Photosynthesis Research

, Volume 92, Issue 2, pp 205–215 | Cite as

The essential role of phosphatidylglycerol in photosynthesis

  • Hajime Wada
  • Norio Murata
Research Article


Since the first identification of phosphatidylglycerol in Scenedesmus by Benson and Maruo in 1958, researchers have studied many biological functions of this phospholipid. Genetic, biochemical, and structural studies of photosynthetic organisms have revealed that phosphatidylglycerol is crucial to the photosynthetic transport of electrons, the development of chloroplasts, and tolerance to chilling. In this review, we summarize our present understanding of the biochemical and physiological functions of phosphatidylglycerol in cyanobacteria and higher plants.


Andrew Benson Chilling sensitivity Membrane lipid Phosphatidylglycerol Photosystem II Thylakoid membrane 



Acyl-carrier protein








Endoplasmic reticulum


Glycerol 3-phosphate


Light-harvesting complex


Lysophosphatidic acid




Phosphatidic acid












Photosystem I


Photosystem II




Fatty acid containing X carbon atoms with Y double bonds, in the cis-configuration, at position Z counted from the carboxyl terminus



This work was supported by a Grant-in-Aid for Scientific Research (no. 16570029) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.


  1. Andersson B, Aro E-M (2001) Photodamage and D1 protein turnover in photosystem II. In: Aro E-M, Andersson B (eds) Regulation of photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 377–393Google Scholar
  2. Andrews J, Mudd JB (1985) Phosphatidylglycerol synthesis in pea chloroplasts. Pathway and localization. Plant Physiol 79:259–265PubMedGoogle Scholar
  3. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedCrossRefGoogle Scholar
  4. Babiychuk E, Müller F, Eubel H, Braun H-P, Frentzen M, Kushnir S (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33:899–909PubMedCrossRefGoogle Scholar
  5. Benson AA, Maruo B (1958) Plant phospholipids. Identification of the phosphatidyl glycerols. Biochim Biophys Acta 27:189–195PubMedCrossRefGoogle Scholar
  6. Benson AA, Maruo B (1989) A ‘nova’ in phosphate metabolism, GPG, and discovery of phosphatidylglycerol. Biochim Biophys Acta 1000:447–451PubMedGoogle Scholar
  7. Block MA, Dorne A-J, Joyard J, 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
  8. Browse J, McCourt P, Somerville CR (1985) A mutant of Arabidopsis lacking a chloroplast-specific lipid. Science 227:763–765CrossRefPubMedGoogle Scholar
  9. Browse J, Somerville C (1991) Glycerolipid synthesis – biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42:467–506CrossRefGoogle Scholar
  10. Carman GM, Henry SA (1999) Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog Lipid Res 38:361–399PubMedCrossRefGoogle Scholar
  11. Demonkos I, Malec P, Sallai A, Kovács L, Itoh K, Shen G, Ughy B, Bogos B, Sakurai I, Kis M, Strzalka K, Wada H, Itoh S, Farkas T, Gombos Z (2004) Phosphatidylglycerol is essential for oligomerization of photosystem I reaction center. Plant Physiol 134:1471–1478CrossRefGoogle Scholar
  12. Dorne AJ, Joyard J, Douce R (1990) Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87:71–74PubMedCrossRefGoogle Scholar
  13. Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232PubMedCrossRefGoogle Scholar
  14. Droppa M, Horváth G, Hideg E, Farkas T (1995) The role of phospholipids in regulating photosynthetic electron transport activities: treatment of thylakoids with phospholipase C. Photosynth Res 46:287–293CrossRefGoogle Scholar
  15. Dubertret G, Mirshahi A, Mirshahi M, Gerard-Hirne C, Tremolieres A (1994) Evidence from in vivo manipulations of lipid composition in mutants that the Δ3-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 226:473–482PubMedCrossRefGoogle Scholar
  16. Dubertret G, Gerard-Hirne C, Trémolières A (2002) Importance of trans3-hexadecenoic acid-containing phosphatidylglycerol in the formation of the trimeric light-harvesting complex in Chlamydomonas. Plant Physiol Biochem 40:829–836CrossRefGoogle Scholar
  17. Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7:270–276PubMedCrossRefGoogle Scholar
  18. Frentzen M, Heinz E, McKeon TA, Stumpf PK (1983) Specificities and selectivities of glycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. Eur J Biochem 129:629–636PubMedCrossRefGoogle Scholar
  19. Frentzen M, Nishida I, Murata N (1987) Properties of the plastidial acyl-(acyl-carrier protein): glycerol-3-phosphate acyltransferase from the chilling-sensitive plant squash (Cucurbita moschata). Plant Cell Physiol 28:1195–1201Google Scholar
  20. Gombos Z, Várkonyi Z, Hagio M, Iwaki M, Kovács L, Masamoto K, Itoh S, Wada H (2002) Phosphatidylglycerol requirement for the function of electron acceptor plastoquinone QB in the photosystem II reaction center. Biochemistry 41:3796–3802PubMedCrossRefGoogle Scholar
  21. Griebau R, Frentzen M (1994) Biosynthesis of phosphatidylglycerol in isolated mitochondria of etiolated mung bean (Vigna radiata L) seedlings. Plant Physiol 105:1269–1274PubMedGoogle Scholar
  22. Hagio M, Gombos Z, Várkonyi Z, Masamoto K, Sato N, Tsuzuki M, Wada H (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol 124:795–804PubMedCrossRefGoogle Scholar
  23. Hagio M, Sakurai I, Sato S, Kato T, Tabata S, Wada H (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43:1456–1464PubMedCrossRefGoogle Scholar
  24. Hobe S, Prytulla S, Kühlbrandt W, Paulsen H (1994) Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J 13:3423–3429PubMedGoogle Scholar
  25. Hobe S, Förster R, Klingler J, Paulsen H (1995) N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34:10224–10228PubMedCrossRefGoogle Scholar
  26. Ishizaki O, Nishida I, Agata K, Eguchi G, Murata N (1988) Cloning and nucleotide sequence of cDNA for the plastid glycerol-3-phosphate acyltransferase from squash. FEBS Lett 238:424–430PubMedCrossRefGoogle Scholar
  27. Ishizaki-Nishizawa O, Fujii T, Azuma M, Sekiguchi K, Murata N, Ohtani T, Toguri T (1996) Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase. Nat Biotechnol 14:1003–1006PubMedCrossRefGoogle Scholar
  28. Jordan BR, Chow W-S, Baker AJ (1983) The role of phospholipids in the molecular organisation of pea chloroplast membranes: effect of phospholipid depletion on photosynthetic activities. Biochim Biophys Acta 725:77–86CrossRefGoogle Scholar
  29. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917PubMedCrossRefGoogle Scholar
  30. Joyard J, Maréchal E, Miege C, Block MA, Dorne A-J, Douce R (1998) Structure, distribution and biosynthesis of glycerolipids from higher plant chloroplasts. In: Siegenthaler P-A, Murata N (eds) Lipids in Photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 21–52Google Scholar
  31. Kenrick JR, Bishop DG (1986) Phosphatidylglycerol and sulphoquinovosyldiacylglycerol in leaves and fruits of chilling-sensitive plants. Phytochemistry 25:1293–1295CrossRefGoogle Scholar
  32. Kruse O, Schmid GH (1995) The role of phosphatidylglycerol as a functional effector and membrane anchor of the D1-core peptide from photosystem II-particles of the cyanobacterium Oscillatoria chalybea. Z Naturforsch 50c:380–390Google Scholar
  33. Kruse O, Hankamer B, Konczak C, Gerle C, Morris E, Radunz A, Schmid GH, Barber J (2000) Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem 275:6509–6514PubMedCrossRefGoogle Scholar
  34. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014PubMedCrossRefGoogle Scholar
  35. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292PubMedCrossRefGoogle Scholar
  36. Loll B, Kern J, Seanger W, Zouni A, Biesiadka J (2005) Toward complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  37. Lyons JK (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466CrossRefGoogle Scholar
  38. Maanni AE, Dubertret G, Delrieu MJ, Roche O, Trémolières A (1998) Mutants of Chlamydomonas reinhardtii affected in phosphatidylglycerol metabolism and thylakoid biogenesis. Plant Physiol Biochem 36:609–619CrossRefGoogle Scholar
  39. Malkin R, Niyogi K (2000) Photosynthesis. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, Maryland, pp 568–628Google Scholar
  40. Matsumoto K (2001) Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol Microbiol 39:1427–1433PubMedCrossRefGoogle Scholar
  41. McCourt P, Browse J, Watson J, Arntzen CJ, Somerville CR (1985) Analysis of photosynthetic antenna function in a mutant of Arabidopsis thaliana (L.) lacking trans-hexadecenoic acid. Plant Physiol 78:853–858PubMedGoogle Scholar
  42. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106CrossRefGoogle Scholar
  43. 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 92:6219–6223PubMedCrossRefGoogle Scholar
  44. Moore TS Jr (1974) Phosphatidylglycerol synthesis in castor bean endosperm. Kinetics, requirements, and intracellular localization. Plant Physiol 54:164–168PubMedGoogle Scholar
  45. Moore TS Jr (1982) Phospholipid biosynthesis. Annu Rev Plant Physiol 33:235–259CrossRefGoogle Scholar
  46. Mudd JB, Dezacks R (1981) Synthesis of phosphatidylglycerol by chloroplasts from leaves of Spinacia oleracea L. (spinach). Arch Biochem Biophys 209:584–591PubMedCrossRefGoogle Scholar
  47. Murata N (1983) Molecular species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 24:81–86Google Scholar
  48. Murata N, Nishida I (1987) Lipids of blue-green algae (cyanobacteria). In: Stumpf PK, Conn EE (eds) The biochemistry of plants, vol 9. Academic Press, Orlando, USA, pp 315–347Google Scholar
  49. Murata N, Tasaka Y (1997) Glycerol-3-phosphate acyltransferase in plants. Biochim Biophys Acta 1348:10–16PubMedGoogle Scholar
  50. Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1–8PubMedGoogle Scholar
  51. Murata N, Yamaya J (1984) Temperature-dependent phase behavior of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Physiol 74:1016–1024PubMedCrossRefGoogle Scholar
  52. Murata N, Sato N, Takahashi N, Hamazaki Y (1982) Compositions and positional distributions of fatty acids in phospholipids from leaves of chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 23:1071–1079Google Scholar
  53. Murata N, Wada H, Gombos Z (1992a) Modes of fatty-acid desaturation in cyanobacteria. Plant Cell Physiol 33:933–941Google Scholar
  54. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992b) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713CrossRefGoogle Scholar
  55. Nishida I, 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
  56. Nishida I, Frentzen M, Ishizaki O, Murata N (1987) Purification of isomeric forms of acyl-(acyl-carrier protein): glycerol-3-phosphate acyltransferase from greening squash cotyledons. Plant Cell Physiol 28:1071–1079Google Scholar
  57. 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 21:267–277PubMedCrossRefGoogle Scholar
  58. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749PubMedCrossRefGoogle Scholar
  59. Nußberger S, Dörr K, Wang DN, Kühlbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234:347–356PubMedCrossRefGoogle Scholar
  60. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970PubMedCrossRefGoogle Scholar
  61. Ohnishi M, Thompson Jr GA (1991) Biosynthesis of the unique trans3-hexadecenoic acid component of chloroplast phosphatidylglycerol: evidence concerning its site and mechanism of formation. Arch Biochem Biophys 288:591–599PubMedCrossRefGoogle Scholar
  62. Okazaki K, Sato N, Tsuji N, Tsuzuki M, Nishida I (2006) The significance of C16 fatty acids at the sn-2 positions of glycerolipids in the photosynthetic growth of Synechocystis sp. PCC6803. Plant Physiol 141:546–556PubMedCrossRefGoogle Scholar
  63. Phillips MC, Hauser H, Paltauf F (1972) The inter- and intra-molecular mixing of hydrocarbon chains in lecithin/water systems. Chem Phys Lipids 8:127–133PubMedCrossRefGoogle Scholar
  64. Raison JK (1973) The influence of temperature-induced phase changes on kinetics of respiratory and other membrane-associated enzymes. J Bioenerg 4:285–309PubMedCrossRefGoogle Scholar
  65. Raison JK, Wright LC (1983) Thermal phase transitions in the polar lipids of plant membranes. Their induction by diunsaturated phospholipids and their possible relation to chilling injury. Biochim Biophys Acta 731:69–78CrossRefGoogle Scholar
  66. Roughan G, Slack R (1984) Glycerolipid synthesis in leaves. Trends Biochem Sci 9:383–386CrossRefGoogle Scholar
  67. Roughan PG, Thompson GA Jr, Cho SH (1987) Metabolism of exogenous long-chain fatty acids by spinach leaves. Arch Biochem Biophys 259:481–496PubMedCrossRefGoogle Scholar
  68. Sakamoto A, Sulpice R, Kaneseki T, Hou C-X, Kinoshita M, Higashi S, Moon BY, Nonaka H, Murata N (2004) Genetic modification of fatty acid unsaturation of chloroplastic phosphatidylglycerol alters the sensitivity to cold stress. Plant Cell Environ 27:99–105CrossRefGoogle Scholar
  69. Sakurai I, Hagio M, Gombos Z, Tyystjärvi T, Paakkarinen V, Aro E-M, Wada H (2003) Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiol 133:1376–1384PubMedCrossRefGoogle Scholar
  70. Sakurai I, Shen J-R, Leng J, Ohashi S, Kobayashi M, Wada H (2006) Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J Biochem 140:201–209PubMedCrossRefGoogle Scholar
  71. Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117:495–505PubMedCrossRefGoogle Scholar
  72. Sato N, Murata N (1982a) Lipid biosynthesis in the blue-green alga Anabaena variabilis. I. Lipid classes. Biochim Biophys Acta 710:271–278Google Scholar
  73. Sato N, Murata N (1982b) Lipid biosynthesis in the blue-green alga, Anabaena variabilis. II. Fatty acids and lipid molecular species. Biochim Biophys Acta 710:279–289Google Scholar
  74. Sato N, Hagio M, Wada H, Tuzuki M (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97:10655–10660PubMedCrossRefGoogle Scholar
  75. Sato N, Suda K, Tsuzuki M (2004) Responsibility of phosphatidylglycerol for biogenesis of the PSI complex. Biochim Biophys Acta 1658:235–243PubMedCrossRefGoogle Scholar
  76. Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288PubMedCrossRefGoogle Scholar
  77. Shibuya I (1992) Metabolic regulations and biological functions of phospholipids in Escherichia coli. Prog Lipid Res 31:245–299PubMedCrossRefGoogle Scholar
  78. Siegenthaler P-A (1998) Molecular organization of acyl lipids in photosynthetic membranes of higher plants. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 119–144Google Scholar
  79. Somerville C, Browse J, Jaworski JG, Ohlrogge JB (2000) Lipids. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Maryland, pp 456–527Google Scholar
  80. Stroebel D, Choquest Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418PubMedCrossRefGoogle Scholar
  81. Szalontai B, Kota Z, Nonaka H, Murata N (2003) Structural consequences of genetically engineered saturation of the fatty acids of phosphatidylglycerol in tobacco thylakoid membranes. An FTIR study. Biochemistry 42:4292–4299PubMedCrossRefGoogle Scholar
  82. Tasaka Y, Nishida I, Higashi S, Beppu T, Murata N (1990) Fatty acid composition of phosphatidylglycerols in relation to chilling sensitivity of woody plants. Plant Cell Physiol 31:545–550Google Scholar
  83. Trémolières A, Siegenthaler P-A (1998) Reconstitution with lipids. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 175–189Google Scholar
  84. Wada H, Murata N (1989) Synechocystis PCC6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978Google Scholar
  85. Wada H, Murata N (1998) Membrane lipids in cyanobacteria. In: Siegenthaler P-A, Murata N (eds) Lipids in photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 65–81Google Scholar
  86. Weier D, Müller C, Gaspers C, Frentzen M (2005) Characterization of acyltransferases from Synechocystis sp. PCC6803. Biochem Biophys Res Commun 334:1127–1134PubMedCrossRefGoogle Scholar
  87. Wolter FP, Schmidt R, Heinz E (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J 11:4685–4692PubMedGoogle Scholar
  88. Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C, Benning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerophosphate synthase with impaired activity. Plant Physiol 129:594–604PubMedCrossRefGoogle Scholar
  89. 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 99:5732–5737PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesUniversity of TokyoMeguro-kuJapan
  2. 2.National Institute for Basic BiologyMyodaijiJapan

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