Journal of Plant Research

, Volume 129, Issue 4, pp 565–580 | Cite as

Role of membrane glycerolipids in photosynthesis, thylakoid biogenesis and chloroplast development

Current Topics in Plant Research


The lipid bilayer of the thylakoid membrane in plant chloroplasts and cyanobacterial cells is predominantly composed of four unique lipid classes; monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulfoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG). MGDG and DGDG are uncharged galactolipids that constitute the bulk of thylakoid membrane lipids and provide a lipid bilayer matrix for photosynthetic complexes as the main constituents. The glycolipid SQDG and phospholipid PG are anionic lipids with a negative charge on their head groups. SQDG and PG substitute for each other to maintain the amount of total anionic lipids in the thylakoid membrane, with PG having indispensable functions in photosynthesis. In addition to biochemical studies, extensive analyses of mutants deficient in thylakoid lipids have revealed important roles of these lipids in photosynthesis and thylakoid membrane biogenesis. Moreover, recent studies of Arabidopsis thaliana suggest that thylakoid lipid biosynthesis triggers the expression of photosynthesis-associated genes in both the nucleus and plastids and activates the formation of photosynthetic machineries and chloroplast development. Meanwhile, galactolipid biosynthesis is regulated in response to chloroplast functionality and lipid metabolism at transcriptional and post-translational levels. This review summarizes the roles of thylakoid lipids with their biosynthetic pathways in plants and discusses the coordinated regulation of thylakoid lipid biosynthesis with the development of photosynthetic machinery during chloroplast biogenesis.


Arabidopsis thaliana Chloroplast Membrane lipid Photosynthesis Thylakoid membrane 



I thank Hajime Wada for comments and suggestions on this manuscript. I thank Kiminori Toyooka, Mayuko Sato, and Mayumi Wakazaki for providing leaf section images in Fig. 3. This work was supported by Grants-in-Aid for Young Scientists (A) (No. 26711016) from Japan Society for the Promotion of Science.


  1. Alban C, Joyard J, Douce R (1988) Preparation and characterization of envelope membranes from nongreen plastids. Plant Physiol 88:709–717. doi: 10.1104/pp.88.3.709 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Andersson MX, Stridh MH, Larsson KE et al (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132. doi: 10.1016/S0014-5793(03)00109-1 PubMedCrossRefGoogle Scholar
  3. Andersson MX, Larsson KE, Tjellström H et al (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 280:27578–27586. doi: 10.1074/jbc.M503273200 PubMedCrossRefGoogle Scholar
  4. Andriankaja M, Dhondt S, De Bodt S et al (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 22:64–78. doi: 10.1016/j.devcel.2011.11.011 PubMedCrossRefGoogle Scholar
  5. Aoki M, Sato N, Meguro A, Tsuzuki M (2004) Differing involvement of sulfoquinovosyl diacylglycerol in photosystem II in two species of unicellular cyanobacteria. Eur J Biochem 271:685–693. doi: 10.1111/j.1432-1033.2003.03970.x PubMedCrossRefGoogle Scholar
  6. Aronsson H, Schöttler MA, Kelly AA et al (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. doi: 10.1104/pp.108.123372 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Awai K, Maréchal E, Block MA et al (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. doi: 10.1073/pnas.181331498 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Awai K, Kakimoto T, Awai C et al (2006) Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis. Plant Physiol 141:1120–1127. doi: 10.1104/pp.106.082859.1120 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Awai K, Ohta H, Sato N (2014) Oxygenic photosynthesis without galactolipids. Proc Natl Acad Sci USA 111:13571–13575. doi: 10.1073/pnas.1403708111 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Babiychuk E, Müller F, Eubel H et al (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33:899–909. doi: 10.1046/j.1365-313X.2003.01680.x PubMedCrossRefGoogle Scholar
  11. Bae G, Choi G (2008) Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol 59:281–311. doi: 10.1146/annurev.arplant.59.032607.092859 PubMedCrossRefGoogle Scholar
  12. Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280:2397–2400. doi: 10.1074/jbc.R400032200 PubMedCrossRefGoogle Scholar
  13. Benning C, Beatty JT, Prince RC, Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci USA 90:1561–1565PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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
  15. Botella C, Sautron E, Boudiere L et al (2016) ALA10, a phospholipid flippase, controls FAD2/FAD3 desaturation of phosphatidylcholine in the ER, and affects chloroplast lipid composition in Arabidopsis thaliana. Plant Physiol 170:1300–1314. doi: 10.1104/pp.15.01557 PubMedGoogle Scholar
  16. Botté CY, Deligny M, Roccia A et al (2011) Chemical inhibitors of monogalactosyldiacylglycerol synthases in Arabidopsis thaliana. Nat Chem Biol 7:834–842. doi: 10.1038/nchembio.658 PubMedCrossRefGoogle Scholar
  17. Covés 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. doi: 10.1073/pnas.85.14.4966 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Demé B, Cataye C, Block MA et al (2014) Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids. FASEB J 28:3373–3383. doi: 10.1096/fj.13-247395 PubMedCrossRefGoogle Scholar
  19. Domonkos I, Malec P, Sallai A et al (2004) Phosphatidylglycerol is essential for oligomerization of photosystem I reaction center. Plant Physiol 134:1471–1478. doi: 10.1104/pp.103.037754 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Domonkos I, Laczkó-Dobos H, Gombos Z (2008) Lipid-assisted protein-protein interactions that support photosynthetic and other cellular activities. Prog Lipid Res 47:422–435. doi: 10.1016/j.plipres.2008.05.003 PubMedCrossRefGoogle Scholar
  21. Dörmann P, Hoffmann-Benning S, Balbo I, Benning C (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7:1801–1810. doi: 10.1105/tpc.7.11.1801 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dörmann P, Balbo I, Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284:2181–2184PubMedCrossRefGoogle Scholar
  23. Dorne A, Joyard J, Douce R (1990) Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87:71–74PubMedPubMedCentralCrossRefGoogle Scholar
  24. Droppa M, Horváth G, Hideg É, Farkas T (1995) The role of phospholipids in regulating photosynthetic electron transport activities: treatment of thylakoids with phospholipase C. Photosynth Res 46:287–293. doi: 10.1007/BF00020442 PubMedCrossRefGoogle Scholar
  25. Dubertret G, Mirshahi A, Mirshahi M et al (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. doi: 10.1111/j.1432-1033.1994.tb20072.x PubMedCrossRefGoogle Scholar
  26. Dubots E, Audry M, Yamaryo Y et al (2010) Activation of the chloroplast monogalactosyldiacylglycerol synthase MGD1 by phosphatidic acid and phosphatidylglycerol. J Biol Chem 285:6003–6011. doi: 10.1074/jbc.M109.071928 PubMedCrossRefGoogle Scholar
  27. El Maanni A, Dubertret G, Delrieu M-J et al (1998) Mutants of Chlamydomonas reinhardtii affected in phosphatidylglycerol metabolism and thylakoid biogenesis. Plant Physiol Biochem 36:609–619. doi: 10.1016/S0981-9428(98)80009-0 CrossRefGoogle Scholar
  28. Endo K, Mizusawa N, Shen J-R et al (2015) Site-directed mutagenesis of amino acid residues of D1 protein interacting with phosphatidylglycerol affects the function of plastoquinone QB in photosystem II. Photosynth Res 126:385–397. doi: 10.1007/s11120-015-0150-9 PubMedCrossRefGoogle Scholar
  29. Essigmann B, Güler S, Narang RA et al (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 95:1950–1955PubMedPubMedCentralCrossRefGoogle Scholar
  30. Froehlich JE, Benning C, Dörmann 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. doi: 10.1074/jbc.M104652200 PubMedCrossRefGoogle Scholar
  31. Fujii S, Kobayashi K, Nakamura Y, Wada H (2014) Inducible knockdown of MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE1 reveals roles of galactolipids in organelle differentiation in Arabidopsis cotyledons. Plant Physiol 166:1436–1449. doi: 10.1104/pp.114.250050 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gaude N, Tippmann H, Flemetakis E et al (2004) The galactolipid digalactosyldiacylglycerol accumulates in the peribacteroid membrane of nitrogen-fixing nodules of soybean and Lotus. J Biol Chem 279:34624–34630. doi: 10.1074/jbc.M404098200 PubMedCrossRefGoogle Scholar
  33. Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56:1469–1479. doi: 10.1093/jxb/eri178 PubMedCrossRefGoogle Scholar
  34. Gombos Z, Várkonyi Z, Hagio M et al (2002) Phosphatidylglycerol requirement for the function of electron acceptor plastoquinone QB in the photosystem II reaction center. Biochemistry 41:3796–3802. doi: 10.1021/bi011884h PubMedCrossRefGoogle Scholar
  35. Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59:115–142. doi: 10.1146/annurev.arplant.59.032607.092938 PubMedCrossRefGoogle Scholar
  36. Güler S, Seeliger A, Härtel H et al (1996) A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271:7501–7507PubMedCrossRefGoogle Scholar
  37. Guo J, Zhang Z, Bi Y et al (2005) Decreased stability of photosystem I in dgd1 mutant of Arabidopsis thaliana. FEBS Lett 579:3619–3624. doi: 10.1016/j.febslet.2005.05.049 PubMedCrossRefGoogle Scholar
  38. Guskov A, Kern J, Gabdulkhakov A et al (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342. doi: 10.1038/nsmb.1559 PubMedCrossRefGoogle Scholar
  39. Hagio M, Gombos Z, Várkonyi Z et al (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol 124:795–804. doi: 10.1104/pp.124.2.795 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hagio M, Sakurai I, Sato S et al (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43:1456–1464. doi: 10.1093/pcp/pcf185 PubMedCrossRefGoogle Scholar
  41. Härtel H, Lokstein H, Dörmann P et al (1997) Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiol 115:1175–1184. doi: 10.1104/pp.115.3.1175 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Haselier A, Akbari H, Weth A et al (2010) Two closely related genes of Arabidopsis encode plastidial cytidinediphosphate diacylglycerol synthases essential for photoautotrophic growth. Plant Physiol 153:1372–1384. doi: 10.1104/pp.110.156422 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hennig R, Heidrich J, Saur M et al (2015) IM30 triggers membrane fusion in cyanobacteria and chloroplasts. Nat Commun 6:7018. doi: 10.1038/ncomms8018 PubMedCrossRefGoogle Scholar
  44. Hölzl G, Witt S, Kelly AA et al (2006) Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants. Proc Natl Acad Sci USA 103:7512–7517. doi: 10.1073/pnas.0600525103 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hölzl G, Witt S, Gaude N et al (2009) The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol 150:1147–1159. doi: 10.1104/pp.109.139758 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hung C-H, Kobayashi K, Wada H, Nakamura Y (2015) Isolation and characterization of a phosphatidylglycerophosphate phosphatase1, PGPP1, in Chlamydomonas reinhardtii. Plant Physiol Biochem 92:56–61. doi: 10.1016/j.plaphy.2015.04.002 PubMedCrossRefGoogle Scholar
  47. Itoh S, Kozuki T, Nishida K et al (2012) Two functional sites of phosphatidylglycerol for regulation of reaction of plastoquinone QB in photosystem II. Biochim Biophys Acta 1817:287–297. doi: 10.1016/j.bbabio.2011.10.002 PubMedCrossRefGoogle Scholar
  48. Ivanov AG, Hendrickson L, Krol M et al (2006) Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to photosystem I acceptor-side limitations. Plant Cell Physiol 47:1146–1157. doi: 10.1093/pcp/pcj089 PubMedCrossRefGoogle Scholar
  49. Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14. doi: 10.1016/j.bbabio.2008.09.013 PubMedCrossRefGoogle Scholar
  50. Jarvis P, Dörmann P, Peto CA et al (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97:8175–8179. doi: 10.1073/pnas.100132197 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Jordan BR, Chow W, 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. doi: 10.1016/0005-2728(83)90226-8 CrossRefGoogle Scholar
  52. Jordan P, Fromme P, Witt HT et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. doi: 10.1038/35082000 PubMedCrossRefGoogle Scholar
  53. Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci 4:494. doi: 10.3389/fpls.2013.00494 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jouhet J, Maréchal E, Baldan B et al (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167:863–874. doi: 10.1083/jcb.200407022 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Joyard J, Teyssier E, Miège C et al (1998) The biochemical machinery of plastid envelope membranes. Plant Physiol 118:715–723PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kansy M, Wilhelm C, Goss R (2014) Influence of thylakoid membrane lipids on the structure and function of the plant photosystem II core complex. Planta 240:781–796. doi: 10.1007/s00425-014-2130-2 PubMedCrossRefGoogle Scholar
  57. Karim S, Aronsson H (2014) The puzzle of chloroplast vesicle transport—involvement of GTPases. Front Plant Sci 5:472. doi: 10.3389/fpls.2014.00472 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kelly AA, Dörmann 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. doi: 10.1074/jbc.M110066200 PubMedCrossRefGoogle Scholar
  59. Kelly AA, Froehlich JE, 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 15:2694–2706. doi: 10.1105/tpc.016675 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kim E-H, Razeghifard R, Anderson JM, Chow WS (2007) Multiple sites of retardation of electron transfer in Photosystem II after hydrolysis of phosphatidylglycerol. Photosynth Res 93:149–158. doi: 10.1007/s11120-006-9126-0 PubMedCrossRefGoogle Scholar
  61. Kobayashi K, Ohta H (2008) Possible requirement of galactolipids for embryogenesis. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the Sun. Springer, Dordrecht, pp 783–786CrossRefGoogle Scholar
  62. 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. doi: 10.1104/pp.103.032656 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kobayashi K, Kondo M, Fukuda H et al (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc Natl Acad Sci USA 104:17216–17221. doi: 10.1073/pnas.0704680104 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kobayashi K, Awai K, Nakamura M et al (2009a) Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation. Plant J 57:322–331. doi: 10.1111/j.1365-313X.2008.03692.x PubMedCrossRefGoogle Scholar
  65. Kobayashi K, Nakamura Y, Ohta H (2009b) Type A and type B monogalactosyldiacylglycerol synthases are spatially and functionally separated in the plastids of higher plants. Plant Physiol Biochem 47:518–525. doi: 10.1016/j.plaphy.2008.12.012 PubMedCrossRefGoogle Scholar
  66. Kobayashi K, Narise T, Sonoike K et al (2013) Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis. Plant J 73:250–261. doi: 10.1111/tpj.12028 PubMedCrossRefGoogle Scholar
  67. Kobayashi K, Fujii S, Sasaki D et al (2014) Transcriptional regulation of thylakoid galactolipid biosynthesis coordinated with chlorophyll biosynthesis during the development of chloroplasts in Arabidopsis. Front Plant Sci 5:272. doi: 10.3389/fpls.2014.00272 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kobayashi K, Fujii S, Sato M et al (2015) Specific role of phosphatidylglycerol and functional overlaps with other thylakoid lipids in Arabidopsis chloroplast biogenesis. Plant Cell Rep 34:631–642. doi: 10.1007/s00299-014-1719-z PubMedCrossRefGoogle Scholar
  69. Kobayashi K, Endo K, Wada H (2016) Multiple impacts of loss of plastidic phosphatidylglycerol biosynthesis on photosynthesis during seedling growth of Arabidopsis. Front Plant Sci 7:336. doi: 10.3389/fpls.2016.00336 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Koussevitzky S, Nott A, Mockler TC et al (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719. doi: 10.1126/science PubMedCrossRefGoogle Scholar
  71. Kruse O, Hankamer B, Konczak C et al (2000) Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem 275:6509–6514. doi: 10.1074/jbc.275.9.6509 PubMedCrossRefGoogle Scholar
  72. Lee J, He K, Stolc V et al (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749. doi: 10.1105/tpc.106.047688 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Li C, Wang Y, Liu L et al (2011) A rice plastidial nucleotide sugar epimerase is involved in galactolipid biosynthesis and improves photosynthetic efficiency. PLoS Genet 7:e1002196. doi: 10.1371/journal.pgen.1002196 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Masuda S, Harada J, Yokono M et al (2011) A monogalactosyldiacylglycerol synthase found in the green sulfur bacterium Chlorobaculum tepidum reveals important roles for galactolipids in photosynthesis. Plant Cell 23:2644–2658. doi: 10.1105/tpc.111.085357 PubMedPubMedCentralCrossRefGoogle Scholar
  75. Miège C, Maréchal E, Shimojima M et al (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. doi: 10.1046/j.1432-1327.1999.00801.x PubMedCrossRefGoogle Scholar
  76. Minoda A, Sato N, Nozaki H et al (2002) Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269:2353–2358. doi: 10.1046/j.1432-1033.2002.02896.x PubMedCrossRefGoogle Scholar
  77. Minoda A, Sonoike K, Okada K et al (2003) Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas. FEBS Lett 553:109–112. doi: 10.1016/S0014-5793(03)00981-5 PubMedCrossRefGoogle Scholar
  78. Mizusawa N, Wada H (2012) The role of lipids in photosystem II. Biochim Biophys Acta 1817:194–208. doi: 10.1016/j.bbabio.2011.04.008 PubMedCrossRefGoogle Scholar
  79. Mizusawa N, Sakata S, Sakurai I et al (2009a) Involvement of digalactosyldiacylglycerol in cellular thermotolerance in Synechocystis sp. PCC 6803. Arch Microbiol 191:595–601. doi: 10.1007/s00203-009-0486-7 PubMedCrossRefGoogle Scholar
  80. Mizusawa N, Sakurai I, Sato N, Wada H (2009b) Lack of digalactosyldiacylglycerol increases the sensitivity of Synechocystis sp. PCC 6803 to high light stress. FEBS Lett 583:718–722. doi: 10.1016/j.febslet.2009.01.021 PubMedCrossRefGoogle Scholar
  81. Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci 16:98–107. doi: 10.1016/j.tplants.2010.11.004 PubMedCrossRefGoogle Scholar
  82. Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228. doi: 10.1126/science.1191803 PubMedCrossRefGoogle Scholar
  83. Moreau P, Bessoule JJ, Mongrand S et al (1998) Lipid trafficking in plant cells. Prog Lipid Res 37:371–391PubMedCrossRefGoogle Scholar
  84. Myers AM, James MG, Lin Q et al (2011) Maize opaque5 encodes monogalactosyldiacylglycerol synthase and specifically affects galactolipids necessary for amyloplast and chloroplast function. Plant Cell 23:2331–2347. doi: 10.1105/tpc.111.087205 PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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. doi: 10.1074/jbc.M704385200 PubMedCrossRefGoogle Scholar
  86. 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. doi: 10.1006/jmbi.1993.1591 PubMedCrossRefGoogle Scholar
  87. Ohta H, Shimojima M, Arai T et al (1995a) UDP-galactose: diacylglycerol galactosyltransferase in cucumber seedlings: purification of the enzyme and the activation by phosphatidic acid. Plant Lipid Metab. doi: 10.1007/978-94-015-8394-7_42 Google Scholar
  88. Ohta H, Shimojima M, Ookata K et al (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
  89. Okazaki Y, Shimojima M, Sawada Y et al (2009) A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 21:892–909. doi: 10.1105/tpc.108.063925 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Okazaki Y, Otsuki H, Narisawa T et al (2013) A new class of plant lipid is essential for protection against phosphorus depletion. Nat Commun 4:1510. doi: 10.1038/ncomms2512 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Peterhansel C, Horst I, Niessen M et al (2010) Photorespiration. Arabidopsis Book 12:e0130. doi: 10.1199/tab.0130 CrossRefGoogle Scholar
  92. Pineau B, Girard-bascou J, Eberhard S et al (2004) A single mutation that causes phosphatidylglycerol deficiency impairs synthesis of photosystem II cores in Chlamydomonas reinhardtii. Eur J Biochem 271:329–338. doi: 10.1046/j.1432-1033.2003.03931.x PubMedCrossRefGoogle Scholar
  93. Powikrowska M, Oetke S, Jensen PE, Krupinska K (2014) Dynamic composition, shaping and organization of plastid nucleoids. Front Plant Sci 5:424. doi: 10.3389/fpls.2014.00424 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Qin X, Suga M, Kuang T, Shen J-R (2015) Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348:989–995. doi: 10.1126/science.aab0214 PubMedCrossRefGoogle Scholar
  95. Rast A, Heinz S, Nickelsen J (2015) Biogenesis of thylakoid membranes. Biochim Biophys Acta 1847:821–830. doi: 10.1016/j.bbabio.2015.01.007 PubMedCrossRefGoogle Scholar
  96. Reifarth F, Christen G, Seeliger AG et al (1997) Modification of the water oxidizing complex in leaves of the dgd1 mutant of Arabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol. Biochemistry 36:11769–11776. doi: 10.1021/bi9709654 PubMedCrossRefGoogle Scholar
  97. Rocha J, Sarkis J, Thomas A et al (2016) Structural insights and membrane binding properties of MGD1, the major galactolipid synthase in plants. Plant J 85:622–633. doi: 10.1111/tpj.13129 PubMedCrossRefGoogle Scholar
  98. Ruckle ME, Larkin RM (2009) Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on GENOMES UNCOUPLED 1 and cryptochrome 1. New Phytol 182:367–379. doi: 10.1111/j.1469-8137.2008.02729.x PubMedCrossRefGoogle Scholar
  99. Sakurai I, Hagio M, Gombos Z et al (2003) Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiol 133:1376–1384. doi: 10.1104/pp.103.026955 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Sakurai I, Mizusawa N, Ohashi S et al (2007a) Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol 144:1336–1346. doi: 10.1104/pp.107.098731 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Sakurai I, Mizusawa N, Wada H, Sato N (2007b) Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol 145:1361–1370. doi: 10.1104/pp.107.106781 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Sarkis J, Rocha J, Maniti O et al (2014) The influence of lipids on MGD1 membrane binding highlights novel mechanisms for galactolipid biosynthesis regulation in chloroplasts. FASEB J 28:3114–3123. doi: 10.1096/fj.14-250415 PubMedCrossRefGoogle Scholar
  103. Sasaki Y, Kozaki A, Hatano M (1997) Link between light and fatty acid synthesis: thioredoxin-linked reductive activation of plastidic acetyl-CoA carboxylase. Proc Natl Acad Sci USA 94:11096–11101. doi: 10.1073/pnas.94.20.11096 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117:495–505. doi: 10.1007/s10265-004-0183-1 PubMedCrossRefGoogle Scholar
  105. Sato N (2015) Is monoglucosyldiacylglycerol a precursor to monogalactosyldiacylglycerol in all cyanobacteria? Plant Cell Physiol 56:1890–1899. doi: 10.1093/pcp/pcv116 PubMedCrossRefGoogle Scholar
  106. Sato N, Murata N (1982) Lipid biosynthesis in the blue-green alga, Anabaena variabilis. I. Lipid classes. Biochim Biophys Acta 710:271–278CrossRefGoogle Scholar
  107. Sato N, Sonoike K, Tsuzuki M, Kawaguchi A (1995a) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234:16–23. doi: 10.1111/j.1432-1033.1995.016_c.x PubMedCrossRefGoogle Scholar
  108. Sato N, Tsuzuki M, Matsuda Y et al (1995b) Isolation and characterization of mutants affected in lipid metabolism of Chlumydomonas reinhardtii. Eur J Biochem 230:987–993. doi: 10.1111/j.1432-1033.1995.0987g.x PubMedCrossRefGoogle Scholar
  109. Schaller S, Latowski D, Jemioła-Rzemińska M et al (2010) The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim Biophys Acta 1797:414–424. doi: 10.1016/j.bbabio.2009.12.011 PubMedCrossRefGoogle Scholar
  110. Schaller S, Latowski D, Jemioła-Rzemińska M et al (2011) Regulation of LHCII aggregation by different thylakoid membrane lipids. Biochim Biophys Acta 1807:326–335. doi: 10.1016/j.bbabio.2010.12.017 PubMedCrossRefGoogle Scholar
  111. Sekine K, Hase T, Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277:24399–24404. doi: 10.1074/jbc.M201714200 PubMedCrossRefGoogle Scholar
  112. Serrato AJ, Fernández-Trijueque J, Barajas-López J-D et al (2013) Plastid thioredoxins: a “one-for-all” redox-signaling system in plants. Front Plant Sci 4:463. doi: 10.3389/fpls.2013.00463 PubMedPubMedCentralCrossRefGoogle Scholar
  113. Shimojima M, Ohta H, Iwamatsu A et al (1997) Cloning of the gene for monogalactosyldiacylglycerol synthase and its evolutionary origin. Proc Natl Acad Sci USA 94:333–337PubMedPubMedCentralCrossRefGoogle Scholar
  114. Shimojima M, Watanabe T, Madoka Y et al (2013) Differential regulation of two types of monogalactosyldiacylglycerol synthase in membrane lipid remodeling under phosphate-limited conditions in sesame plants. Front Plant Sci 4:469. doi: 10.3389/fpls.2013.00469 PubMedPubMedCentralCrossRefGoogle Scholar
  115. Shipley GG, Green JP, Nichols BW (1973) The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochim Biophys Acta 311:531–544. doi: 10.1016/0005-2736(73)90128-4 PubMedCrossRefGoogle Scholar
  116. Steffen R, Kelly AA, Huyer J et al (2005) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana wild type plants and mutants with genetically modified lipid content. Biochemistry 44:3134–3142. doi: 10.1021/bi048465f PubMedCrossRefGoogle Scholar
  117. Tanoue R, Kobayashi M, Katayama K et al (2014) Phosphatidylglycerol biosynthesis is required for the development of embryos and normal membrane structures of chloroplasts and mitochondria in Arabidopsis. FEBS Lett 588:1680–1685. doi: 10.1016/j.febslet.2014.03.010 PubMedCrossRefGoogle Scholar
  118. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60. doi: 10.1038/nature09913 PubMedCrossRefGoogle Scholar
  119. Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541:91–101. doi: 10.1016/S0167-4889(01)00153-7 PubMedCrossRefGoogle Scholar
  120. Wada H, Murata N (1989) Synechocystis PCC6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978Google Scholar
  121. Wada H, Murata N (1998) Membrane lipids in cyanobacteria. In: Siegenthaler P-A, Murata N (eds) Lipids in Photosynthesis: Structure, Function and Genetics. Springer, Dordrecht, pp 65–81Google Scholar
  122. Wada H, Murata N (2007) The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res 92:205–215. doi: 10.1007/s11120-007-9203-z PubMedCrossRefGoogle Scholar
  123. Waters MT, Wang P, Korkaric M et al (2009) GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21:1109–1128. doi: 10.1105/tpc.108.065250 PubMedPubMedCentralCrossRefGoogle Scholar
  124. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395. doi: 10.1038/nrg2348 PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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. doi: 10.1104/pp.106.083451.1274 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Wu W, Ping W, Wu H et al (2013) Monogalactosyldiacylglycerol deficiency in tobacco inhibits the cytochrome b6f-mediated intersystem electron transport process and affects the photostability of the photosystem II apparatus. Biochim Biophys Acta 1827:709–722. doi: 10.1016/j.bbabio.2013.02.013 PubMedCrossRefGoogle Scholar
  127. Xu C, Härtel H, Wada H et al (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129:594–604. doi: 10.1104/pp.002725 PubMedPubMedCentralCrossRefGoogle Scholar
  128. Yamaryo Y, Kanai D, Awai K et al (2003) Light and cytokinin play a co-operative role in MGDG synthesis in greening cucumber cotyledons. Plant Cell Physiol 44:844–855. doi: 10.1093/pcp/pcg110 PubMedCrossRefGoogle Scholar
  129. Yamaryo Y, Motohashi K, Takamiya K et al (2006) In vitro reconstitution of monogalactosyldiacylglycerol (MGDG) synthase regulation by thioredoxin. FEBS Lett 580:4086–4090. doi: 10.1016/j.febslet.2006.06.050 PubMedCrossRefGoogle Scholar
  130. Yu B, Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36:762–770. doi: 10.1046/j.1365-313X.2003.01918.x PubMedCrossRefGoogle Scholar
  131. 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. doi: 10.1073/pnas.082696499 PubMedPubMedCentralCrossRefGoogle Scholar
  132. Zhang L, Sakamoto W (2015) Possible function of VIPP1 in maintaining chloroplast membranes. Biochim Biophys Acta 1847:831–837. doi: 10.1016/j.bbabio.2015.02.013 PubMedCrossRefGoogle Scholar
  133. Zhou F, Liu S, Hu Z et al (2009) Effect of monogalactosyldiacylglycerol on the interaction between photosystem II core complex and its antenna complexes in liposomes of thylakoid lipids. Photosynth Res 99:185–193. doi: 10.1007/s11120-008-9388-9 PubMedCrossRefGoogle Scholar
  134. Zhou Y, Peisker H, Weth A et al (2013) Extraplastidial cytidinediphosphate diacylglycerol synthase activity is required for vegetative development in Arabidopsis thaliana. Plant J 75:867–879. doi: 10.1111/tpj.12248 PubMedCrossRefGoogle Scholar

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© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesThe University of TokyoTokyoJapan

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