Abstract
Photosynthetic membranes provide much of the usable energy for life on earth. To produce photosynthetic membrane lipids, multiple transport steps are required, including fatty acid export from the chloroplast stroma to the endoplasmic reticulum, and lipid transport from the endoplasmic reticulum to the chloroplast envelope membranes. Transport of hydrophobic molecules through aqueous space is energetically unfavorable and must be catalyzed by dedicated enzymes, frequently on specialized membrane structures. Here, we review photosynthetic membrane lipid transport to the chloroplast in the context of photosynthetic membrane lipid synthesis. We independently consider the identity of transported lipids, the proteinaceous transport components, and membrane structures which may allow efficient transport. Recent advances in lipid transport of chloroplasts, bacteria, and other systems strongly suggest that lipid transport is achieved by multiple mechanisms which include membrane contact sites with specialized protein machinery. This machinery is likely to include the TGD1, 2, 3 complex with the TGD5 and TGD4/LPTD1 systems, and may also include a number of proteins with domains similar to other membrane contact site lipid-binding proteins. Importantly, the likelihood of membrane contact sites does not preclude lipid transport by other mechanisms including vectorial acylation and vesicle transport. Substantial progress is needed to fully understand all photosynthetic membrane lipid transport processes and how they are integrated.
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References
AhYoung AP, Jiang J, Zhang J, Khoi Dang X, Loo JA, Zhou ZH, Egea PF (2015) Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci USA 112:E3179–E3188. https://doi.org/10.1073/pnas.1422363112
Alban C, Joyard J, Douce R (1988) Preparation and characterization of envelope membranes from nongreen plastids. Plant Physiol 88:709–717
Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132
Andersson MX, Kjellberg JM, Sandelius AS (2004) The involvement of cytosolic lipases in converting phosphatidyl choline to substrate for galactolipid synthesis in the chloroplast envelope. Biochim Biophys 1684:46–53
Andersson MX, Larsson KE, Tjellström H, Liljenberg C, 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 280:27578–27586
Andersson MX, Goksor M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282:1170–1174
Angkawijaya AE, Nakamura Y (2017) Arabidopsis PECP1 and PS2 are phosphate starvation-inducible phosphocholine phosphatases. Biochem Biophys Res Commun https://doi.org/10.1016/j.bbrc.2017.09.094
Awai K, Xu C, Tamot B, Benning C (2006) A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad Sci USA 103:10817–10822
Barnes AC, Benning C, Roston R (2016) Chloroplast membrane remodeling during freezing stress is accompanied by cytoplasmic acidification activating SENSITIVE TO FREEZING 2. Plant Physiol 171:2140–2149. https://doi.org/10.1104/pp.16.00286
Baslam M, Oikawa K, Kitajima-Koga A, Kaneko K, Mitsui T (2016) Golgi-to-plastid trafficking of proteins through secretory pathway: insights into vesicle-mediated import toward the plastids. Plant Signal Behav. https://doi.org/10.1080/15592324.2016.1221558
Bates PD, Ohlrogge JB, Pollard M (2007) Incorporation of newly synthesized fatty acids into cytosolic glycerolipids in pea leaves occurs via acyl editing. J Biol Chem 282:31206–31216
Bayer EM, Sparkes I, Vanneste S, Rosado A (2017) From shaping organelles to signalling platforms: the emerging functions of plant ER–PM contact sites. Curr Opin Plant Biol 40:89–96. https://doi.org/10.1016/j.pbi.2017.08.006
Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280:2397–2400. https://doi.org/10.1074/jbc.R400032200
Bessoule JJ, Testet E, Cassagne C (1995) Synthesis of phosphatidylcholine in the chloroplast envelope after import of lysophosphatidylcholine from endoplasmic reticulum membranes. Eur J Biochem 228:490–497
Black PN, DiRusso CC (2007) Yeast acyl-CoA synthetases at the crossroads of fatty acid metabolism and regulation. Biochim Biophys Acta Mol Cell Biol Lipids 1771:286–298. https://doi.org/10.1016/j.bbalip.2006.05.003
Block MA, Jouhet J (2015) Lipid trafficking at endoplasmic reticulum–chloroplast membrane contact sites. Curr Opin Cell Biol 35:35. https://doi.org/10.1016/j.ceb.2015.03.004
Block MA, Dorne AJ, 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
Botella C, Sautron E, Boudiere L, Michaud M, Dubots E, Yamaryo-Botte Y, Albrieux C, Marechal E, Block MA, Jouhet J (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. https://doi.org/10.1104/pp.15.01557
Botella C, Jouhet J, Block MA (2017) Importance of phosphatidylcholine on the chloroplast surface. Prog Lipid Res 65:12–23. https://doi.org/10.1016/j.plipres.2016.11.001
Brdiczka DG, Zorov DB, Sheu S-S (2006) Mitochondrial contact sites: their role in energy metabolism and apoptosis. Biochim Biophys 1762:148–163. https://doi.org/10.1016/j.bbadis.2005.09.007
Browse J, Warwick N, Somerville CR, Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the “16:3” plant Arabidopsis thaliana. Biochem J 235:25–31
Browse J, McConn M, James D Jr, Miquel M (1993) Mutants of Arabidopsis deficient in the synthesis of alpha-linolenate. Biochemical and genetic characterization of the endoplasmic reticulum linoleoyl desaturase. J Biol Chem 268:16345–16351
Brunkard JO, Runkel AM, Zambryski PC (2015) Chloroplasts extend stromules independently and in response to internal redox signals. Proc Natl Acad Sci USA 112:10044–10049. https://doi.org/10.1073/pnas.1511570112
Buchner O, Holzinger A, LÜTz C (2007) Effects of temperature and light on the formation of chloroplast protrusions in leaf mesophyll cells of high alpine plants. Plant Cell Environ 30:1347–1356. https://doi.org/10.1111/j.1365-3040.2007.01707.x
Buren S, Ortega-Villasante C, Blanco-Rivero A, Martinez-Bernardini A, Shutova T, Shevela D, Messinger J, Bako L, Villarejo A, Samuelsson G (2011) Importance of post-translational modifications for functionality of a chloroplast-localized carbonic anhydrase (CAH1) in Arabidopsis thaliana. PLoS ONE. https://doi.org/10.1371/journal.pone.0021021
Chen LJ, Li HM (2017) Stable megadalton TOC-TIC supercomplexes as major mediators of protein import into chloroplasts. Plant J 92:178–188. https://doi.org/10.1111/tpj.13643
Coves J, Block MA, Joyard J, Douce R (1986) Solubilization and partial purification of UDP-galactose—diacylglycerol galactosyltransferase activity from spinach chloroplast envelope. FEBS Lett 208:401–406
Cran DG, Dyer AF (1973) Membrane continuity and associations in the fern Dryopteris borreri. Protoplasma 76:103–108. https://doi.org/10.1007/BF01279676
Crotty WJ, Ledbetter MC (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182:839–841. https://doi.org/10.1126/science.182.4114.839
Cruz-Ramirez A, Oropeza-Aburto A, Razo-Hernandez F, Ramirez-Chavez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103:6765–6770
Daum G, Vance JE (1997) Import of lipids into mitochondria. Prog Lipid Res 36:103–130. https://doi.org/10.1016/S0163-7827(97)00006-4
Davletov BA, Sudhof TC (1993) A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J Biol Chem 268:26386–26390
Delfosse K, Wozny MR, Jaipargas E-A, Barton KA, Anderson C, Mathur J (2016) Fluorescent protein aided insights on plastids and their extensions: a critical appraisal frontiers in plant science. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01253
Dong H, Xiang Q, Gu Y, Wang Z, Paterson NG, Stansfeld PJ, He C, Zhang Y, Wang W, Dong C (2014) Structural basis for outer membrane lipopolysaccharide insertion. Nature 511:52–56. https://doi.org/10.1038/nature13464
Dormann P, Benning C (2002) Galactolipids rule in seed plants. Trends Plant Sci 7:112–118
Dörmann P, Balbo I, Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284:2181–2184
Dorne AJ, Joyard J, Block MA, Douce R (1985) Localization of phosphatidylcholine in outer envelope membrane of spinach-chloroplasts. J Cell Biol 100:1690–1697. https://doi.org/10.1083/jcb.100.5.1690
Dorne AJ, Joyard J, Douce R (1990) Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87:71–74
Dubots E, Audry M, Yamaryo Y, Bastien O, Ohta H, Breton C, Marechal E, Block MA (2010) Activation of the chloroplast monogalactosyldiacylglycerol synthase MGD1 by phosphatidic acid and phosphatidylglycerol. J Biol Chem 285:6003–6011. https://doi.org/10.1074/jbc.M109.071928
Eisenberg-Bord M, Shai N, Schuldiner M, Bohnert M (2016) A tether is a tether is a tether: tethering at membrane contact sites. Dev Cell 39:395–409. https://doi.org/10.1016/j.devcel.2016.10.022
Ekiert DC, Bhabha G, Isom GL, Greenan G, Ovchinnikov S, Henderson IR, Cox JS, Vale RD (2017) Architectures of lipid transport systems for the bacterial outer membrane. Cell 169:273–285 e217. https://doi.org/10.1016/j.cell.2017.03.019
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971
Falcone DL, Gibson S, Lemieux B, Somerville C (1994) Identification of a gene that complements an Arabidopsis mutant deficient in chloroplast omega 6 desaturase activity. Plant Physiol 106:1453–1459
Fan J, Zhai Z, Yan C, Xu C (2015) Arabidopsis TRIGALACTOSYLDIACYLGLYCEROL5 interacts with TGD1, TGD2, and TGD4 to facilitate lipid transfer from the endoplasmic reticulum to plastids. Plant Cell 27:2941–2955. https://doi.org/10.1105/tpc.15.00394
Finn RD et al (2017) InterPro in 2017—beyond protein family and domain annotations. Nucleic Acids Res 45:D199. https://doi.org/10.1093/nar/gkw1107
Flinner N, Ellenrieder L, Stiller SB, Becker T, Schleiff E, Mirus O (2013) Mdm10 is an ancient eukaryotic porin co-occurring with the ERMES complex. Biochim Biophys Acta Mol Cell Res 1833:3314–3325. https://doi.org/10.1016/j.bbamcr.2013.10.006
Frentzen M (1986) Biosynthesis and desaturation of the different diacylglycerol moieties in higher plants. J Plant Physiol 124:193–209
Frentzen M (1990) Comparison of certain properties of membrane-bound and solubilized acyltransferase activities of plant microsomes. Plant Sci 69:39–48. https://doi.org/10.1016/0168-9452(90)90103-U
Frentzen M, Heinz E, McKeon TA, Stumpf PK (1983) Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. Eur J Biochem 129:629–636
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
Gaude N, Nakamura Y, Scheible WR, Ohta H, Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56:28–39
Goode JH, Dewey RE (1999) Characterization of aminoalcoholphosphotransferases from Arabidopsis thaliana and soybean. Plant Physiol Biochem 37:445–457. https://doi.org/10.1016/S0981-9428(99)80049-7
Gray JC, Hansen MR, Shaw DJ, Graham K, Dale R, Smallman P, Natesan SKA, Newell CA (2012) Plastid stromules are induced by stress treatments acting through abscisic acid. Plant J 69:387–398. https://doi.org/10.1111/j.1365-313X.2011.04800.x
Hamilton JA, Bhamidipati SP, Kodali DR, Small DM (1991) The interfacial conformation and transbilayer movement of diacylglycerols in phospholipid-bilayers. J Biol Chem 266:1177–1186
Härtel H, Dormann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97:10649–10654. https://doi.org/10.1073/pnas.180320497
Heilmann I, Mekhedov S, King B, Browse J, Shanklin J (2004) Identification of the Arabidopsis palmitoyl-monogalactosyldiacylglycerol Delta 7-desaturase gene FAD5, and effects of plastidial retargeting of Arabidopsis desaturases on the fad5 mutant phenotype. Plant Physiol 136:4237–4245. https://doi.org/10.1104/pp.104.052951
Heinz E, Roughan G (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72:273–279
Heldt HW, Sauer F (1971) The inner membrane of the chloroplast envelope as the site of specific metabolite transport. Biochim Biophys Acta 234:83–91. https://doi.org/10.1016/0005-2728(71)90133-2
Hessenberger M, Zerbes RM, Rampelt H, Kunz S, Xavier AH, Purfürst B, Lilie H, Pfanner N, van der Laan M, Daumke O (2017) Regulated membrane remodeling by Mic60 controls formation of mitochondrial crista junctions. Nat Commun 8:15258. https://doi.org/10.1038/ncomms15258
Holzinger A, Kwok EY, Hanson MR (2008) Effects of arc3, arc5 and arc6 mutations on plastid morphology and stromule formation in green and nongreen tissues of Arabidopsis thaliana. Photochem Photobiol 84:1324–1335. https://doi.org/10.1111/j.1751-1097.2008.00437.x
Hsueh YC, Ehmann C, Flinner N, Ladig R, Schleiff E (2017) The plastid outer membrane localized LPTD1 is important for glycerolipid remodelling under phosphate starvation. Plant Cell Environ 40:1643–1657. https://doi.org/10.1111/pce.12973
Hua R, Cheng D, Coyaud É, Freeman S, Di Pietro E, Wang Y, Vissa A, Yip CM, Fairn GD, Braverman N, Brumell JH, Trimble WS, Raught B, Kim PK (2017) VAPs and ACBD5 tether peroxisomes to the ER for peroxisome maintenance and lipid homeostasis. J Cell Biol 216:367–377. https://doi.org/10.1083/jcb.201608128
Huynen MA, Mühlmeister M, Gotthardt K, Guerrero-Castillo S, Brandt U (2016) Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex. Biochim Biophys Acta Mol Cell Res 1863:91–101. https://doi.org/10.1016/j.bbamcr.2015.10.009
Iba K, Gibson S, Nishiuchi T, Fuse T, Nishimura M, Arondel V, Hugly S, Somerville C (1993) A gene encoding a chloroplast omega-3 fatty acid desaturase complements alterations in fatty acid desaturation and chloroplast copy number of the fad7 mutant of Arabidopsis thaliana. J Biol Chem 268:24099–24105
Im YJ, Raychaudhuri S, Prinz WA, Hurley JH (2005) Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437:154–158. https://doi.org/10.1038/nature03923
Jans DC, Wurm CA, Riedel D, Wenzel D, Stagge F, Deckers M, Rehling P, Jakobs S (2013) STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria. Proc Natl Acad Sci USA 110:8936–8941. https://doi.org/10.1073/pnas.1301820110
Jessen D, Roth C, Wiermer M, Fulda M (2015) Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis. Plant Physiol 167:351–575. https://doi.org/10.1104/pp.114.250365
Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00494
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. https://doi.org/10.1083/jcb.200407022
Joyard J, Douce R (1977) Site of synthesis of phosphatidic acid and diacylglcyerol in spinach chloroplasts. Biochim Biophys 486:273–285
Joyard J, Douce R (1979) Characterization of phosphatidate phosphohydrolase activity associated with chloroplast envelope membranes. FEBS Lett 102:147–150
Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2010) Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Prog Lipid Res 49:128–158. https://doi.org/10.1016/j.plipres.2009.10.003
Kaneko K, Takamatsu T, Inomata T, Oikawa K, Itoh K, Hirose K, Amano M, Nishimura SI, Toyooka K, Matsuoka K, Pozueta-Romero J, Mitsui T (2016) N-glycomic and microscopic subcellular localization analyses of NPP1, 2 and 6 strongly indicate that trans-Golgi compartments participate in the Golgi to plastid traffic of nucleotide pyrophosphatase/phosphodiesterases in rice. Plant Cell Physiol 57:1610–1628. https://doi.org/10.1093/pcp/pcw089
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
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. https://doi.org/10.1105/tpc016675
Kelly AA, Kalisch B, Holzl G, Schulze S, Thiele J, Melzer M, Roston RL, Benning C, Dormann P (2016) Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana. Proc Natl Acad Sci USA 113:10714–10719. https://doi.org/10.1073/pnas.1609184113
Kennedy EP (1961) Biosynthesis of complex lipids. Fed Proc 20:934–940
Kikuchi S, Oishi M, Hirabayashi Y, Lee DW, Hwang I, Nakai M (2009) A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell 21:1781–1797. https://doi.org/10.1105/tpc.108.063552
Kim EH, 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. https://doi.org/10.1007/s11120-006-9126-0
Kirchhoff H, Mukherjee U, Galla HJ (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41:4872–4882
Kitajima A, Asatsuma S, Okada H, Hamada Y, Kaneko K, Nanjo Y, Kawagoe Y, Toyooka K, Matsuoka K, Takeuchi M, Nakano A, Mitsui T (2009) The rice alpha-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. Plant Cell 21:2844–2858. https://doi.org/10.1105/tpc.109.068288
Kobayashi K, Fujii S, Sato M, Toyooka K, Wada H (2015) Specific role of phosphatidylglycerol and functional overlaps with other thylakoid lipids in Arabidopsis chloroplast biogenesis. Plant Cell Rep 34:631–642. https://doi.org/10.1007/s00299-014-1719-z
Köhler RH, Hanson MR (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113(Pt 1):81–89
Koo AJ, Ohlrogge JB, Pollard M (2004) On the export of fatty acids from the chloroplast. J Biol Chem 279:16101–16110. https://doi.org/10.1074/jbc.M311305200
Kozjak-Pavlovic V (2017) The MICOS complex of human mitochondria. Cell Tissue Res 367:83–93. https://doi.org/10.1007/s00441-016-2433-7
Kunst L, Browse J, Somerville C (1988) Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc Natl Acad Sci USA 85:4143–4147
Kwok EY, Hanson MR (2004) Stromules and the dynamic nature of plastid morphology. J Microsc 214:124–137. https://doi.org/10.1111/j.0022-2720.2004.01317.x
Li Z, Gao J, Benning C, Sharkey TD (2012) Characterization of photosynthesis in Arabidopsis ER-to-plastid lipid trafficking mutants. Photosynth Res 112:49–61. https://doi.org/10.1007/s11120-012-9734-9
Li N, Gugel IL, Giavalisco P, Zeisler V, Schreiber L, Soll J, Philippar K (2015) FAX1, a novel membrane protein mediating plastid fatty acid export. PLoS Biol 13:e1002053. https://doi.org/10.1371/journal.pbio.1002053
Li N, Xu C, Li-Beisson Y, Philippar K (2016) Fatty acid and lipid transport in plant cells. Trends Plant Sci 21:145–158. https://doi.org/10.1016/j.tplants.2015.10.011
Li-Beisson Y et al (2013) Acyl-lipid metabolism. Arabidopsis Book 11:e0161. https://doi.org/10.1199/tab.0161
Li-Beisson Y, Neunzig J, Lee Y, Philippar K (2017) Plant membrane-protein mediated intracellular traffic of fatty acids and acyl lipids. Curr Opin Plant Biol 40:138–146. https://doi.org/10.1016/j.pbi.2017.09.006
Lindquist E, Solymosi K, Aronsson H (2016) Vesicles are persistent features of different plastids. Traffic 17:1125–1138. https://doi.org/10.1111/tra.12427
Lu B, Benning C (2009) A 25-amino acid sequence of the Arabidopsis TGD2 protein is sufficient for specific binding of phosphatidic acid. J Biol Chem 284:17420–17427
Lu B, Xu C, Awai K, Jones AD, Benning C (2007) A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J Biol Chem 282:35945–35953
Malherbe A, Block MA, Joyard J, Douce R (1992) Feedback inhibition of phosphatidate phosphatase from spinach chloroplast envelope membranes by diacylglycerol. J Biol Chem 267:23546–23553
Manjarrés IM, Alonso MT, García-Sancho J (2011) Calcium entry-calcium refilling (CECR) coupling between store-operated Ca(2+) entry and sarco/endoplasmic reticulum Ca(2+)-ATPase. Cell Calcium 49:153–161. https://doi.org/10.1016/j.ceca.2011.01.007
Marchive C, Nikovics K, To A, Lepiniec L, Baud S (2014) Transcriptional regulation of fatty acid production in higher plants: molecular bases and biotechnological outcomes. Eur J Lipid Sci Tech 116:1332–1343. https://doi.org/10.1002/ejlt.201400027
Marechal E, Bastien O (2014) Modeling of regulatory loops controlling galactolipid biosynthesis in the inner envelope membrane of chloroplasts. J Theor Biol 361:1–13. https://doi.org/10.1016/j.jtbi.2014.07.013
Marechal E, Block MA, Joyard J, Douce R (1994) Kinetic properties of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes. J Biol Chem 269:5788–5798
Marechal E, Miege C, Block MA, Douce R, Joyard J (1995) The catalytic site of monogalactosyldiacylglycerol synthase from spinach chloroplast envelope membranes. Biochemical analysis of the structure of the metal content. J Biol Chem 270:5714–5722
McConn M, Hugly S, Browse J, Somerville C (1994) A mutation at the fad8 locus of Arabidopsis identifies a second chloroplast [omega]-3 desaturase. Plant Physiol 106:1609–1614
Mehrshahi P, Stefano G, Andaloro JM, Brandizzi F, Froehlich JE, DellaPenna D (2013) Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. Proc Natl Acad Sci USA 110:12126–12131. https://doi.org/10.1073/pnas.1306331110
Michaud M, Gros V, Tardif M, Brugière S, Ferro M, Prinz William A, Toulmay A, Mathur J, Wozny M, Falconet D, Maréchal E, Block Maryse A, Jouhet J (2016) AtMic60 is involved in plant mitochondria lipid trafficking and is part of a large complex. Curr Biol 26:627–639. https://doi.org/10.1016/j.cub.2016.01.011
Miege C, Marechal E, Shimojima M, Awai K, Block MA, Ohta H, Takamiya K, Douce R, Joyard J (1999) Biochemical and topological properties of type A MGDG synthase, a spinach chloroplast envelope enzyme catalyzing the synthesis of both prokaryotic and eukaryotic MGDG. Eur J Biochem 265:990–1001
Miquel M, Browse J (1992) Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. J Biol Chem 267:1502–1509
Miquel M, Block MA, Joyard J, Dorne AJ, Dubacq JP, Kader JC, Douce R (1988) Protein-mediated transfer of phosphatidylcholine from liposomes to spinach chloroplast envelope membranes. Biochim Biophys 937:219–228. https://doi.org/10.1016/0005-2736(88)90244-1
Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228. https://doi.org/10.1126/science.1191803
Mongrand S, Besoule JJ, Cabantous F, Cassagne C (1998) The C16:3/C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry 49:1049–1064
Mongrand S, Cassagne C, Bessoule JJ (2000) Import of lyso-phosphatidylcholine into chloroplasts likely at the origin of eukaryotic plastidial lipids. Plant Physiol 122:845–852
Muthan B, Roston RL, Froehlich JE, Benning C (2013) Probing Arabidopsis chloroplast diacylglycerol pools by selectively targeting bacterial diacylglycerol kinase to suborganellar membranes. Plant Physiol 163:61–74. https://doi.org/10.1104/pp.113.222513
Nakamura Y (2013) Phosphate starvation and membrane lipid remodeling in seed plants. Prog Lipid Res 52:43–50. https://doi.org/10.1016/j.plipres.2012.07.002
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. https://doi.org/10.1074/jbc.M704385200
Nanjo Y, Oka H, Ikarashi N, Kaneko K, Kitajima A, Mitsui T, Munoz FJ, Rodriguez-Lopez M, Baroja-Fernandez E, Pozueta-Romero J (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-Golgi to the chloroplast through the secretory pathway. Plant Cell 18:2582–2592. https://doi.org/10.1105/tpc.105.039891
Natesan SKA, Sullivan JA, Gray JC (2005) Stromules: a characteristic cell-specific feature of plastid morphology. J Exp Bot 56:787–797. https://doi.org/10.1093/jxb/eri088
Okuda S, Freinkman E, Kahne D (2012) Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338:1214–1217. https://doi.org/10.1126/science.1228984
Oursel A, Escoffier A, Kader JC, Dubacq JP, Tremolieres A (1987) Last step in the cooperative pathway for galactolipid synthesis in spinach leaves—formation of monogalactosyldiacylglycerol with C18 polyunsaturated acyl-groups at both carbon-atoms of the glycerol. FEBS Lett 219:393–399. https://doi.org/10.1016/0014-5793(87)80259-4
Pain D, Kanwar YS, Blobel G (1988) Identification of a receptor for protein import into chloroplasts and its localization to envelope contact zones. Nature 331:232–237. https://doi.org/10.1038/331232a0
Pawley JB (1991) Fundamental and practical limits in confocal light microscopy. Scanning 13:184–198. https://doi.org/10.1002/sca.4950130205
Pérez-Sancho J, Vanneste S, Lee E, McFarlane HE, Esteban Del Valle A, Valpuesta V, Friml J, Botella MA, Rosado A (2015) The Arabidopsis synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol 168:132–143. https://doi.org/10.1104/pp.15.00260
Pérez-Sancho J, Tilsner J, Samuels AL, Botella MA, Bayer EM, Rosado A (2016) Stitching organelles: organization and function of specialized membrane contact sites. Plants Trends Cell Biol 26:705–717. https://doi.org/10.1016/j.tcb.2016.05.007
Phillips MJ, Voeltz GK (2016) Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol 17:69. https://doi.org/10.1038/nrm.2015.8
Prinz WA (2014) Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J Cell Biol 205:759–769. https://doi.org/10.1083/jcb.201401126
Qin X, Suga M, Kuang T, Shen JR (2015) Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348:989–995. https://doi.org/10.1126/science.aab0214
Quon E, Beh CT (2015) Membrane contact sites: complex zones for membrane association and lipid exchange. Lipid Insights 8:55–63. https://doi.org/10.4137/LPI.S37190
Reichert AS, Neupert W (2002) Contact sites between the outer and inner membrane of mitochondria—role in protein transport. Biochim Biophys Acta Mol Cell Res 1592:41–49. https://doi.org/10.1016/S0167-4889(02)00263-X
Renaudin S, Capdepon M (1977) Association of the endoplasmic reticulum and the plastids in Tozzia alpina L. scale leaves. J Ultrastruct Res 61:303–308. https://doi.org/10.1016/S0022-5320(77)80055-5
Rolland N, Ferro M, Seigneurin-Berny D, Garin J, Block M, Joyard J (2009) The chloroplast envelope proteome and lipidome. In: The chloroplast, vol 13. Plant cell monographs. Springer, Berlin, pp 41–88. https://doi.org/10.1007/978-3-540-68696-5_2
Rolland N, Curien G, Finazzi G, Kuntz M, Marechal E, Matringe M, Ravanel S, Seigneurin-Berny D (2012) The biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes. Annu Rev Genet 46:233–264. https://doi.org/10.1146/annurev-genet-110410-132544
Roston R, Gao J, Xu C, Benning C (2011) Arabidopsis chloroplast lipid transport protein TGD2 disrupts membranes and is part of a large complex. Plant J 66:759–769. https://doi.org/10.1111/j.1365-313X.2011.04536.x
Roston RL, Gao JP, Murcha MW, Whelan J, Benning C (2012) TGD1,-2, and-3 proteins involved in lipid trafficking form ATP-binding cassette (ABC) transporter with multiple substrate-binding proteins. J Biol Chem 287:21406–21415. https://doi.org/10.1074/jbc.M112.370213
Roston RL, Hurlock AK, Benning C (2014) Plastidic ABC proteins. In: Geisler M (ed) Plant ABC transporters, vol 22. Signaling and communication in plants. Springer International Publishing, Berlin, pp 103–136. https://doi.org/10.1007/978-3-319-06511-3_7
Roughan PG, Slack CR (1982) Cellular organization of glycerolipid metabolism. Annu Rev Plant Physiol 33:97–132
Saravanan RS, Slabaugh E, Singh VR, Lapidus LJ, Haas T, Brandizzi F (2009) The targeting of the oxysterol-binding protein ORP3a to the endoplasmic reticulum relies on the plant VAP33 homolog PVA12. Plant J 58:817–830. https://doi.org/10.1111/j.1365-313X.2009.03815.x
Sastri M, Darshi M, Mackey M, Ramachandra R, Ju S, Phan S, Adams S, Stein K, Douglas CR, Kim JJ, Ellisman MH, Taylor SS, Perkins GA (2017) Sub-mitochondrial localization of the genetic-tagged mitochondrial intermembrane space-bridging components Mic19, Mic60 and Sam50. J Cell Sci 130:3248–3260. https://doi.org/10.1242/jcs.201400
Schattat M, Barton K, Baudisch B, Klösgen RB, Mathur J (2011a) Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiol 155:1667–1677. https://doi.org/10.1104/pp.110.170480
Schattat M, Barton K, Mathur J (2011b) Correlated behavior implicates stromules in increasing the interactive surface between plastids and ER tubules. Plant Signal Behav 6:715–718. https://doi.org/10.4161/psb.6.5.15085
Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, Wenk MR, Camilli PD, Reinisch KM (2014) Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510:552. https://doi.org/10.1038/nature13269
Schnell DJ, Blobel G (1993) Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J Cell Biol 120:103–115. https://doi.org/10.1083/jcb.120.1.103
Schnell DJ, Blobel G, Pain D (1990) The chloroplast import receptor is an integral membrane protein of chloroplast envelope contact sites. J Cell Biol 111:1825–1838
Schnurr JA, Shockey JM, de Boer GJ, Browse JA (2002) Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol 129:1700–1709
Schumann U, Prestele J, O’Geen H, Brueggeman R, Wanner G, Gietl C (2007) Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proc Natl Acad Sci USA 104:1069–1074. https://doi.org/10.1073/pnas.0610402104
Schwertner HA, Biale JB (1973) Lipid composition of plant mitochondria and of chloroplasts. J Lipid Res 14:235–242
Seifert U, Heinz E (1992) Enzymatic characteristics of UDP-sulfoquinovose: diacylglycerol sulfoquinovosyltransferase from chloroplast envelopes. Bot Acta 105:197–205. https://doi.org/10.1111/j.1438-8677.1992.tb00287.x
Shaw G (1996) The pleckstrin homology domain: an intriguing multifunctional protein module. BioEssays 18:35–46. https://doi.org/10.1002/bies.950180109
Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD (2011) Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144:389–401. https://doi.org/10.1016/j.cell.2010.12.034
Sun Q, Zybailov B, Majeran W, Friso G, Olinares PDB, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucleic Acids Res 37:D969–D974. https://doi.org/10.1093/Nar/Gkn654
Szabadkai G, Bianchi K, Várnai P, De Stefani D, Wieckowski MR, Cavagna D, Nagy AI, Balla T, Rizzuto R (2006) Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol 175:901–911. https://doi.org/10.1083/jcb.200608073
Tan XL, Wang QY, Tian BX, Zhang HA, Lu DL, Zhou J (2011) A Brassica napus lipase locates at the membrane contact sites involved in chloroplast development. PLoS ONE. https://doi.org/10.1371/journal.pone.0026831
Tanoue R, Kobayashi M, Katayama K, Nagata N, Wada H (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. https://doi.org/10.1016/j.febslet.2014.03.010
Tavassoli S, Chao JT, Young BP, Cox RC, Prinz WA, de Kroon AIPM, Loewen CJR (2013) Plasma membrane–endoplasmic reticulum contact sites regulate phosphatidylcholine synthesis. EMBO Rep 14:434–440. https://doi.org/10.1038/embor.2013.36
Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62:2349–2361. https://doi.org/10.1093/jxb/err079
Thong S, Ercan B, Torta F, Fong ZY, Wong HY, Wenk MR, Chng SS (2016) Defining key roles for auxiliary proteins in an ABC transporter that maintains bacterial outer membrane lipid asymmetry. Elife. https://doi.org/10.7554/eLife.19042
Tjellström H, Andersson MX, Larsson KE, Sandelius AS (2008) Membrane phospholipids as a phosphate reserve: the dynamic nature of phospholipid-to-digalactosyl diacylglycerol exchange in higher plants. Plant Cell Environ 31:1388–1398. https://doi.org/10.1111/j.1365-3040.2008.01851.x
Tong J, Yang H, Yang H, Eom SH, Im YJ (2013) Structure of Osh3 reveals a conserved mode of phosphoinositide binding in oxysterol-binding proteins. Structure 21:1203–1213. https://doi.org/10.1016/j.str.2013.05.007
Troncoso-Ponce MA, Nikovics K, Marchive C, Lepiniec L, Baud S (2016) New insights on the organization and regulation of the fatty acid biosynthetic network in the model higher plant Arabidopsis thaliana. Biochimie 120:3–8. https://doi.org/10.1016/j.biochi.2015.05.013
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature 473:55–60. https://doi.org/10.1038/Nature09913
Vigani G, Faoro F, Ferretti AM, Cantele F, Maffi D, Marelli M, Maver M, Murgia I, Zocchi G (2015) Three-dimensional reconstruction, by TEM tomography, of the ultrastructural modifications occurring in Cucumis sativus L. mitochondria under Fe deficiency. PLoS ONE 10:e0129141. https://doi.org/10.1371/journal.pone.0129141
Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rollands N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7:1224–1231
Vismans G, van der Meer T, Langevoort O, Schreuder M, Bouwmeester H, Peisker H, Dörman P, Ketelaar T, van der Krol A (2016) Low-phosphate induction of plastidal stromules is dependent on strigolactones but not on the canonical strigolactone signaling component MAX2. Plant Physiol 172:2235–2244. https://doi.org/10.1104/pp.16.01146
Wada H, Murata N (1989) Synechocystis Pcc6803 mutants defective in desaturation of fatty-acids. Plant Cell Physiol 30:971–978
Waese J, Fan J, Pasha A, Yu H, Fucile G, Shi R, Cumming M, Kelley LA, Sternberg MJ, Krishnakumar V, Ferlanti E, Miller J, Town C, Stuerzlinger W, Provart NJ (2017) ePlant: visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell 29:1806–1821. https://doi.org/10.1105/tpc.17.00073
Wang Z, Xu CC, Benning C (2012) TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J 70:614–623. https://doi.org/10.1111/j.1365-313X.2012.04900.x
Wang Z, Anderson NS, Benning C (2013) The phosphatidic acid binding site of the Arabidopsis trigalactosyldiacylglycerol 4 (TGD4) protein required for lipid import into chloroplasts. J Biol Chem 288:4763–4771. https://doi.org/10.1074/jbc.M112.438986
Warakanont J, Tsai CH, Michel EJ, Murphy GR 3rd, Hsueh PY, Roston RL, Sears BB, Benning C (2015) Chloroplast lipid transfer processes in Chlamydomonas reinhardtii involving a TRIGALACTOSYLDIACYLGLYCEROL 2 (TGD2) orthologue. Plant J 84:1005–1020. https://doi.org/10.1111/tpj.13060
Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J 363:657–666
Wink M (1993) The plant vacuole: a multifunctional compartment. J Exp Bot 44:231–246
Xu C, Fan J, Riekhof W, Froehlich JE, Benning C (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 22:2370–2379
Xu C, Fan J, Froehlich J, Awai K, Benning C (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17:3094–3110
Xu C, Fan J, Cornish AJ, Benning C (2008) Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein. Plant Cell 20:2190–2204
Yin C, Andersson MX, Zhang H, Aronsson H (2015) Phosphatidylcholine is transferred from chemically-defined liposomes to chloroplasts through proteins of the chloroplast outer envelope membrane. FEBS Lett 589:177–181. https://doi.org/10.1016/j.febslet.2014.11.044
Yu B, Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36:762–770
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
Zhang C, Hicks GR, Raikhel NV (2014) Plant vacuole morphology and vacuolar trafficking. Front Plant Sci 5:476. https://doi.org/10.3389/fpls.2014.00476
Zhao L, Katavic V, Li F, Haughn GW, Kunst L (2010) Insertional mutant analysis reveals that long-chain acyl-CoA synthetase 1 (LACS1), but not LACS8, functionally overlaps with LACS9 in Arabidopsis seed oil biosynthesis. Plant J 64:1048–1058. https://doi.org/10.1111/j.1365-313X.2010.04396.x
Zou Z, Tong F, Faergeman NJ, Borsting C, Black PN, DiRusso CC (2003) Vectorial acylation in Saccharomyces cerevisiae. Fat1p and fatty acyl-CoA synthetase are interacting components of a fatty acid import complex. J Biol Chem 278:16414–16422. https://doi.org/10.1074/jbc.M210557200
Acknowledgements
We gratefully acknowledge all authors who contributed to our current understanding of chloroplast lipid transport, and apologize to those whom we did not cite directly due to space limits. RR was partially funded by United States Department of Agriculture NIFA Grant 2016-67013-24613.
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LaBrant, E., Barnes, A.C. & Roston, R.L. Lipid transport required to make lipids of photosynthetic membranes. Photosynth Res 138, 345–360 (2018). https://doi.org/10.1007/s11120-018-0545-5
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DOI: https://doi.org/10.1007/s11120-018-0545-5