–150

    Article  PubMed  CAS  Google Scholar 

  • Joyard J, Blée E, Douce R (1986) Sulfolipid synthesis from 35SO42- and [1-14C]-acetate in isolated intact spinach chloroplasts. Biochim Biophys Acta 879:78–87

    Article  CAS  Google Scholar 

  • Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2010) Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Prog Lipid Res 49:128–158

    Article  PubMed  CAS  Google Scholar 

  • Kelly AA, Dormann P (2002) DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalactosyldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions. J Biol Chem 277:1166–1173

    Article  PubMed  CAS  Google Scholar 

  • Kelly AA, Froehlich JE, Dormann P (2003) Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15:2694–2706

    Article  PubMed  CAS  Google Scholar 

  • Kelly AA, Öhman A, Sedoud A, Wieslander A (2007) Membrane homeostasis mechanisms for plant glycosyl-transferases involved in galactolipid biosynthesis: biochemical and in-silico structure studies of key enzymes. In: Benning C, Olhlrogge J (eds) Current advances in the biochemistry and cell biology of plant lipids. Aardvark Global, Salt Lake City, pp 25–31

    Google Scholar 

  • Kim HU, Huang AH (2004) Plastid lysophosphatidyl acyltransferase is essential for embryo development in Arabidopsis. Plant Physiol 134:1206–1216

    Article  PubMed  CAS  Google Scholar 

  • Kim HU, Li Y, Huang AH (2005) Ubiquitous and endoplasmic reticulum-located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell 17:1073–1089

    Article  PubMed  CAS  Google Scholar 

  • Klaus D, Hartel H, Fitzpatrick LM, Froehlich JE, Hubert J, Benning C, Dormann P (2002) Digalacto­syldiacylglycerol synthesis in chloroplasts of the Arabidopsis dgd1 mutant. Plant Physiol 128:885–895

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Awai K, Takamiya K, Ohta H (2004) Arabidopsis type B monogalactosyldiacylglycerol synthase genes are expressed during pollen tube growth and induced by phosphate starvation. Plant Physiol 134:640–648

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Kondo M, Fukuda H, Nishimura M, Ohta H (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc Natl Acad Sci USA 104:17216–17221

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Awai K, Nakamura M, Nagatani A, Masuda T, Ohta H (2009) Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation. Plant J 57:322–331

    Article  PubMed  CAS  Google Scholar 

  • Koo AJ, Ohlrogge JB, Pollard M (2004) On the export of fatty acids from the chloroplast. J Biol Chem 279:16101–16110

    Article  PubMed  CAS  Google Scholar 

  • Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci USA 98:4238–4242

    Article  PubMed  CAS  Google Scholar 

  • Krumova SB, Koehorst RB, Bota A, Pali T, van Hoek A, Garab G, van Amerongen H (2008) Temperature dependence of the lipid packing in thylakoid membranes studied by time- and spectrally resolved fluorescence of Merocyanine 540. Biochim Biophys Acta 1778:2823–2833

    Article  PubMed  CAS  Google Scholar 

  • Krumova SB, Laptenok SP, Kovacs L, Toth T, van Hoek A, Garab G, van Amerongen H (2010) Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. Photosynth Res 105(3):229–242

    Article  PubMed  CAS  Google Scholar 

  • Li HM, Kaneko Y, Keegstra K (1994) Molecular cloning of a chloroplastic protein associated with both the envelope and thylakoid membranes. Plant Mol Biol 25:619–632

    Article  PubMed  CAS  Google Scholar 

  • Li MY, Qin C, Welti R, Wang XM (2006a) Double knockouts of phospholipases Dζ1 and Dζ2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770

    Article  PubMed  CAS  Google Scholar 

  • Li MY, Welti R, Wang XM (2006b) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761

    Article  PubMed  CAS  Google Scholar 

  • Liu CM, Willmund F, Whitelegge JP, Hawat S, Knapp B, Lodha M, Schroda M (2005) J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle-inducing protein in plastids 1. Mol Biol Cell 16:1165–1177

    Article  PubMed  CAS  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2007) Lipids in photosystem II: interactions with protein and cofactors. Biochim Biophys Acta 1767:509–519

    Article  PubMed  CAS  Google Scholar 

  • Lu BB, Xu CC, Awai K, Jones AD, Benning C (2007) A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J Biol Chem 282:35945–35953

    Article  PubMed  CAS  Google Scholar 

  • Malherbe A, Block MA, Joyard J, Douce R (1992) Feedback inhibition of phosphatidate phosphatase from spinach chloroplast envelope membranes by diacylglycerol. J Biol Chem 267:23546–23553

    PubMed  CAS  Google Scholar 

  • Maréchal E, Block MA, Joyard J, Douce R (1994a) Kinetic properties of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes. J Biol Chem 269:5788–5798

    PubMed  Google Scholar 

  • Maréchal E, Block MA, Joyard J, Douce R (1994b) Comparison of the kinetic properties of MGDG synthase in mixed micelles and in envelope membranes from spinach chloroplast. FEBS Lett 352:307–310

    Article  PubMed  Google Scholar 

  • Maréchal E, Miège C, Block MA, Douce R, Joyard J (1995) The catalytic site of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes. Biochemical analysis of the structure and of the metal content. J Biol Chem 270:5714–5722

    Article  PubMed  Google Scholar 

  • Miège C, Maréchal E, Shimojima M, Awai K, Block MA, Ohta H, Takamiya K, Douce R, Joyard J (1999) Biochemical and topological properties of type A MGDG synthase, a spinach chloroplast envelope enzyme catalyzing the synthesis of both prokaryotic and eukaryotic MGDG. Eur J Biochem 265:990–1001

    Article  PubMed  Google Scholar 

  • Miquel M, Block MA, Joyard J, Dorne AJ, Dubacq JP, Kader JC, Douce R (1988) Protein-mediated transfer of phosphatidylcholine from liposomes to spinach chloroplast envelope membranes. Biochim Biophys Acta 937:219–228

    Article  Google Scholar 

  • Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228

    Article  PubMed  CAS  Google Scholar 

  • Moon BY, Higashi S, Gombos Z, Murata N (1995) Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc Natl Acad Sci USA 92:6219–6223

    Article  PubMed  CAS  Google Scholar 

  • Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  PubMed  CAS  Google Scholar 

  • Morre DJ, Morre JT, Morre SR, Sundqvist C, Sandelius AS (1991) Chloroplast biogenesis. Cell-free transfer of envelope monogalactosylglycerides to thylakoids. Biochim Biophys Acta 1070:437–445

    Article  PubMed  CAS  Google Scholar 

  • Mulichak AM, Theisen MJ, Essigmann B, Benning C, Garavito RM (1999) Crystal structure of SQD1, an enzyme involved in the biosynthesis of the plant sulfolipid headgroup donor UDP-sulfoquinovose. Proc Natl Acad Sci USA 96:13097–13102

    Article  PubMed  CAS  Google Scholar 

  • Muller F, Frentzen M (2001) Phosphatidylglycerophos­phate synthases from Arabidopsis thaliana. FEBS Lett 509:298–302

    Article  PubMed  CAS  Google Scholar 

  • Munnik T, Testerink C (2009) Plant phospholipid signaling: “in a nutshell”. J Lipid Res 50:260–265

    Article  CAS  Google Scholar 

  • Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K, Ohta H (2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem 280:7469–7476

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y, Tsuchiya M, Ohta H (2007) Plastidic phosphatidic acid phosphatases identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J Biol Chem 282:29013–29021

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y, Kobayashi K, Ohta H (2009a) Activation of galactolipid biosynthesis in development of pistils and pollen tubes. Plant Physiol Biochem 47:535–539

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y, Koizumi R, Shui G, Shimojima M, Wenk MR, Ito T, Ohta H (2009b) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc Natl Acad Sci USA 106:20978–20983

    Article  PubMed  CAS  Google Scholar 

  • Nishida I, Tasaka Y, Shiraishi H, Murata N (1993) The gene and the RNA for the precursor to the plastid-located glycerol-3-phosphate acyltransferase of Arabidopsis thaliana. Plant Mol Biol 21:267–277

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Hardre-Lienard H, Miras S, Miège C, Block MA, Revah F, Joyard J, Maréchal E (2003) Refolding from denatured inclusion bodies, purification to homogeneity and simplified assay of MGDG synthases from land plants. Protein Expr Purif 31:79–87

    Article  PubMed  CAS  Google Scholar 

  • Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge JB, Browse J, Somerville CR (1991) The genetics of plant lipids. Biochim Biophys Acta 1082:1–26

    Article  PubMed  CAS  Google Scholar 

  • 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 28:567–573

    Article  PubMed  CAS  Google Scholar 

  • Ohta H, Shimojima M, Arai T, Masuda T, Shioi Y, Takamiya K (1995) UDP–galactose:diacylglycerol galactosyltransferase in cucumber seedlings: purification of the enzyme and the activation by phosphatidic acid. In: Kader JC, Mazliak P (eds) Plant lipid metabolism. Kluwer, Dordrecht, pp 152–155

    Chapter  Google Scholar 

  • Okuley J, Lightner J, Feldmann K, Yadav N, Lark E, Browse J (1994) Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Plant Cell 6:147–158

    PubMed  CAS  Google Scholar 

  • Park JM, Cho JH, Kang SG, Jang HJ, Pih KT, Piao HL, Cho MJ, Hwang I (1998) A dynamin-like protein in Arabidopsis thaliana is involved in biogenesis of thylakoid membranes. EMBO J 17:859–867

    Article  PubMed  CAS  Google Scholar 

  • Pineau B, Girard-Bascou J, Eberhard S, Choquet Y, Tremolieres A, Gerard-Hirne C, Bennardo-Connan A, Decottignies P, Gillet S, Wollman FA (2004) A single mutation that causes phosphatidylglycerol deficiency impairs synthesis of photosystem II cores in Chlamydomonas reinhardtii. Eur J Biochem 271:329–338

    Article  PubMed  CAS  Google Scholar 

  • Räntfors M, Everstsson I, Kjellberg JM, Sandelius AS (2000) Intraplastidial lipid trafficking: regulation of galactolipid release from isolated chloroplast envelope. Physiol Plant 110:262–270

    Article  Google Scholar 

  • Rawsthorne S (2002) Carbon flux and fatty acid synthesis in plants. Prog Lipid Res 41:182–196

    Article  PubMed  CAS  Google Scholar 

  • Sakaki T, Saito K, Kawaguchi A, Kondo N, Yamada M (1990) Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol 94:766–772

    Article  PubMed  CAS  Google Scholar 

  • Sanda S, Leustek T, Theisen MJ, Garavito RM, Benning C (2001) Recombinant Arabidopsis SQD1 converts udp-glucose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J Biol Chem 276:3941–3946

    Article  PubMed  CAS  Google Scholar 

  • Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117:495–505

    Article  PubMed  CAS  Google Scholar 

  • Sato N, Hagio M, Wada H, Tsuzuki M (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97:10655–10660

    Article  PubMed  CAS  Google Scholar 

  • Schmidt H, Heinz E (1990) Involvement of ferredoxin indesaturation of lipid-bound oleate in chloroplasts. Plant Physiol 94:214–220

    Article  PubMed  CAS  Google Scholar 

  • Schmidt H, Heinz E (1993) Direct desaturation of intact galactolipids by a desaturase solubilized from spinach (Spinacia oleracea) chloroplast envelopes. Biochem J 289:777–782

    PubMed  CAS  Google Scholar 

  • Schnurr JA, Shockey JM, de Boer GJ, Browse JA (2002) Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol 129:1700–1709

    Article  PubMed  CAS  Google Scholar 

  • Seifert U, Heinz E (1992) Enzymatic characteristics of UDP-sulfoquinovose: DAG sulfoquinovosyltransferase from chloroplast envelopes. Botanica Acta 105:197–205

    CAS  Google Scholar 

  • Shimojima M, Ohta H, Iwamatsu A, Masuda T, Shioi Y, Takamiya K (1997) Cloning of the gene for monogalactosyldiacylglycerol synthase and its evolutionary origin. Proc Natl Acad Sci USA 94:333–337

    Article  PubMed  CAS  Google Scholar 

  • Siebertz HP, Heinz E, Joyard J, Douce R (1980) Labelling in vivo and in vitro of molecular species of lipids from chloroplast envelopes and thylakoids. Eur J Biochem 108:177–185

    Article  PubMed  CAS  Google Scholar 

  • Simidjiev I, Stoylova S, Amenitsch H, Javorfi T, Mustardy L, Laggner P, Holzenburg A, Garab G (2000) Self-assembly of large, ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro. Proc Natl Acad Sci USA 97:1473–1476

    Article  PubMed  CAS  Google Scholar 

  • Slack CR, Roughan PG, Balasingham N (1977) Labelling studies in vivo on the metabolism of the acyl and glycerol moieties of the glycerolipids in the developing maize leaf. Biochem J 162:289–296

    PubMed  CAS  Google Scholar 

  • Tietje C, Heinz E (1998) Uridine-diphospho-sulfo­quinovose: diacylglycerol sulfoquinovosyltransferase activity is concentrated in the inner membrane of chloroplast envelopes. Planta 206:72–78

    Article  CAS  Google Scholar 

  • van Besouw A, Wintermans JF (1978) Galactolipid formation in chloroplast envelopes. I. Evidence for two mechanisms in galactosylation. Biochim Biophys Acta 529:44–53

    Article  PubMed  Google Scholar 

  • Vojta L, Soll J, Bolter B (2007) Protein transport in chloroplasts: targeting to the intermembrane space. FEBS J 274:5043–5054

    Article  PubMed  CAS  Google Scholar 

  • Wada H, Murata N (1990) Temperature-induced changes in the fatty acid composition of the cyanobacterium, Synechocystis PCC6803. Plant Physiol 92:1062–1069

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Sullivan RW, Kight A, Henry RL, Huang JR, Jones AM, Korth KL (2004) Deletion of the chloroplast-localized Thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol 136:3594–3604

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45:250–278

    Article  PubMed  CAS  Google Scholar 

  • Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002

    Article  PubMed  CAS  Google Scholar 

  • Wintermans JF, Van Besouw A, Bogemann G (1981) Galactolipid formation in chloroplast envelopes. II. Isolation-induced changes in galactolipid composition. Biochim Biophys Acta 663:99–107

    Article  PubMed  CAS  Google Scholar 

  • Wu F, Yang Z, Kuang T (2006) Impaired photosynthesis in phosphatidylglycerol-deficient mutant of cyanobacterium Anabaena sp. PCC7120 with a disrupted gene encoding a putative phosphatidylglycerophosphatase. Plant Physiol 141:1274–1283

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Hartel H, Wada H, Hagio M, Yu B, Eakin C, Benning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129:594–604

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Fan J, Riekhof W, Froehlich JE, Benning C (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 22:2370–2379

    Article  PubMed  CAS  Google Scholar 

  • Xu CC, Fan J, Froehlich JE, Awai K, Benning C (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17:3094–3110

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Yu B, Cornish AJ, Froehlich JE, Benning C (2006) Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3- phosphate acyltransferase. Plant J 47:296–309

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Fan J, Cornish AJ, Benning C (2008) Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein. Plant Cell 20:2190–2204

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Moellering ER, Muthan B, Fan J, Benning C (2010) Lipid transport mediated by Arabidopsis TGD proteins is unidirectional from the endoplasmic reticulum to the plastid. Plant Cell Physiol 51:1019–1028

    Article  PubMed  CAS  Google Scholar 

  • Yamaryo Y, Dubots E, Albrieux C, Baldan B, Block MA (2008) Phosphate availability affects the tonoplast localization of PLDzeta2, an Arabidopsis thaliana phospholipase D. FEBS Lett 582:685–690

    Article  PubMed  CAS  Google Scholar 

  • Yang MF, Zheng GL, Zhang FY, Xu YN (2006) FAD2-silencing has pleiotropic effect on polar lipids of leaves and varied effect in different organs of transgenic tobacco. Plant Sci 170:170–177

    Article  CAS  Google Scholar 

  • Yu B, Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36:762–770

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Xu C, Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99:5732–5737

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Wakao S, Fan J, Benning C (2004) Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol 45:503–510

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Jacques Joyard and Roland Douce for initiating this research in our laboratory and for the guidance they gave us. We are thankful to Denis Falconet and Juliette Jouhet for helpful reading of the manuscript. The research conducted in the authors’ laboratory was supported by Centre National de la Recherche Scienti­fique (CNRS), Com­missariat à l’Energie Atomique et aux Energies Alternatives (CEA), Institut National de la Recherche Agronomique (INRA) and Université Joseph Fourier (UJF).

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  1. CEA-Grenoble, iRTSV/LPCV, 17 Rue des Martyrs, F-38054, Grenoble, France

    Maryse A. Block & Eric Maréchal

  2. Department of Medicine, Biochemistry Unit, University of Fribourg, CH-1700, Fribourg, Switzerland

    Emmanuelle Dubots

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  1. Maryse A. Block
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  2. Emmanuelle Dubots
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  3. Eric Maréchal
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Correspondence to Maryse A. Block .

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  1. , School of Life Sciences, Sambalpur University, Jyotivihar, Sambalpur, 768019, Orissa, India

    Basanti Biswal

  2. Botanisches Institut, Universität Kiel, Olshausenstr. 40, Kiel, 24118, Germany

    Karin Krupinska

  3. School of Life Sciences, Sambalpur University, Orissa, 768 019, India

    Udaya C. Biswal

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Block, M.A., Dubots, E., Maréchal, E. (2013). Glycerolipid Biosynthesis and Chloroplast Biogenesis. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_7

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