Abstract
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.
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Abbreviations
- ACP:
-
Acyl-carrier protein
- CDP-DG:
-
CDP-diacylglycerol
- Cyt:
-
Cytochrome
- DGDG:
-
Digalactosyldiacylglycerol
- ER:
-
Endoplasmic reticulum
- G3P:
-
Glycerol 3-phosphate
- LHC:
-
Light-harvesting complex
- LPA:
-
Lysophosphatidic acid
- MGDG:
-
Monogalactosyldiacylglycerol
- PA:
-
Phosphatidic acid
- PC:
-
Phosphatidylcholine
- PE:
-
Phosphatidylethanolamine
- PG:
-
Phosphatidylglycerol
- PGP:
-
Phosphatidylglycerophosphate
- PQ:
-
Plastoquinone
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- SQDG:
-
Sulfoquinovosyldiacylglycerol
- X:Y(Z):
-
Fatty acid containing X carbon atoms with Y double bonds, in the cis-configuration, at position Z counted from the carboxyl terminus
References
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 377–393
Andrews J, Mudd JB (1985) Phosphatidylglycerol synthesis in pea chloroplasts. Pathway and localization. Plant Physiol 79:259–265
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134
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 33:899–909
Benson AA, Maruo B (1958) Plant phospholipids. Identification of the phosphatidyl glycerols. Biochim Biophys Acta 27:189–195
Benson AA, Maruo B (1989) A ‘nova’ in phosphate metabolism, GPG, and discovery of phosphatidylglycerol. Biochim Biophys Acta 1000:447–451
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 258:13281–13286
Browse J, McCourt P, Somerville CR (1985) A mutant of Arabidopsis lacking a chloroplast-specific lipid. Science 227:763–765
Browse J, Somerville C (1991) Glycerolipid synthesis – biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42:467–506
Carman GM, Henry SA (1999) Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog Lipid Res 38:361–399
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 134:1471–1478
Dorne AJ, Joyard J, Douce R (1990) Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87:71–74
Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232
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 46:287–293
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 226:473–482
Dubertret G, Gerard-Hirne C, Trémolières A (2002) Importance of trans-Δ3-hexadecenoic acid-containing phosphatidylglycerol in the formation of the trimeric light-harvesting complex in Chlamydomonas. Plant Physiol Biochem 40:829–836
Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7:270–276
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 129:629–636
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 28:1195–1201
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 41:3796–3802
Griebau R, Frentzen M (1994) Biosynthesis of phosphatidylglycerol in isolated mitochondria of etiolated mung bean (Vigna radiata L) seedlings. Plant Physiol 105:1269–1274
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 124:795–804
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 43:1456–1464
Hobe S, Prytulla S, Kühlbrandt W, Paulsen H (1994) Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J 13:3423–3429
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 34:10224–10228
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 238:424–430
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 14:1003–1006
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 725:77–86
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 411:909–917
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 21–52
Kenrick JR, Bishop DG (1986) Phosphatidylglycerol and sulphoquinovosyldiacylglycerol in leaves and fruits of chilling-sensitive plants. Phytochemistry 25:1293–1295
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:380–390
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 275:6509–6514
Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014
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 428:287–292
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 438:1040–1044
Lyons JK (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466
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 36:609–619
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 568–628
Matsumoto K (2001) Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol Microbiol 39:1427–1433
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 78:853–858
Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106
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
Moore TS Jr (1974) Phosphatidylglycerol synthesis in castor bean endosperm. Kinetics, requirements, and intracellular localization. Plant Physiol 54:164–168
Moore TS Jr (1982) Phospholipid biosynthesis. Annu Rev Plant Physiol 33:235–259
Mudd JB, Dezacks R (1981) Synthesis of phosphatidylglycerol by chloroplasts from leaves of Spinacia oleracea L. (spinach). Arch Biochem Biophys 209:584–591
Murata N (1983) Molecular species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 24:81–86
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 315–347
Murata N, Tasaka Y (1997) Glycerol-3-phosphate acyltransferase in plants. Biochim Biophys Acta 1348:10–16
Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1–8
Murata N, Yamaya J (1984) Temperature-dependent phase behavior of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Physiol 74:1016–1024
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 23:1071–1079
Murata N, Wada H, Gombos Z (1992a) Modes of fatty-acid desaturation in cyanobacteria. Plant Cell Physiol 33:933–941
Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992b) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713
Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568
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 28:1071–1079
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
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 1757:742–749
Nußberger S, Dörr K, Wang DN, Kühlbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234:347–356
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970
Ohnishi M, Thompson Jr GA (1991) Biosynthesis of the unique trans-Δ3-hexadecenoic acid component of chloroplast phosphatidylglycerol: evidence concerning its site and mechanism of formation. Arch Biochem Biophys 288:591–599
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 141:546–556
Phillips MC, Hauser H, Paltauf F (1972) The inter- and intra-molecular mixing of hydrocarbon chains in lecithin/water systems. Chem Phys Lipids 8:127–133
Raison JK (1973) The influence of temperature-induced phase changes on kinetics of respiratory and other membrane-associated enzymes. J Bioenerg 4:285–309
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 731:69–78
Roughan G, Slack R (1984) Glycerolipid synthesis in leaves. Trends Biochem Sci 9:383–386
Roughan PG, Thompson GA Jr, Cho SH (1987) Metabolism of exogenous long-chain fatty acids by spinach leaves. Arch Biochem Biophys 259:481–496
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 27:99–105
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 133:1376–1384
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 140:201–209
Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117:495–505
Sato N, Murata N (1982a) Lipid biosynthesis in the blue-green alga Anabaena variabilis. I. Lipid classes. Biochim Biophys Acta 710:271–278
Sato N, Murata N (1982b) Lipid biosynthesis in the blue-green alga, Anabaena variabilis. II. Fatty acids and lipid molecular species. Biochim Biophys Acta 710:279–289
Sato N, Hagio M, Wada H, Tuzuki M (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97:10655–10660
Sato N, Suda K, Tsuzuki M (2004) Responsibility of phosphatidylglycerol for biogenesis of the PSI complex. Biochim Biophys Acta 1658:235–243
Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288
Shibuya I (1992) Metabolic regulations and biological functions of phospholipids in Escherichia coli. Prog Lipid Res 31:245–299
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 119–144
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 456–527
Stroebel D, Choquest Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418
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 42:4292–4299
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 31:545–550
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 175–189
Wada H, Murata N (1989) Synechocystis PCC6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978
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 65–81
Weier D, Müller C, Gaspers C, Frentzen M (2005) Characterization of acyltransferases from Synechocystis sp. PCC6803. Biochem Biophys Res Commun 334:1127–1134
Wolter FP, Schmidt R, Heinz E (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J 11:4685–4692
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 129:594–604
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
Acknowledgment
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.
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Submitted to the special issue in honor of Andrew A. Benson
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Wada, H., Murata, N. The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res 92, 205–215 (2007). https://doi.org/10.1007/s11120-007-9203-z
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DOI: https://doi.org/10.1007/s11120-007-9203-z