Lipids in Plant Mitochondria

  • Radin SadreEmail author
  • Margrit Frentzen
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 30)


Mitochondria perform a variety of fundamental functions and are of pivotal importance in plant physiology and development. They possess a typical membrane lipid composition that is largely conserved in all eukaryotes. To establish and maintain their lipid pattern, they have to cooperate with other organelles, where a significant portion of their lipids are produced and subsequently assembled into the mitochondrial membranes. Certain lipids are, however, synthesized by the mitochondria themselves. Recent data provide new insight into the mitochondrial lipid biosynthetic pathways and the importance of their reaction products for mitochondrial structure and function. Mitochondrial de novo fatty acid synthesis, for instance, produces the precursor for the formation of lipoate, a sulfur-containing cofactor of several mitochondrial multi-enzyme complexes. This pathway has been shown to be indispensable for photoautotrophic growth of C3 plants to meet the high demand of lipoylated glycine decarboxylase complexes catalyzing a key step in photorespiration. Polyprenyl diphosphates are channeled into mitochondrial ubiquinone synthesis by a para-hydroxybenzoate prenyltransferase. The central role of ubiquinone in oxidative phosphorylation is reflected in the embryo-lethal phenotype of plant mutants lacking mitochondrial prenyltransferase activity. In addition, de novo glycerolipid synthesis results in the formation of phosphatidylglycerol and cardiolipin, the typical mitochondrial membrane lipid with a unique tetraacyl structure. Mitochondria were found to require a defined level of these anionic lipids for proper structural integrity and function. Hereby phosphati-dylglycerol can partly substitute cardiolipin. Cardiolipin is, however, essential for optimal mitochondrial functions and for maintaining mitochondrial activities under unfavorable conditions. Furthermore, cardioli-pin has been shown to play a decisive role in controlling the dynamic equilibrium between mitochondrial fission and fusion and is indispensable for proper plant development.


Phosphatidic Acid Lipoic Acid Plant Mitochondrion Isopentenyl Diphosphate Dimethylallyl Diphosphate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Acyl carrier protein


Cytidine 5′-diphosphate-diacylglycerol






Endoplasmic reticulum




Isopente-nyl diphosphate isomerase


β-Ketoacyl acyl carrier protein synthase


Lysophosphatidic acid, 1-acylglyc-erol-3-phosphate


Mitochondrial β-ketoacyl acyl carrier protein synthase




Phosphatidic acid















We are indebted to K. Katayama, S. Tanabashi, N. Nagata and H. Wada for sharing unpublished data and K. Katayama and H. Wada for providing us with Fig. 5. The work conducted in the authors' laboratory was supported by Deutsche Forschungsgemeinschaft.


  1. Ardail D, Popa I, Alcantara K, Pons A, Zanetta J P, Louisot P, Thomas L and Portoukalian J (2001) Occurrence of cera-mides and neutral glycolipids with unusual long-chain base composition in purified rat liver mitochondria. FEBS Lett 488: 160–164PubMedCrossRefGoogle Scholar
  2. Arimura S and Tsutsumi N (2005) Plant mitochondrial fission and fusion. Plant Biotechnol 22: 415–418CrossRefGoogle Scholar
  3. Athenstaedt K and Daum G (1999) Phosphatidic acid, a key intermediate in lipid metabolism. Eur J Biochem 266: 1–16PubMedCrossRefGoogle Scholar
  4. Avelange-Macherel MH and Joyard J (1998) Cloning and functional expression of AtCOQ3, the Arabidopsis homo-logue of the yeast COQ3 gene, encoding a methyltrans-ferase from plant mitochondria involved in ubiquinone biosynthesis. Plant J 14: 203–213PubMedCrossRefGoogle Scholar
  5. Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M and Kushnir S (2003) Arabidopsis phosphatidylglycerophos-phate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33: 899–909PubMedCrossRefGoogle Scholar
  6. Bayir H, Fadeel B, Palladino MJ, Witasp E, Kurnikov I V, Tyurina YY, Tyurin VA, Amoscato AA, Jiang J, Kochanek PM, DeKosky ST, Greenberger JS, Shvedova AA and Kagan VE (2006) Apoptotic interactions of cytochrome c: redox flirting with anionic phospholipids within and outside of mitochondria. Biochim Biophys Acta 1757: 648–659PubMedCrossRefGoogle Scholar
  7. Beranek A, Rechberger G, Knauer H, Wolinski H, Kohlwein SD and Leber R (2009) Identification of a cardiolipin-specific phospholipase encoded by the gene CLD1 (YGR110W) in yeast. J Biol Chem,
  8. Beisson F, Koo AJK, Ruuska S, Schwender J, Pollard M, Thelen JJ, Paddock T, Salas JJ, Savage L, Milcamps A, Mhaske VB, Cho Y and Ohlrogge JB (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol 132: 681–697PubMedCrossRefGoogle Scholar
  9. Birner R, Bürgermeister M, Schneiter R and Daum G (2001) Roles of phosphatidylethanolamine and of its several biosynthetic pathways in Saccharomyces cerevisiae. Mol Biol Cell 12: 997–1007PubMedGoogle Scholar
  10. Bouvier F, Rahier A and Camara B (2005) Biogenesis, molecular regulation and function of plant isoprenoids. Prog Lipid Res 44: 357–429PubMedCrossRefGoogle Scholar
  11. Brandner K, Mick DU, Frazier AE, Taylor RD, Meisinger C and Rehling P (2005) Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth syndrome. Mol Biol Cell 16: 5202–5214PubMedCrossRefGoogle Scholar
  12. Caiveau O, Fortune D, Cantrel C, Zachowski A and Moreau F (2001) Consequences of ω-6-oleate desaturase deficiency on lipid dynamics and functional properties of mitochondrial membranes of Arabidopsis thaliana. J Biol Chem 276: 5788–5794PubMedCrossRefGoogle Scholar
  13. Campbell M, Hahn FM, Poulter CD and Leustek T (1998) Analysis of the isopentenyl diphosphate isomerase gene family from Arabidopsis thaliana. Plant Mol Biol 36: 323–328PubMedCrossRefGoogle Scholar
  14. Chang SC, Heacock PN, Clancey CJ and Dowhan W (1998a) The PEL1 gene (renamed PGS1) encodes the phosphati-dylglycerophosphate synthase of Saccharomyces cerevi-siae. J Biol Chem 273: 9829–9836CrossRefGoogle Scholar
  15. Chang SC, Heacock PN, Mileykovskaya E, Voelker DR and Dowhan W (1998b) Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharo-myces cerevisiae. J Biol Chem 273: 14933–14941CrossRefGoogle Scholar
  16. Chen D, Zhang XY and Shi Y (2006) Identification and functional characterization of hCLS1, a human cardiolipin syn-thase localized in mitochondria. Biochem J 398: 169–176PubMedCrossRefGoogle Scholar
  17. Chen S, He Q and Greenberg ML (2008a) Loss of tafazzin in yeast leads to increased oxidative stress during respiratory growth. Mol Microbiol 68: 1061–1072CrossRefGoogle Scholar
  18. Chen S, Tarsi M, Kane PM and Greenberg ML (2008b) Car-diolipin mediates cross-talk between mitochondria and the vacuole. Mol Biol Cell 19: 5047–5058CrossRefGoogle Scholar
  19. Choi SY, Huang P, Jenkins GM, Chan DC, Schiller J and Frohman MA (2006) A common lipid links Mfn-medi-ated mitochondrial fusion and SNARE-regulated exocy-tosis. Nat Cell Biol 8: 1255–1262PubMedCrossRefGoogle Scholar
  20. Choi SY, Gonzalvez F, Jenkins GM, Slomianny C, Chretien D, Arnoult D, Petit PX and Frohman MA (2007) Cardi-olipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Differ 14: 597–606PubMedCrossRefGoogle Scholar
  21. Christensen CE, Kragelund BB, von Wettstein-Knowles P and Henriksen A (2007) Structure of the human β-ketoacyl [ACP] synthase from the mitochondrial type II fatty acid synthase. Protein Sci 16: 261–272PubMedCrossRefGoogle Scholar
  22. Chuman L and Brody S (1989) Acyl carrier protein is present in the mitochondria of plants and eucaryotic micro-organisms. Eur J Biochem 184: 643–649PubMedCrossRefGoogle Scholar
  23. Clancey CJ, Chang SC and Dowhan W (1993) Cloning of a gene (PSD1) encoding phosphatidylserine decarboxylase from Saccharomyces cerevisiae by complementation of an Escherichia coli mutant. J Biol Chem 268: 24580–24590PubMedGoogle Scholar
  24. Claypool SM, McCaffery JM and Koehler CM (2006) Mito-chondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J Cell Biol 174: 379–390PubMedCrossRefGoogle Scholar
  25. Cunillera N, Boronat A and Ferrer A (1997) The Arabidop-sis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 272: 15381–15388PubMedCrossRefGoogle Scholar
  26. Cunningham FX Jr and Gantt E (2000) Identification of multi-gene families encoding isopentenyl diphosphate isomerase in plants by heterologous complementation in Escherichia coli. Plant Cell Physiol 41: 119–123PubMedCrossRefGoogle Scholar
  27. Daum G and Vance JE (1997) Import of lipids into mitochondria. Prog Lipid Res 36: 103–130PubMedCrossRefGoogle Scholar
  28. de Andrade Rosa I, Einicker-Lamas M, Roney Bernardo R, Previatto LM, Mohana-Borges R, Morgado-Díaz JA and Benchimol M (2006) Cardiolipin in hydrogenosomes: evidence of symbiotic origin. Eukaryot Cell 5: 784–787CrossRefGoogle Scholar
  29. Disch A, Hemmerlin A, Bach TJ and Rohmer M (1998) Mevalonate-derived isopentenyl diphosphate is the biosyn-thetic precursor of ubiquinone prenyl side chain in tobacco BY-2 cells. Biochem J 331: 615–621PubMedGoogle Scholar
  30. Dorne AJ and Heinz E (1989) Position and pairing of fatty acids in phosphatidylglycerol from pea leaf chloroplasts and mitochondria. Plant Sci 60: 39–46CrossRefGoogle Scholar
  31. Douce R (1985) Mitochondria in Higher Plants: Structure, Function and Biogenesis. Academic Press, New YorkGoogle Scholar
  32. Douce R, Bourguignon J, Neuburger M and Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6: 167–176PubMedCrossRefGoogle Scholar
  33. Dowhan W (1997) Molecular basis for membrane phosphol-ipid diversity: why are there so many lipids? Annu Rev Biochem 66: 199–232PubMedCrossRefGoogle Scholar
  34. Dzugasová V, Obernauerová M, Horváthová K, Vachová M, Záková M, Subík J (1998) Phosphatidylglycerol-phosphate synthase encoded by the PEL1/PGS1 gene in Saccharomyces cerevisiae is localized in mitochondria and its expression is regulated by phospholipid precursors. Curr Genet 34: 297–302Google Scholar
  35. Edman K and Ericson I (1987) Phospholipid and fatty acid composition in mitochondria from spinach (Spinacia oleracea) leaves and petioles. A comparative study. Biochem J 243: 575–558Google Scholar
  36. Epand RF, Schlattner U, Wallimann T, Lacombe ML and Epand RM (2007a) Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Biophys J 92: 126–137CrossRefGoogle Scholar
  37. Epand RF, Tokarska-Schlattner M, Schlattner U, Wallimann T and Epand RM (2007b) Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J Mol Biol 365: 968–980CrossRefGoogle Scholar
  38. Ewald R, Kolukisaoglu U, Bauwe U, Mikkat S and Bauwe H (2007) Mitochondrial protein lipoylation does not exclusively depend on the mtKAS pathway of de novo fatty acid synthesis in Arabidopsis. Plant Physiol 145: 41–48PubMedCrossRefGoogle Scholar
  39. Focke M, Gieringer E, Schwan S, Jänsch L, Binder S and Braun HP (2003) Fatty acid biosynthesis in mitochondria of grasses: malonyl-coenzyme A is generated by a mitochondrial-localized acetyl-coenzyme A carboxylase. Plant Physiol 133: 875–884PubMedCrossRefGoogle Scholar
  40. Frentzen M (2004) Phosphatidylglycerol and sulfoquinovo-syldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7: 270–276PubMedCrossRefGoogle Scholar
  41. Frentzen M and Griebau R (1994) Biosynthesis of cardioli-pin in plant mitochondria. Plant Physiol 106: 1527–1532PubMedGoogle Scholar
  42. Frentzen M, Neuburger M, Joyard J and Douce R (1990) Intraorganelle localisation and substrate specificities of the mitochondrial acyl-CoA:sn-glycerol-3-phosphate O-acyltransferase and acyl-CoA:1-acyl-sn-glycerol-3-phosphate O-acyltransferase from potato tubers and pea leaves. Eur J Biochem 187: 395–402PubMedCrossRefGoogle Scholar
  43. Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA and Phinney BS (2003) Proteomic study of the Arabidopsis thaliana chloroplas-tic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J Proteome Res 2: 413–425PubMedCrossRefGoogle Scholar
  44. Gohil VM, Hayes P, Matsuyama S, Schägger H, Schlame M and Greenberg ML (2004) Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J Biol Chem 279: 42612–42618PubMedCrossRefGoogle Scholar
  45. Gonzalez-Baró MR, Lewin TM and Coleman RA (2007) Regulation of triglyceride metabolism. II. Function of mitochondrial GPAT1 in the regulation of triacylglycerol biosynthesis and insulin action. Am J Physiol Gastrointest Liver Physiol 292: G1195–G1199PubMedCrossRefGoogle Scholar
  46. Gonzalvez F and Gottlieb E (2007) Cardiolipin: setting the beat of apoptosis. Apoptosis 12: 877–885PubMedCrossRefGoogle Scholar
  47. Griebau R and Frentzen M (1994) Biosynthesis of phos-phatidylglycerol in isolated mitochondria of etiolated mung bean (Vigna radiata L.) seedlings. Plant Physiol 105: 1269–1274PubMedGoogle Scholar
  48. Gu Z, Valianpour F, Chen S, Vaz FM, Hakkaart GA, Wanders RJ and Greenberg ML (2004) Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome. Mol Microbiol 51: 149–158PubMedCrossRefGoogle Scholar
  49. Gueguen V, Macherel D, Jaquinod M, Douce R and Bour-guignon J (2000) Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J Biol Chem 275: 5016–5025PubMedCrossRefGoogle Scholar
  50. Guillot-Salomon T, Remy R, Cantrel C, Demandre C and Moreau F (1997) Phospholipids and polypeptides in the outer membrane of maize mitochondria. Phytochemistry 44: 29–34CrossRefGoogle Scholar
  51. Hackstein JH, Tjaden J and Huynen M (2006) Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50: 225–245PubMedCrossRefGoogle Scholar
  52. Hagio M, Sakurai I, Sato S, Kato T, Tabata S and Wada H (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43: 1456–1464PubMedCrossRefGoogle Scholar
  53. Haines TH and Dencher NA (2002) Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett 528: 35–39PubMedCrossRefGoogle Scholar
  54. Han X, Yang J, Cheng H, Yang K, Abendschein DR and Gross RW (2005) Shotgun lipidomics identifies cardi-olipin depletion in diabetic myocardium linking altered substrate utilization with mitochondrial dysfunction. Biochemistry. 44: 16684–16694PubMedCrossRefGoogle Scholar
  55. Hatch GM, Gu Y, Xu FY, Cizeau J, Neumann S, Park JS, Loewen S and Mowat MR (2008) StARD13(Dlc-2) RhoGap mediates ceramide activation of phosphatidylg-lycerolphosphate synthase and drug response in Chinese hamster ovary cells. Mol Biol Cell 19: 1083–1092PubMedCrossRefGoogle Scholar
  56. He Q and Greenberg ML (2004) Post-translational regulation of phosphatidylglycerolphosphate synthase in response to inositol. Mol Microbiol 53: 1243–1249PubMedCrossRefGoogle Scholar
  57. Heazlewood JL, Howell KA, Whelan J and Millar AH (2003) Towards an analysis of the rice mitochondrial proteome. Plant Physiol 132: 230–242PubMedCrossRefGoogle Scholar
  58. Heazlewood JL, Tonti-Filippini J, Verboom RE and Millar AH (2005) Combining experimental and predicted datasets for determination of the subcellular location of proteins in Arabidopsis. Plant Physiol 139: 598–609PubMedCrossRefGoogle Scholar
  59. Hiltunen JK, Okubo F, Kursu VA, Autio KJ and Kastaniotis AJ (2005) Mitochondrial fatty acid synthesis and maintenance of respiratory competent mitochondria in yeast. Biochem Soc Trans 33: 1162–1165PubMedCrossRefGoogle Scholar
  60. Hirooka K, Bamba T, Fukusaki E and Kobayashi A (2003) Cloning and kinetic characterization of Arabidopsis thal-iana solanesyl diphosphate synthase. Biochem J 370: 679–686PubMedCrossRefGoogle Scholar
  61. Houtkooper RH, Akbari H, van Lenthe H, Kulik W, Wanders RJA, Frentzen M and Vaz FM (2006) Identification and characterization of human cardiolipin synthase. FEBS Lett 580: 3059–3064PubMedCrossRefGoogle Scholar
  62. Huang Z, Jiang J, Tyurin VA, Zhao Q, Mnuskin A, Ren J, Belikova NA, Feng W, Kurnikov IV and Kagan VE (2008) Cardiolipin deficiency leads to decreased cardi-olipin peroxidation and increased resistance of cells to apoptosis. Free Radic Biol Med 44: 1935–1944PubMedCrossRefGoogle Scholar
  63. Ikeda M and Kagei K (1979) Ubiquinone content of eight plant species in cell culture. Phytochemistry 18: 1577–1578CrossRefGoogle Scholar
  64. Inglis-Broadgate SL, Ocaka L, Banerjee R, Gaasenbeek M, Chapple JP, Cheetham ME, Clark BJ, Hunt DM and Halford S (2005) Isolation and characterization of murine CDS (CDP-diacylglycerol synthase) 1 and 2. Gene 356: 19–31PubMedCrossRefGoogle Scholar
  65. Jiang F, Rizavi HS and Greenberg ML (1997) Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources. Mol Microbiol 26: 481–491PubMedCrossRefGoogle Scholar
  66. Jiang F, Ryan MT, Schlame M, Zhao M, Gu Z, Klingenberg M, Pfanner N and Greenberg ML (2000) Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochon-drial function. J Biol Chem 275: 22387–22394PubMedCrossRefGoogle Scholar
  67. Joshi AS, Zhou J, Gohil VM, Chen S and Greenberg ML (2009) Cellular functions of cardiolipin in yeast. Biochim Biophys Acta 1793: 212–218PubMedCrossRefGoogle Scholar
  68. Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J and Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167: 863–874PubMedCrossRefGoogle Scholar
  69. Jouhet J, Maréchal E and Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Prog Lipid Res 46: 37–55PubMedCrossRefGoogle Scholar
  70. Kang SG, Jeong HK, Lee E and Natarajan S (2007) Characterization of a lipoate-protein ligase A gene of rice (Oryza sativa L.). Gene 393: 53–61PubMedCrossRefGoogle Scholar
  71. Katayama K, Sakurai I and Wada H (2004) Identification of an Arabidopsis thaliana gene for cardiolipin synthase located in the mitochondria. FEBS Lett 577: 193–198PubMedCrossRefGoogle Scholar
  72. Kawamukai M (2002) Biosynthesis, bioproduction and novel roles of ubiquinone. J Biosci Bioeng 94: 511–517PubMedGoogle Scholar
  73. Kawasaki K, Kuge O, Chang SC, Heacock PN, Rho M, Suzuki K, Nishijima M and Dowhan W (1999) Isolation of a Chinese hamster ovary (CHO) cDNA encoding phos-phatidylglycerophosphate (PGP) synthase, expression of which corrects the mitochondrial abnormalities of a PGP synthase-defective mutant of CHO-K1 cells. J Biol Chem 274: 1828–1834PubMedCrossRefGoogle Scholar
  74. Kim HU and Huang AH (2004) Plastid lysophosphatidyl acyltransferase is essential for embryo development in Arabidopsis. Plant Physiol 134: 1206–1216PubMedCrossRefGoogle Scholar
  75. Kim HU, Li Y and Huang AH (2005) Ubiquitous and endo-plasmic reticulum-located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell 17: 1073–1089PubMedCrossRefGoogle Scholar
  76. Kleppinger-Sparace KF and Moore TS Jr (1985) Biosynthesis of cytidine 5′-diphosphate-diacylglycerol in endoplas-mic reticulum and mitochondria of castor bean endosperm. Plant Physiol 77: 12–15PubMedCrossRefGoogle Scholar
  77. Kobayashi K, Suzuki M, Tang J, Nagata N, Ohyama K, Seki H, Kiuchi R, Kaneko Y, Nakazawa M, Matsui M, Matsumoto S, Yoshida S and Muranaka T (2007) Lovastatin insensitive 1, a novel pentatricopeptide repeat protein, is a potential regulatory factor of isoprenoid biosynthesis in Arabidopsis. Plant Cell Physiol 48: 322–331PubMedCrossRefGoogle Scholar
  78. Kopka J, Ludewig M and Müller-Röber B (1997) Complementary DNAs encoding eukaryotic-type cytidine-5′-diphosphate-diacylglycerol synthases of two plant species. Plant Physiol 13: 997–1002CrossRefGoogle Scholar
  79. Koshkin V and Greenberg ML (2002) Cardiolipin prevents rate-dependent uncoupling and provides osmotic stability in yeast mitochondria. Biochem J 364: 317–322PubMedGoogle Scholar
  80. Kuge O, Nishijima M and Akamatsu Y (1991) A cloned gene encoding phosphatidylserine decarboxylase complements the phosphatidylserine biosynthetic defect of a Chinese hamster ovary cell mutant. J Biol Chem 266: 6370–6376PubMedGoogle Scholar
  81. Lange C, Nett JH, Trumpower BL and Hunte C (2001) Specific roles of protein-phospholipid interactions in the yeast cyto-chrome bc 1 complex structure. EMBO J 20: 6591–6600PubMedCrossRefGoogle Scholar
  82. Lester RL and Crane FL (1959) The natural occurrence of coenzyme Q and related compounds. J Biol Chem 234: 2169–2175PubMedGoogle Scholar
  83. Liang PH, Ko TP and Wang AH (2002) Structure, mechanism and function of prenyltransferases. Eur J Biochem 269: 3339–3354PubMedCrossRefGoogle Scholar
  84. Liu J, Chen J, Dai Q and Lee RM (2003a) Phospholipid scramblase 3 is the mitochondrial target of protein kinase C δ-induced apoptosis. Cancer Res 63: 1153–1156Google Scholar
  85. Liu J, Dai Q, Chen J, Durrant D, Freeman A, Liu T, Grossman D and Lee RM (2003b) Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response. Mol Cancer Res 1: 892–902Google Scholar
  86. Logan DC (2006) The mitochondrial compartment. J Exp Bot 57: 1225–1243PubMedCrossRefGoogle Scholar
  87. Lu B, Xu F, Jiang YJ, Choy PC, Hatch GM, Grunfeld C and Feingold KR (2006) Cloning and characterization of a cDNA encoding human cardiolipin synthase (hCLS1). J Lipid Res 47: 1140–1145PubMedCrossRefGoogle Scholar
  88. Lütke-Brinkhaus F, Liedvogel B and Kleinig H (1984) On the biosynthesis of ubiquinones in plant mitochondria. Eur J Biochem 141: 537–541PubMedCrossRefGoogle Scholar
  89. Lykidis A, Jackson PD, Rock CO and Jackowski S (1997) The role of CDP-diacylglycerol synthetase and phos-phatidylinositol synthase activity levels in the regulation of cellular phosphatidylinositol content. J Biol Chem 272: 33402–33409PubMedCrossRefGoogle Scholar
  90. Manella CA and Bonner WD Jr (1975) Biochemical characteristics of the outer membranes of plant mitochondria. Biochim Biophys Acta 413: 213–225CrossRefGoogle Scholar
  91. Manzano D, Busquets A, Closa M, Hoyerová K, Schaller H, Kamínek M, Arró M and Ferrer A (2006) Overexpression of farnesyl diphosphate synthase in Arabidopsis mitochondria triggers light-dependent lesion formation and alters cytokinin homeostasis. Plant Mol Biol 61: 195–213PubMedCrossRefGoogle Scholar
  92. McKenzie M, Lazarou M, Thorburn DR and Ryan MT (2006) Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients. J Mol Biol 361: 462–469PubMedCrossRefGoogle Scholar
  93. Meance J, Duperon P and Duperon R (1976) Répartition des substances stéroliques à l'intérieur des mitochondries de l'inforescence de chou fleur. Physiol Veg 14: 746–755Google Scholar
  94. Meyer EH, Heazlewood JL and Millar AH (2007) Mito-chondrial acyl carrier proteins in Arabidopsis thaliana are predominantly soluble matrix proteins and none can be confirmed as subunits of respiratory complex I. Plant Mol Biol 64: 319–327PubMedCrossRefGoogle Scholar
  95. Mizoi J, Nakamura M and Nishida I (2006) Defects in CTP:phosphorylethanolamine cytidylyltransferase affect embryonic and postembryonic development in Arabidop-sis. Plant Cell 18: 3370–3385PubMedCrossRefGoogle Scholar
  96. Moore TS (1982) Phospholipid biosynthesis. Annu Rev Plant Physiol 33: 235–259CrossRefGoogle Scholar
  97. Müller F and Frentzen M (2001) Phosphatidylglycerophos-phate synthases from Arabidopsis thaliana. FEBS Lett 509: 298–302PubMedCrossRefGoogle Scholar
  98. Nerlich A, von Orlow M, Rontein D, Hanson AD and Dör-mann P (2007) Deficiency in phosphatidylserine decar-boxylase activity in the psd1 psd2 psd3 triple mutant of Arabidopsis affects phosphatidylethanolamine accumulation in mitochondria. Plant Physiol 144: 904–914PubMedCrossRefGoogle Scholar
  99. Neupert W and Herrmann JM (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76: 723–749PubMedCrossRefGoogle Scholar
  100. Noctor G, De Paepe R and Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12: 125–134PubMedCrossRefGoogle Scholar
  101. Nowicki M, Müller F and Frentzen M (2005) Cardioli-pin synthase of Arabidopsis thaliana. FEBS Lett 579: 2161–2165PubMedCrossRefGoogle Scholar
  102. Nunes-Nesi A and Fernie AR (2008) Mitochondrial metabolism. In: Logan DC (ed) Plant Mitochondria, Ann Plant Rev, Vol 31, pp 212–277. Blackwell, OxfordGoogle Scholar
  103. Nunes-Nesi A, Sulpice R, Gibon Y and Fernie AR (2008) The enigmatic contribution of mitochondrial function in photosynthesis. J Exp Bot 59: 1675–1684PubMedCrossRefGoogle Scholar
  104. Ohara K, Kokado Y, Yamamoto H, Sato F and Yazaki K (2004) Engineering of ubiquinone biosynthesis using the yeast coq2 gene confers oxidative stress tolerance in transgenic tobacco. Plant J 40: 734–743PubMedCrossRefGoogle Scholar
  105. Ohara K, Yamamoto K, Hamamoto M, Sasaki K and Yazaki K (2006) Functional characterization of OsPPT1, which encodes p-hydroxybenzoate polyprenyltransferase involved in ubiquinone biosynthesis in Oryza sativa. Plant Cell Physiol 47: 581–590PubMedCrossRefGoogle Scholar
  106. Okada K, Saito T, Nakagawa T, Kawamukai M and Kamiya Y (2000) Five geranylgeranyl diphosphate syn-thases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol 122: 1045–1056PubMedCrossRefGoogle Scholar
  107. Okada K, Ohara K, Yazaki K, Nozaki K, Uchida N, Kawa-mukai M, Nojiri H and Yamane H (2004) The AtPPT1 gene encoding 4-hydroxybenzoate polyprenyl diphos-phate transferase in ubiquinone biosynthesis is required for embryo development in Arabidopsis thaliana. Plant Mol Biol 55: 567–577PubMedCrossRefGoogle Scholar
  108. Okada K, Kasahara H, Yamaguchi S, Kawaide H, Kamiya Y, Nojiri H and Yamane H (2008) Genetic evidence for the role of isopentenyl diphosphate isomerases in the meval-onate pathway and plant development in Arabidopsis. Plant Cell Physiol 49: 604–616PubMedCrossRefGoogle Scholar
  109. Olsen JG, Rasmussen AV, von Wettstein-Knowles P and Henriksen A (2004) Structure of the mitochondrial β-ketoacyl-[acyl carrier protein] synthase from Arabi-dopsis and its role in fatty acid synthesis. FEBS Lett 577: 170–174PubMedCrossRefGoogle Scholar
  110. Ostrander DB, Zhang M, Mileykovskaya E, Rho M and Dowhan W (2001) Lack of mitochondrial anionic phos-pholipids causes an inhibition of translation of protein components of the electron transport chain. A yeast genetic model system for the study of anionic phos-pholipid function in mitochondria. J Biol Chem 276: 25262–25272Google Scholar
  111. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trézéguet V, Lauquin GJ and Brandolin G (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxy-atractyloside. Nature 426: 39–44PubMedCrossRefGoogle Scholar
  112. Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Green-berg ML and Schägger H (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278: 52873–52880PubMedCrossRefGoogle Scholar
  113. Phillips MA, D'Auria JC, Gershenzon J and Pichersky E (2008) The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcel-lular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell 20: 677–796PubMedCrossRefGoogle Scholar
  114. Rasmusson AG, Geisler DA and Møller IM (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8: 47–60PubMedCrossRefGoogle Scholar
  115. Rébeillé F, Alban C, Bourguignon J, Ravanel S and Douce R (2007) The role of plant mitochondria in the biosynthesis of coenzymes. Photosynth Res 92: 149–162PubMedCrossRefGoogle Scholar
  116. Rontein D, Wu WI, Voelker DR and Hanson AD (2003) Mitochondrial phosphatidylserine decarboxylase from higher plants. Functional complementation in yeast, localization in plants, and overexpression in Arabidopsis. Plant Physiol 132: 1678–1687PubMedCrossRefGoogle Scholar
  117. Schindler S and Lichtenthaler HK (1984) Comparison of the ubiquinone homologue pattern in plant mitochondria and their possible prokaryotic ancestors. In: Siegenthaler PA and Eichenberger W (eds) Structure, Function and Metabolism of Plant Lipids, pp. 273–276. Elsevier Science, AmsterdamGoogle Scholar
  118. Schlame M (2008) Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J Lipid Res 49: 1607–1620PubMedCrossRefGoogle Scholar
  119. Schlame M and Ren M (2006) Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett 580: 5450–5455PubMedCrossRefGoogle Scholar
  120. Schlame M, Brody S and Hostetler KY (1993) Mitochon-drial cardiolipin in diverse eukaryotes. Comparison of biosynthetic reactions and molecular acyl species. Eur J Biochem 212: 727–735PubMedCrossRefGoogle Scholar
  121. Schlame M, Rua D and Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39: 257–288PubMedCrossRefGoogle Scholar
  122. Schlame M, Ren M, Xu Y, Greenberg ML and Haller I (2005) Molecular symmetry in mitochondrial cardiolipins. Chem Phys Lipids 138: 38–49PubMedCrossRefGoogle Scholar
  123. Sheahan MB, McCurdy DW and Rose RJ (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant J 44: 744–755PubMedCrossRefGoogle Scholar
  124. Shen H, Heacock PN, Clancey CJ and Dowhan W (1996) The CDS1 gene encoding CDP-diacylglycerol synthase in Saccharomyces cerevisiae is essential for cell growth. J Biol Chem 271: 789–795PubMedCrossRefGoogle Scholar
  125. Shintani DK and Ohlrogge JB (1994) The characterization of a mitochondrial acyl carrier protein isoform isolated from Arabidopsis thaliana. Plant Physiol 104: 1221–1229PubMedCrossRefGoogle Scholar
  126. Shinzawa-Itoh K, Aoyama H, Muramoto K, Terada H, Kurauchi T, Tadehara Y, Yamasaki A, Sugimura T, Kurono S, Tsujimoto K, Mizushima T, Yamashita E, Tsukihara T and Yoshikawa S (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26: 1713–1725PubMedCrossRefGoogle Scholar
  127. Simockova M, Holič R, Tahotná D, Patton-Vogt J and Griač P (2008) Yeast Pgc1p (YPL206c) controls the amount of phosphatidylglycerol via a phospholipase C-type degradation mechanism. J Biol Chem 283: 17107–17115PubMedCrossRefGoogle Scholar
  128. Steenbergen R, Nanowski TS, Beigneux A, Kulinski A, Young SG and Vance JE (2005) Disruption of the phos-phatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects. J Biol Chem 280: 40032–40040PubMedCrossRefGoogle Scholar
  129. Storey MK, Clay KL, Kutateladze T, Murphy RC, Overduin M and Voelker DR (2001) Phosphatidylethanolamine has an essential role in Saccharomyces cerevisiae that is independent of its ability to form hexagonal phase structures. J Biol Chem 276: 48539–48548PubMedGoogle Scholar
  130. Su X and Dowhan W (2006a) Regulation of cardiolipin synthase levels in Saccharomyces cerevisiae. Yeast 23: 279–291CrossRefGoogle Scholar
  131. Su X and Dowhan W (2006b) Translational regulation of nuclear gene COX4 expression by mitochondrial content of phosphatidylglycerol and cardiolipin in Saccharomy-ces cerevisiae. Mol Cell Biol 26: 743–753CrossRefGoogle Scholar
  132. Swiezewska E, Dallner G, Andersson B and Ernster L (1993) Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves. J Biol Chem 268: 1494–1499PubMedGoogle Scholar
  133. Takahashi S, Ogiyama Y, Kusano H, Shimada H, Kawamu-kai M and Kadowaki K (2006) Metabolic engineering of coenzyme Q by modification of isoprenoid side chain in plant. FEBS Lett 580: 955–959PubMedCrossRefGoogle Scholar
  134. Trotter PJ, Pedretti J and Voelker DR (1993) Phosphatidyl-serine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J Biol Chem 268: 21416–21424PubMedGoogle Scholar
  135. Trotter PJ, Pedretti J, Yates R and Voelker DR (1995) Phos-phatidylserine decarboxylase 2 of Saccharomyces cer-evisiae. Cloning and mapping of the gene, heterologous expression, and creation of the null allele. J Biol Chem 270: 6071–6080PubMedCrossRefGoogle Scholar
  136. Tuller G, Hrastnik C, Achleitner G, Schiefthaler U, Klein F and Daum G (1998) YDL142c encodes cardiolipin syn-thase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae. FEBS Lett 421: 15–18PubMedCrossRefGoogle Scholar
  137. Vaena de Avalos S, Su X, Zhang M, Okamoto Y, Dowhan W and Hannun YA (2005) The phosphatidylglycerol/cardi-olipin biosynthetic pathway is required for the activation of inositol phosphosphingolipid phospholipase C, Isc1p, during growth of Saccharomyces cerevisiae. J Biol Chem 280: 7170–7177PubMedCrossRefGoogle Scholar
  138. Vance JE and Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44: 207–234PubMedCrossRefGoogle Scholar
  139. Vaz FM, Houtkooper RH, Valianpour F, Barth PG and Wanders RJ (2003) Only one splice variant of the human TAZ gene encodes a functional protein with a role in cardiolipin metabolism. J Biol Chem 278: 43089–43094PubMedCrossRefGoogle Scholar
  140. Wada H, Shintani D and Ohlrogge J (1997) Why do mitochondria synthesize fatty acids? Evidence for involvement in lipoic acid production. Proc Natl Acad Sci USA 94: 1591–1596PubMedCrossRefGoogle Scholar
  141. Wada M, Yasuno R and Wada H (2001a) Identification of an Arabidopsis cDNA encoding a lipoyltransferase located in plastids. FEBS Lett 506: 286–290CrossRefGoogle Scholar
  142. Wada M, Yasuno R, Jordan SW, Cronan JE Jr and Wada H (2001b) Lipoic acid metabolism in Arabidopsis thaliana: cloning and characterization of a cDNA encoding lipoyltransferase. Plant Cell Physiol 42: 650–656CrossRefGoogle Scholar
  143. Witkowski A, Joshi AK and Smith S (2007) Coupling of the de novo fatty acid biosynthesis and lipoylation pathways in mammalian mitochondria. J Biol Chem 282: 14178–14185PubMedCrossRefGoogle Scholar
  144. Woodson JD and Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9: 383–395PubMedCrossRefGoogle Scholar
  145. Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C and Benning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129: 594–604PubMedCrossRefGoogle Scholar
  146. Xu Y, Kelley RI, Blanck TJ and Schlame M (2003) Remodelling of cardiolipin by phospholipid transacylation. J Biol Chem 278: 51380–51385PubMedCrossRefGoogle Scholar
  147. Xu Y, Malhotra A, Ren M and Schlame M (2006a) The enzymatic function of tafazzin. J Biol Chem 281: 39217–3924CrossRefGoogle Scholar
  148. Xu Y, Condell M, Plesken H, Edelman-Novemsky I, Ma J, Ren M and Schlame M (2006b) A Drosophila model of Barth syndrome. Proc Natl Acad Sci USA 103: 11584–11588CrossRefGoogle Scholar
  149. Yao N and Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18: 397–411PubMedCrossRefGoogle Scholar
  150. Yao N, Eisfelder BJ, Marvin J and Greenberg JT (2004) The mitochondrion — an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40: 596–610PubMedCrossRefGoogle Scholar
  151. Yasuno R and Wada H (1998) Biosynthesis of lipoic acid in Arabidopsis: cloning and characterization of the cDNA for lipoic acid synthase. Plant Physiol 118: 935–943PubMedCrossRefGoogle Scholar
  152. Yasuno R and Wada H (2002) The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. FEBS Lett 517: 110–114PubMedCrossRefGoogle Scholar
  153. Yasuno R, von Wettstein-Knowles P and Wada H (2004) Identification and molecular characterization of the β-ketoacyl-[acyl carrier protein] synthase component of the Arabidopsis mitochondrial fatty acid synthase. J Biol Chem 279: 8242–8251PubMedCrossRefGoogle Scholar
  154. Yu B, Wakao S, Fan J and Benning C (2004) Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol 45: 503–510PubMedCrossRefGoogle Scholar
  155. Zhang M, Mileykovskaya E and Dowhan W (2002) Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J Biol Chem 277: 43553–43556PubMedCrossRefGoogle Scholar
  156. Zhang M, Mileykovskaya E and Dowhan W (2005) Cardi-olipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem 280: 29403–29408PubMedCrossRefGoogle Scholar
  157. Zheng Z, Xia Q, Dauk M, Shen W, Selvaraj G and Zou J (2003) Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell 15: 1872–1887PubMedCrossRefGoogle Scholar
  158. Zhong Q, Gohil VM, Ma L and Greenberg ML (2004) Absence of cardiolipin results in temperature sensitivity, respiratory defects, and mitochondrial DNA instability independent of pet56. J Biol Chem 279: 32294–32300PubMedCrossRefGoogle Scholar
  159. Zimmermann P, Hennig L and Gruissem W (2005) Gene-expression analysis and network discovery using Gen-evestigator. Trends Plant Sci 10: 407–409PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.RWTH Aachen University, Institute for Biology IBotanyGermany

Personalised recommendations