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Biosynthesis and Function of Chloroplast Lipids

  • Mie Shimojima
  • Hiroyuki OhtaEmail author
  • Yuki Nakamura
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 30)

Summary

Chloroplast membranes are composed of four unique lipids, including monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulfoquinovosyldiacylglycerol (SQDG) and phosphatidyl-glycerol (PG). These lipids are crucial for maintaining the function of chloroplasts not simply because they account for a large fraction of the photosynthetic membranes, but because they are assembled into the photosynthetic machinery and are, therefore, directly involved in photosynthetic processes. Indeed, Ara-bidopsis mutants of these lipids possess some photosynthetic defects. Diacylglycerol (DAG), a common precursor of the glycolipids, is produced by both prokaryotic and eukaryotic pathways but the detailed mechanism of DAG supply to chloroplasts remains ambiguous. Because most of the genes encoding the lipid-synthesizing enzymes have been identified in this decade, significant progress delineating the physiological functions and regulatory mechanisms of lipid biosynthesis in chloroplasts has been achieved. In Arabidopsis, two types of MGDG synthases, Type A (AtMGD1) and Type B (AtMGD2, AtMGD3), were identified and their distinct functions in chloroplasts have been unveiled. Type A MGDG synthase is involved in the bulk of MGDG synthesis whereas Type B MGDG synthase is induced under phosphate (Pi)-limited conditions. Two genes, DGD1 and DGD2, for DGDG synthases, which are involved in DGDG synthesis, were identified. DGD1 is the predominant DGDG synthase whereas DGD2 is induced under Pi-limited growth conditions. SQDG synthesis is mediated by two enzymes, SQD1 and SQD2. The key enzyme for PG synthesis is PG phosphate synthase, which is encoded by two genes, PGP1 and PGP2. Plants have homeostatic mechanisms to balance the amount of these lipids by regulating their biosyntheses under various environmental conditions, such as limiting Pi, which stimulates replacement of phospholipids with glycolipids through regulation of enzymes involved in lipid biosynthesis.

Keywords

Phosphatidic Acid Envelope Membrane Chloroplast Lipid Lipid Phosphate Phosphatase Outer Envelope Membrane 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

CDP

Cytidyldiphosphate

DAG

sn-1,2-diacylglycerol

DGD

Digalactosyldiacylglycerol synthase

DGDG

Digalactosyldiacylglycerol

ER

Endoplasmic reticulum

FdGOGAT

Ferredoxin-dependent glutamate synthase

LPP

Lipid phosphate phosphatase

MGDG

Monogalactosyldiacylglycerol

MGD

Monogalactosyldiacylglycerol synthase

NPC

Non-specific phospholipase C

PA

Phosphatidic acid

PAP

Phosphatidic acid phosphatase

PC

Phosphatidylcholine

PE

Phosphatidylethanolamine

PG

Phosphatidylglycerol

PGP

Phosphatidylglycerol phosphate

Pi

Phosphate

PI

Phosphatidylinositol

PLC

Phospholipase C

PLD

Phospholipase D

SQDG

Sulfoquinovosyldiacylglycerol

SQD2

Sulfoquinovosyldiacylglycerol synthase

UDP-Gal

Uridine diphosphate-galactose

UDP-SQ

Uridine diphosphate-sulfoquinovose

SQD1

Uridine diphosphate-sulfoquinovose synthase

Notes

Acknowledgments

The MGDG and DAG research performed in the Ohta lab has been supported, in part, by a Grand-in-Aid for Scientific Research on Priority Areas Nos.17051009, 18056007, 19039010 and 20053005 from MEXT of Japan.

References

  1. Aloni R, Schwalm K, Langhans M and Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216: 841–853PubMedGoogle Scholar
  2. Andersson MX, Stridh MH, Larsson KE, Liljenberg C and Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537: 128–132PubMedCrossRefGoogle Scholar
  3. Andersson MX, Kjellberg JM and Sandelius AS (2004) The involvement of cytosolic lipases in converting phosphatidyl choline to substrate for galactolipid synthesis in the chloro-plast envelope. Biochim Biophys Acta 1684: 46–53PubMedCrossRefGoogle Scholar
  4. Andersson MX, Larsson KE, Tjellstrom H, Liljenberg C and Sandelius AS (2005) Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280: 27578–27586PubMedCrossRefGoogle Scholar
  5. Andrews J and Mudd JB (1985) Phosphatidylglycerol synthesis in pea chloroplasts: Pathway and localization. Plant Physiol 79: 259–265PubMedCrossRefGoogle Scholar
  6. Aronsson H, Shöttler M, Kelly AA, Sundqvist C, Dörmann P, Karim S and Jarvis P (2008) Monogalactosyldiacylg-lycerol deficiency in Arabidopsis thaliana affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol 148: 580–592PubMedCrossRefGoogle Scholar
  7. Avsian-Kretchmer O, Cheng JC, Chen L, Moctezuma E and Sung ZR (2002) Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol 130: 199–209PubMedCrossRefGoogle Scholar
  8. Awai K, Maréchal E, Block MA, Brun D, Masuda T, Shi-mada H, Takamiya K, Ohta H and 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: 10960–10965PubMedCrossRefGoogle Scholar
  9. Awai K, Xu C, Tamot B and Benning C (2006a) A phospha-tidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad Sci USA 103: 10817–10822CrossRefGoogle Scholar
  10. Awai K, Kakimoto T, Awai C, Kaneko T, Nakamura Y, Taka-miya K, Wada H and Ohta H (2006b) Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis in cyanobacteria. Plant Physiol 141: 1120–1127CrossRefGoogle Scholar
  11. Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M and Kushnir S (2003) Arabidopsis phosphatidylglycerophos-phate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33: 899–909PubMedCrossRefGoogle Scholar
  12. Benning C and Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280: 2397–2400PubMedCrossRefGoogle Scholar
  13. Benning C and Somerville CR (1992a) Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. J Bacteriol 174: 6479–6487Google Scholar
  14. Benning C and Somerville CR (1992b) Isolation and genetic complementation of a sulfolipid-deficient mutant of Rho-dobacter sphaeroides. J Bacteriol 174: 2352–2360Google Scholar
  15. Benning C, Beatty JT, Prince RC and Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodo-bacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci USA 90: 1561–1565PubMedCrossRefGoogle Scholar
  16. Benning C, Xu C and Awai K (2006) Non-vesicular and vesicular lipid trafficking involving plastids. Curr Opin Plant Biol 9: 241–247PubMedCrossRefGoogle Scholar
  17. Benning C, Garavito RM and Shimojima M (2008) Sulfoli-pid biosynthesis and function in plants. In: Hell R, Leus-tek T and Dahl C (eds) Sulfur Metabolism in Phototrophic Organisms, pp. 189–204. Springer-Verlag, BerlinGoogle Scholar
  18. Benson AA (2002) Paving the path. Annu Rev Plant Biol 53: 1–25PubMedCrossRefGoogle Scholar
  19. Bishop WR and Bell RM (1985) Assembly of the endoplas-mic reticulum phospholipid bilayer: the phosphatidylcho-line transporter. Cell 42: 51–60PubMedCrossRefGoogle Scholar
  20. Block MA, Dorne AJ, Joyard J and Douce R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J Biol Chem 258: 13281–13286PubMedGoogle Scholar
  21. Browse J and Somerville CR (1991) Glycerolipid synthesis. Biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42: 467–506CrossRefGoogle Scholar
  22. Browse J, McCourt P and Somerville CR (1985) A mutant of Arabidopsis lacking a chloroplast-specific lipid. Science 227: 763–765PubMedCrossRefGoogle Scholar
  23. Camara B, Bardat F, Dogbo O, Brangeon J and Monéger R (1983) Terpenoid metabolism in plastids: Isolation and biochemical characteristics of Capsicum annuum chromo-plasts. Plant Physiol 73: 94–99PubMedCrossRefGoogle Scholar
  24. Carman GM and Henry SA (1989) Phospholipid biosynthesis in yeast. Annu Rev Biochem 58: 635–669PubMedCrossRefGoogle Scholar
  25. Chang SC, Heacock PN, Clancey CJ and Dowhan W (1998) The PEL1 gene (renamed PGS1) encodes the phosphati-dylglycero-phosphate synthase of Saccharomyces cerevi-siae. J Biol Chem 273: 9829–9836PubMedCrossRefGoogle Scholar
  26. Chrastil J and Parrish FW (1987) Phospholipase C and D in rice grains. J Agric Food Chem 35: 624–627CrossRefGoogle Scholar
  27. Cline K and Keegstra K (1983) Galactosyltransferases involved in galactolipid biosynthesis are located in the outer membrane of pea chloroplast envelopes. Plant Phys-iol 71: 366–372CrossRefGoogle Scholar
  28. Covès J, Joyard J and 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: 4966–4970PubMedCrossRefGoogle Scholar
  29. Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramirez-Chávez E and Herrera-Estrella L (2006) Phos-pholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Ara-bidopsis roots. Proc Natl Acad Sci USA 103: 6765–6770PubMedCrossRefGoogle Scholar
  30. Dörmann P, Hoffmann-Benning S, Balbo I and Benning C (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl dia-cylglycerol. Plant Cell 7: 1801–1810PubMedGoogle Scholar
  31. Dörmann P, Balbo I and Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284: 2181–2184PubMedCrossRefGoogle Scholar
  32. Douce R and Joyard J (1980) Lipids: structure and function. In: Stumpf PK (ed) The Biochemistry of Plants, Vol 4, pp. 321–362. Academic Press, New YorkGoogle Scholar
  33. Essigmann B, Güler S, Narang RA, Linke D and Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 1950–1955PubMedCrossRefGoogle Scholar
  34. Essigmann B, Hespenheide BM, Kuhn LA and 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: 30–41PubMedCrossRefGoogle Scholar
  35. Frentzen M, Heinz E, McKeon TA and Stumpf PK (1983) Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyl-transferase from pea and spinach chloroplasts. Eur J Bio-chem 129: 629–636CrossRefGoogle Scholar
  36. Fritz M, Lokstein H, Hackenberg D, Welti R, Roth M, Zähringer U, Fulda M, Hellmeyer W, Ott C, Wolter FP and Heinz E (2007) Channeling of eukaryotic diacylglyc-erol into the biosynthesis of plastidial phosphatidylglyc-erol. J Biol Chem 282: 4613–4625PubMedCrossRefGoogle Scholar
  37. Froehlich JE, Benning C and Dörmann P (2001) The digalac-tosyldiacylglycerol (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 monogalactos-yldiacylglycerol synthase for DGDG biosynthesis. J Biol Chem 276: 31806–31812PubMedCrossRefGoogle Scholar
  38. Gad M, Awai K, Shimojima M, Yamaryo Y, Shimada H, Masuda T, Takamiya K, Ikai A and Ohta H (2001) Accumulation of plant galactolipid affects cell morphology of Escherichia coli. Biochem Biophys Res Commun 286: 114–118PubMedCrossRefGoogle Scholar
  39. Gage DA, Huang ZH and Benning C (1992) Comparison of sulfoquinovosyl diacylglycerol from spinach and the purple bacterium Rhodobacter spaeroides by fast atom bombardment tandem mass spectrometry. Lipids 27: 632–636PubMedCrossRefGoogle Scholar
  40. Gardiner SE and Roughan PG (1983) Relationship between fatty-acyl composition of diacylgalactosylglycerol and turnover of chloroplast phosphatidate. Biochem J 210: 949–952PubMedGoogle Scholar
  41. Gaude N, Nakamura Y, Scheible WR, Ohta H and Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galac-tolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56: 28–39PubMedCrossRefGoogle Scholar
  42. Goss R, Lohr M, Latowski D, Grzyb J, Vieler A, Wilhelm C and Strzalka K (2005) Role of hexagonal structure-forming lipids in diadinoxanthin and violaxanthin solubiliza-tion and de-epoxidation. Biochemistry 44: 4028–4036PubMedCrossRefGoogle Scholar
  43. Güler S, Seeliger A, Härtel H, Renger G and Benning C (1996) A null mutant of Synechococcus sp. PCC 7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271: 7501–7507PubMedCrossRefGoogle Scholar
  44. Gustafson KR, Cardellina JH, Fuller RW, Weislow OS, Kiser RF, Snader KM, Patterson GM and Boyd MR (1989) AIDS-antiviral sulfolipids from cyanobacteria (blue-green algae). J Natl Cancer Inst 81: 1254–1258PubMedCrossRefGoogle Scholar
  45. Hagio M, Gombos Z, Várkonyi Z, Masamoto K, Sato N, Tsuzuki M and Wada H (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol 124: 795–804PubMedCrossRefGoogle Scholar
  46. Hagio M, Sakurai I, Sato S, Kato T, Tabata S and Wada H (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43: 1456–1464PubMedCrossRefGoogle Scholar
  47. Härtel H, Essigmann B, Lokstein H, Hoffmann-Benning S, Peters-Kottig M and Benning C (1998) The phospholipid-deficient pho1 mutant of Arabidopsis thaliana is affected in the organization, but not in the light acclimation, of the thy-lakoid membrane. Biochim Biophys Acta 1415: 205–218PubMedCrossRefGoogle Scholar
  48. Härtel H, Dörmann P and Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97: 10649–10654PubMedCrossRefGoogle Scholar
  49. Heinz E (1977) Enzymatic reactions in galactolipid biosynthesis. In: Tevini M and Lichtenthaler HK (eds) Lipids and Lipid Polymers, pp. 102–120. Springer-Verlag, BerlinCrossRefGoogle Scholar
  50. Heinz E and Roughan PG (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72: 273–279PubMedCrossRefGoogle Scholar
  51. Heinz E, Schmidt H, Hoch M, Jung KH, Binder H and Schmidt RR (1989) Synthesis of different nucleoside 5'-diphospho-sulfoquinovoses and their use for studies on sulfolipid biosynthesis in chloroplasts. Eur J Biochem 184: 445–453PubMedCrossRefGoogle Scholar
  52. Hobbie L and Estelle M (1995) The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J 7: 211–220PubMedCrossRefGoogle Scholar
  53. Hölzl G, Zahringer U, Warnecke D and Heinz E (2005) Gly-coengineering of cyanobacterial thylakoid membranes for future studies on the role of glycolipids in photosynthesis. Plant Cell Physiol 46: 1766–1778PubMedCrossRefGoogle Scholar
  54. Jarvis P, Dörmann P, Peto CA, Lutes J, Benning C and Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97: 8175–8179PubMedCrossRefGoogle Scholar
  55. Jones MR (2007) Lipids in photosynthetic reaction centres: structural roles and functional holes. Prog Lipid Res 46: 56–87PubMedCrossRefGoogle Scholar
  56. Jouhet J, Maréchal E, Bligny R, Joyard J and Block MA (2003) Transient increase of phosphatidylcholine in plant cells in response to phosphate deprivation. FEBS Lett 544: 63–68PubMedCrossRefGoogle Scholar
  57. Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167: 863–874,PubMedCrossRefGoogle Scholar
  58. Joyard J and Douce R (1977) Site of synthesis of phospha-tidic acid and diacyglycerol in spinach chloroplasts. Biochim Biophys Acta 486: 273–285PubMedCrossRefGoogle Scholar
  59. Joyard J and Douce R (1979) Characterization of phosphati-date phosphohydrolase activity associated with chloro-plast envelope membranes. FEBS Lett 102: 147–150PubMedCrossRefGoogle Scholar
  60. Joyard J and Douce R (1987) Galactolipid synthesis. In: The Biochemistry of Plants, Vol 9, pp. 215–274. Academic Press, New YorkGoogle Scholar
  61. Joyard J, Maréchal E, Miège C, Block MA, Dorne AJ and Douce R (1998) Structure, distribution and biosynthesis of glycerolipids from higher plant chloroplasts. In: Siegenthaler PA and Murata N (eds) Lipid in Photosynthesis: Structure, Function and Genetics, pp. 21–52. Kluwer, DordrechtGoogle Scholar
  62. Kates M (1955) Hydrolysis of lecithin by plant plastid enzymes. Can J Biochem Physiol 33: 575–589PubMedCrossRefGoogle Scholar
  63. Kawasaki K, Kuge O, Chang SC, Heacock PN, Rho M, Suzuki K, Nishijima M and Dowhan W (1999) Isolation of a Chinese hamster ovary (CHO) cDNA encoding phos-phatidylglycerophosphate (PGP) synthase, expression of which corrects the mitochondrial abnormalities of a PGP synthase-defective mutant of CHO-K1 cells. J Biol Chem 274: 1828–1834PubMedCrossRefGoogle Scholar
  64. Kelly AA and Dörmann P (2002) DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalactosyldiacylg-lycerol synthase is expressed during growth under phosphate-limiting conditions. J Biol Chem 277: 1166–1173PubMedCrossRefGoogle Scholar
  65. Kelly AA, Froehlich JE and Dörmann 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: 2694–2706PubMedCrossRefGoogle Scholar
  66. Klaus D, Härtel H, Fitzpatrick LM, Froehlich JE, Hubert J, Benning C and Dörmann P (2002) Digalactosyldiacylg-lycerol synthesis in chloroplasts of the Arabidopsis dgd1 mutant. Plant Physiol 128: 885–895PubMedCrossRefGoogle Scholar
  67. Kleinig H and Liedvogel B (1978) Fatty acid synthesis by isolated chromoplasts from the daffodil. [14C]Acetate incorporation and distribution of labelled acids. Eur J Biochem 83: 499–505PubMedCrossRefGoogle Scholar
  68. Kobayashi K, Awai K, Takamiya K and Ohta H (2004) Arabidopsis type B monogalactosyldiacylglycerol syn-thase genes are expressed during pollen tube growth and induced by phosphate starvation. Plant Physiol 134: 640–648PubMedCrossRefGoogle Scholar
  69. Kobayashi K, Masuda T, Takamiya K and Ohta H (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47: 238–248PubMedCrossRefGoogle Scholar
  70. Kobayashi K, Kondo M, Fukuda H, Nishimura M and Ohta H (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc Natl Acad Sci USA 104: 17216–17221PubMedCrossRefGoogle Scholar
  71. Kobayashi K, Awai K, Nakamura M, Nagatani A, Masuda T and 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: 322–331PubMedCrossRefGoogle Scholar
  72. Lai F, Thacker J, Li Y and Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50: 545–556PubMedCrossRefGoogle Scholar
  73. Li M, Qin C, Welti R and Wang X (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: 761–770CrossRefGoogle Scholar
  74. Li M, Welti R and Wang X (2006b) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases D ζ1 and D ζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylg-lycerol accumulation in phosphorus-starved plants. Plant Physiol 142: 750–761CrossRefGoogle Scholar
  75. López-Bucio J, Cruz-Ramírez A and Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280–287PubMedCrossRefGoogle Scholar
  76. Lu B, Xu C, Awai K, Jones AD and Benning C (2007) A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J Biol Chem 282: 35945–35953PubMedCrossRefGoogle Scholar
  77. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109: 7–13PubMedGoogle Scholar
  78. Malherbe A, Block MA, Joyard J and Douce R (1992) Feedback inhibition of phosphatidate phosphatase from spinach chloroplast envelope membranes by diacylglycerol. J Biol Chem 267: 23546–23553PubMedGoogle Scholar
  79. Maréchal E, Block MA, Joyard J and Douce R (1991) Purification of UDP-galactose:1,2-diacylglycerol galactosyl-transferase from spinach chloroplast envelope membrane. C R Acad Sci Paris t 313: 521–528Google Scholar
  80. Maréchal E, Block MA, Joyard J and Douce R (1994a) Comparison of the kinetic properties of MGDG synthase in mixed micelles and in envelope membranes from spinach chloroplast. FEBS Lett 352: 307–310CrossRefGoogle Scholar
  81. Maréchal E, Block MA, Joyard J and Douce R (1994b) Kinetic properties of monogalactosyldiacylglycerol syn-thase from spinach chloroplast envelope membranes. J Biol Chem 269: 5788–5798Google Scholar
  82. Miège C and Maréchal E (1999) 1,2-sn-Diacylglycerol in plant cells: product, substrate and regulator. Plant Physiol Biochem 37: 795–808PubMedCrossRefGoogle Scholar
  83. Miège C, Maréchal E, Shimojima M, Awai K, Block MA, Ohta H, Takamiya K, Douce R and 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: 990–1001PubMedCrossRefGoogle Scholar
  84. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L and Thibaud M-C (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934–11939PubMedCrossRefGoogle Scholar
  85. Mongrand S, Bessoule JJ and Cassagne C (1997) A re-examination in vivo of the phosphatidylcholine-galactoli-pid metabolic relationship during plant lipid biosynthesis. Biochem J 327: 853–858PubMedGoogle Scholar
  86. Mongrand S, Cassagne C and Bessoule JJ (2000) Import of lyso-phosphatidylcholine into chloroplasts likely at the origin of eukaryotic plastidial lipids. Plant Physiol 122: 845–852PubMedCrossRefGoogle Scholar
  87. Moore TS Jr (1974) Phosphatidylglycerol synthesis in castor bean endosperm. Kinetics, requirements, and intracellular localization. Plant Physiol 54: 164–168PubMedCrossRefGoogle Scholar
  88. Moore TS Jr (1982) Phospholipid biosynthesis. Annu Rev Plant Physiol 33: 235–259CrossRefGoogle Scholar
  89. Mudd JB and Dezacks R (1981) Synthesis of phosphatidylg-lycerol by chloroplasts from leaves of Spinacia oleracea L. (spinach). Arch Biochem Biophys 209: 584–591PubMedCrossRefGoogle Scholar
  90. Müller F and Frentzen M (2001) Phosphatidylglycerophos-phate synthases from Arabidopsis thaliana. FEBS Lett 509: 298–302PubMedCrossRefGoogle Scholar
  91. Murphy DJ (1982) The importance of non-planar bilayer regions in photosynthetic membranes and their stabilization by galactolipids. FEBS Lett 150: 19–26CrossRefGoogle Scholar
  92. Murphy DJ (1986) The molecular organisation of the photo-synthetic membranes of higher plants. Biochim Biophys Acta 864: 33–94CrossRefGoogle Scholar
  93. Nakamura Y and Ohta H (2007) The diacylglycerol forming pathways differ among floral organs of Petunia hybrida. FEBS Lett 581: 5475–5479PubMedCrossRefGoogle Scholar
  94. Nakamura Y, Arimitsu H, Yamaryo Y, Awai K, Masuda T, Shimada H, Takamiya K and Ohta H (2003) Digalactos-yldiacylglycerol is a major glycolipid in floral organs of Petunia hybrida. Lipids 38: 1107–1112PubMedCrossRefGoogle Scholar
  95. Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K and Ohta H (2005) A novel phosphatidylcholine-hydro-lyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem 280: 7469–7476PubMedCrossRefGoogle Scholar
  96. Nakamura Y, Tsuchiya M and Ohta H (2007) Plastidic phos-phatidic acid phosphatases identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J Biol Chem 282: 29013–29021PubMedCrossRefGoogle Scholar
  97. Nishida I and Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol BIol 47: 541–568PubMedCrossRefGoogle Scholar
  98. Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G and Aoyama T (2003) Modulation of phos-pholipid signaling by GLABRA2 in root-hair pattern formation. Science 300: 1427–1430PubMedCrossRefGoogle Scholar
  99. Ohlrogge JB and Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957–970PubMedGoogle Scholar
  100. Ohnishi M, Thompson GA Jr (1991) Biosynthesis of the unique trans-delta 3-hexadecenoic acid component of chloroplast phosphatidylglycerol: evidence concerning its site and mechanism of formation. Arch Biochem Biophys 288: 591–599,PubMedCrossRefGoogle Scholar
  101. Ohta H, Shimojima M, Arai T, Masuda T, Shioi Y and Takamiya K (1995a) UDP-galactose: diacylglycerol galactosyltransferase in cucumber seedlings: purification of the enzyme and the activation by phosphatidic acid In: Kader JC and Mazliak P (eds) Plant Lipid Metabolism, pp. 152–155. Kluwer, DordrechtGoogle Scholar
  102. Ohta H, Shimojima M, Ookata K, Masuda T, Shioi Y and Takamiya K (1995b) A close relationship between increases in galactosyltransferase activity and the accumulation of galactolipids during plastid development in cucumber seedlings. Plant Cell Physiol 36: 1115–1120Google Scholar
  103. Okazaki K, Sato N, Tsuji N, Tsuzuki M and Nishida I (2006) The significance of C16 fatty acids in the sn-2 positions of glycerolipids in the photosynthetic growth of Syne-chocystis sp. PCC 6803. Plant Physiol 141: 546–556PubMedCrossRefGoogle Scholar
  104. Ostrander DB, Zhang M, Mileykovskaya E, Rho M and Dowhan W (2001) Lack of mitochondrial anionic phos-pholipids causes an inhibition of translation of protein components of the electron transport chain. A yeast genetic model system for the study of anionic phos-pholipid function in mitochondria. J Biol Chem 276: 25262–25272PubMedCrossRefGoogle Scholar
  105. Pierrugues O, Brutesco C, Oshiro J, Gouy M, Deveaux Y, Carman GM, Thuriaux P and Kazmaier M (2001) Lipid phosphate phosphatases in Arabidopsis. Regulation of the AtLPP1 gene in response to stress. J Biol Chem 276: 20300–20308PubMedCrossRefGoogle Scholar
  106. Pugh CE, Roy AB, Hawkes T and Harwood JL (1995) A new pathway for the synthesis of the plant sulpholipid, sulpho-quinovosyldiacylglycerol. Biochem J 309: 513–519PubMedGoogle Scholar
  107. Raghothama K (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50: 665–693PubMedCrossRefGoogle Scholar
  108. Riekhof WR, Ruckle ME, Lydic TA, Sears BB and Benning C (2003) The sulfolipids 2′-O-acyl-sulfoquinovosyldia-cylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133: 864–874PubMedCrossRefGoogle Scholar
  109. Rouet-Mayer MA, Valentova O, Simond-Côte E, Daussant J and Thévenot C (1995) Critical analysis of phospholipid hydrolyzing activities in ripening tomato fruits. Study by spectrofluorimetry and high-performance liquid chroma-tography. Lipids 30: 739–746PubMedCrossRefGoogle Scholar
  110. Roughan PG (1970) Turnover of the glycerolipids of pumpkin leaves. The importance of phosphatidylcholine. Bio-chem J 117: 1–8Google Scholar
  111. Roughan PG and Slack CR (1982) Cellular organization of glycerolipid metabolism. Annu Rev Plant Physiol 33: 97–132CrossRefGoogle Scholar
  112. Roughan G and Slack R (1984) Glycerolipid synthesis in leaves. Trends Biochem Sci 9: 383–386CrossRefGoogle Scholar
  113. Roughan G, Thompson GA Jr and Cho SH (1987) Metabolism of exogenous long-chain fatty acids by spinach leaves. Arch Biochem Biophys 259: 481–496PubMedCrossRefGoogle Scholar
  114. Sanda S, Leustek T, Theisen MJ, Garavito RM and 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: 3941–3946PubMedCrossRefGoogle Scholar
  115. Sato N (2004) Roles of the acidic lipids sulfoquinovosyl dia-cylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117: 495–505PubMedCrossRefGoogle Scholar
  116. Sato N and Murata N (1982) Lipid biosynthesis in the bluegreen alga, Anabaena variabilis. I. Lipid classes. Biochim Biophys Acta 710: 271–278CrossRefGoogle Scholar
  117. Sato N, Hagio M, Wada H and Tsuzuki M (2000a) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97: 10655–10660CrossRefGoogle Scholar
  118. Sato N, Hagio M, Wada H and Tsuzuki M (2000b) Environmental effects on acidic lipids of thylakoid membranes. Biochem Soc Trans 28: 912–914CrossRefGoogle Scholar
  119. Sato N, Sugimoto K, Meguro A and Tsuzuki M (2003) Identification of a gene for UDP-sulfoquinovose synthase of a green alga, Chlamydomonas reinhardtii, and its phylog-eny. DNA Res 10: 229–237PubMedCrossRefGoogle Scholar
  120. Scherer GF, Paul RU, Holk A and Martinec J (2002) Down-regulation by elicitors of phosphatidylcholine-hydrolyz-ing phospholipase C and up-regulation of phospholipase A in plant cells. Biochem Biophys Res Commun 293: 766–770PubMedCrossRefGoogle Scholar
  121. Seifert U and Heinz E (1992) Enzymatic characteristics of UDP-sulfoquinovose: diacylglycerol sulfoquinovosyltrans-ferase from chloroplast envelopes. Bot Acta 105: 197–205Google Scholar
  122. Shimojima M and Benning C (2003) Native uridine 5'-diphosphate-sulfoquinovose synthase, SQD1, from spinach purifies as a 250-kDa complex. Arch Biochem Biophys 413: 123–130PubMedCrossRefGoogle Scholar
  123. Shimojima M, Ohta H, Iwamatsu A, Masuda T, Shioi Y and Takamiya K (1997) Cloning of the gene for monogalac-tosyldiacylglycerol synthase and its evolutionary origin. Proc Natl Acad Sci USA 94: 333–337PubMedCrossRefGoogle Scholar
  124. Shimojima M, Hoffmann-Benning S, Garavito RM and Benning C (2005) Ferredoxin-dependent glutamate synthase moonlights in plant sulfolipid biosynthesis by forming a complex with SQD1. Arch Biochem Biophys 436: 206–214PubMedCrossRefGoogle Scholar
  125. Siddique MA, Grossmann J, Gruissem W and Baginsky S (2006) Proteome analysis of bell pepper (Capsicum annum L.) chromoplasts. Plant Cell Physiol 47: 1663–1673PubMedCrossRefGoogle Scholar
  126. Simidjiev I, Stoylova S, Amenitsch H, Javorfi T, Mustardy L, Laggner P, Holzenburg A and 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: 1473–1476PubMedCrossRefGoogle Scholar
  127. Slabas T (1997) Galactolipid biosynthesis genes and endo-symbiosis. Trends Plant Sci 2: 161–162CrossRefGoogle Scholar
  128. Somerville CR, Browse J, Jaworski JG and Ohlrogge JB (2000) Lipids. In: Buchanan BB, Gruissem W and Jones RL (eds) Biochemistry and Molecular Biology of Plants, pp. 456–527. American Society of Plant Physiologists, Rockville, MDGoogle Scholar
  129. Strauss H, Leibovitz-Ben GZ and Heller M (1976) Enzymatic hydrolysis of 1-monoacyl-SN-glycerol-3-phosphoryl-choline (1-lysolecithin) by phospholipases from peanut seeds. Lipids 11: 442–448PubMedCrossRefGoogle Scholar
  130. Stymne S and Stobart A (1987) Triacylglycerol biosynthesis. In: Stumpf PK and Conn EE (eds) The Biochemistry of Plants, pp. 175–214. Academic Press, New YorkGoogle Scholar
  131. Teucher T and Heinz E (1991) Purification of UDP-galactose: diacylglycerol galactosyltransferase from chloroplast envelopes of spinach (Spinacia oleracea L.). Planta 184: 319–326CrossRefGoogle Scholar
  132. Ticconi CA, Delatorre CA and Abel S (2001) Attenuation of phosphate starvation responses by phosphite in Arabidop-sis. Plant Physiol 127: 963–972PubMedCrossRefGoogle Scholar
  133. Tietje C and Heinz E (1998) Uridine-diphospho-sulfo-quinovose:diacylglycerol sulfoquinovosyltransferase activity is concentrated in the inner membrane of chloroplast envelopes. Planta 206: 72–78CrossRefGoogle Scholar
  134. Varadarajan DK, Karthikeyan AS, Matilda PD and Raghoth-ama KG (2002) Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol 129: 1232–1240PubMedCrossRefGoogle Scholar
  135. Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139: 566–573PubMedCrossRefGoogle Scholar
  136. Weier D, Müller C, Gaspers C and Frentzen M (2005) Characterisation of acyltransferases from Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 334: 1127–1134PubMedCrossRefGoogle Scholar
  137. Williams JP, Imperial V, Khan MU and Hodson JN (2000) The role of phosphatidylcholine in fatty acid exchange and desaturation in Brassica napus L. leaves. Biochem J 349: 127–133PubMedCrossRefGoogle Scholar
  138. Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C and Benning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129: 594–604PubMedCrossRefGoogle Scholar
  139. Xu C, Fan J, Riekhof W, Froehlich JE and Benning C (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 22: 2370–2379PubMedCrossRefGoogle Scholar
  140. Xu C, Fan J, Froehlich JE, Awai K and Benning C (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17: 3094–3110PubMedCrossRefGoogle Scholar
  141. Yamamoto HY (2006) Functional roles of the major chloro-plast lipids in the violaxanthin cycle. Planta 224: 719–724PubMedCrossRefGoogle Scholar
  142. Yamamoto M and Yamamoto KT (1999) Effects of natural and synthetic auxins on the gravitropic growth habit of roots in two auxin-resistant mutants of Arabidopsis, axr1 and axr4: evidence for defects in the auxin influx mechanism of axr4. J Plant Res 112: 391–396PubMedCrossRefGoogle Scholar
  143. Yamaryo Y, Kanai D, Awai K, Shimojima M, Masuda T, Shimada H, Takamiya K and Ohta H (2003) Light and cytokinin play a co-operative role in MGDG synthesis in greening cucumber cotyledons. Plant Cell Physiol 44: 844–855PubMedCrossRefGoogle Scholar
  144. Yamaryo Y, Motohashi K, Takamiya K, Hisabori T and Ohta H (2006) In vitro reconstitution of monogalactosyldia-cylglycerol (MGDG) synthase regulation by thioredoxin. FEBS Lett 580: 4086–4090PubMedCrossRefGoogle Scholar
  145. Yu B and Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36: 762–770PubMedCrossRefGoogle Scholar
  146. Yu B, Xu C and Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99: 5732–5737PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Center for Biological Resources and InformaticsTokyo Institute of TechnologyMidori-kuJapan
  2. 2.Research Center for the Evolving Earth and PlanetsTokyo Institute of TechnologyMidori-kuJapan
  3. 3.Temasek Life Sciences LaboratoryNational University of SingaporeSingapore

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