, Volume 243, Issue 4, pp 1011–1022 | Cite as

Acylcarnitines participate in developmental processes associated to lipid metabolism in plants

  • Phuong-Jean Nguyen
  • Sonia Rippa
  • Yannick Rossez
  • Yolande PerrinEmail author
Original Article


Main conclusion

Plant acylcarnitines are present during anabolic processes of lipid metabolism. Their low contents relatively to the corresponding acyl-CoAs suggest that they are associated to specific pools of activated fatty acids.

The non-proteinaceous amino acid carnitine exists in plants either as a free form or esterified to fatty acids. To clarify the biological significance of acylcarnitines in plant lipid metabolism, we have analyzed their content in plant extracts using an optimized tandem mass spectrometry coupled to liquid chromatography method. We have studied different developmental processes (post-germination, organogenesis, embryogenesis) targeted for their high requirement for lipid metabolism. The modulation of the acylcarnitine content was compared to that of the lipid composition and lipid biosynthetic gene expression level in the analyzed materials. Arabidopsis mutants were also studied based on their alteration in de novo fatty acid partitioning between the prokaryotic and eukaryotic pathways of lipid biosynthesis. We show that acylcarnitines cannot specifically be associated to triacylglycerol catabolism but that they are also associated to anabolic pathways of lipid metabolism. They are present during membrane and storage lipid biosynthesis processes. A great divergence in the relative contents of acylcarnitines as compared to the corresponding acyl-CoAs suggests that acylcarnitines are associated to very specific process(es) of lipid metabolism. The nature of their involvement as the transport form of activated fatty acids or in connection with the management of acyl-CoA pools is discussed. Also, the occurrence of medium-chain entities suggests that acylcarnitines are associated with additional lipid processes such as protein acylation for instance. This work strengthens the understanding of the role of acylcarnitines in plant lipid metabolism, probably in the management of specific acyl-CoA pools.


Acyl-CoA Arabidopsis Fatty acid transport Lipid trafficking Plant development Plant metabolism 



Acyl carrier protein


Carnitine acetyltransferase


Carnitine palmitoyltransferase


Fatty acid


Fatty acyl-ACP thioesterase


Free fatty acid


3-Ketoacyl-ACP synthase


Long-chain acyl-CoA synthase


Lysophosphatidic acid acyltransferase


Lysophosphatidylcholine acyltransferase


Response factor




Wild type



We are grateful to Dr. Laurent Gutierrez and Dr. Stéphanie Guénin from Université de Picardie Jules Verne (Amiens, France) for their assistance in RT-qPCR analyses and Franck Merlier from our group for his technical support in mass spectrometry analysis. We are grateful to Dr. Gustavo Bonaventure from Max Planck Institute (Jena, Germany) for kindly providing with the Arabidopsis mutant genotypes. We also thank a lot Dr. George Lomonossoff from John Innes Centre (Norwich, UK) for taking time to carefully read the manuscript. Finally, we appreciate the time and helpful comments from the reviewers. The work was supported by the French Ministry of National Education, Higher Education and Research.

Supplementary material

425_2016_2465_MOESM1_ESM.pdf (131 kb)
Supplementary material 1 (PDF 130 kb)
425_2016_2465_MOESM2_ESM.pdf (26 kb)
Supplementary material 2 (PDF 26 kb)
425_2016_2465_MOESM3_ESM.pdf (10 kb)
Supplementary material 3 (PDF 10 kb)


  1. Abo-Hashema KA, Cake MH, Power GW, Clarke D (1999) Evidence for triacylglycerol synthesis in the lumen of microsomes via a lipolysis-esterification pathway involving carnitine acyltransferases. J Biol Chem 274:35577–35582CrossRefPubMedGoogle Scholar
  2. Antonenkov VD, Hiltunen JK (2012) Transfer of metabolites across the peroxisomal membrane. Biochim Biophys Acta 1822:1374–1386CrossRefPubMedGoogle Scholar
  3. Bach L, Gissot L, Marion J, Tellier F, Moreau P, Satiat-Jeunemaître B, Palauqui JC, Napier JA, Faure JD (2011) Very-long-chain fatty acids are required for cell plate formation during cytokinesis in Arabidopsis thaliana. J Cell Sci 124:3223–3234CrossRefPubMedGoogle Scholar
  4. Bates PD, Stymne S, Ohlrogge J (2013) Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol 16:358–364CrossRefPubMedGoogle Scholar
  5. Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25:71–91CrossRefPubMedGoogle Scholar
  6. Bonaventure G, Salas JJ, Pollard MR, Ohlrogge JB (2003) Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. Plant Cell 15:1020–1033CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bonaventure G, Bao X, Ohlrogge J, Pollard M (2004) Metabolic responses to the reduction in palmitate caused by disruption of the FATB gene in Arabidopsis. Plant Physiol 135:1269–1279CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bourdin B, Adenier H, Perrin Y (2007) Carnitine is associated with fatty acid metabolism in plants. Plant Physiol Biochem 45:926–931CrossRefPubMedGoogle Scholar
  9. Burgess N, Thomas DR (1986) Carnitine acyltransferase in pea cotyledon mitochondria. Planta 167:58–65CrossRefPubMedGoogle Scholar
  10. Cruz-Ramírez A, López-Bucio J, Ramírez-Pimentel G, Zurita-Silva A, Sánchez-Calderon L, Ramírez-Chávez E, González-Ortega E, Herrera-Estrella LL (2004) The xipotl mutant of Arabidopsis reveals a critical role for phospholipid metabolism in root system development and epidermal cell integrity. Plant Cell 16:2020–2034CrossRefPubMedPubMedCentralGoogle Scholar
  11. Elgersma Y, van Roermund CW, Wanders RJ, Tabak HF (1995) Peroxisomal and mitochondrial carnitine acetyltransferases of Saccharomyces cerevisiae are encoded by a single gene. EMBO J 14:3472–3479PubMedPubMedCentralGoogle Scholar
  12. Ewald R, Hoffmann C, Florian A, Neuhaus E, Fernie AR, Bauwe H (2014) Lipoate-protein ligase and octanoyltransferase are essential for protein lipoylation in mitochondria of Arabidopsis. Plant Physiol 165:978–990CrossRefPubMedPubMedCentralGoogle Scholar
  13. Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, Graham I, Baker A, Holdsworth M (2002) Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J 21:2912–2922CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fraenkel G (1953) Studies on the distribution of vitamin BT (carnitine). Biol Bull 104:359–371CrossRefGoogle Scholar
  15. Fraser F, Zammit VA (1999) Submitochondrial and subcellular distributions of the carnitine-acylcarnitine carrier. FEBS Lett 445:41–44CrossRefPubMedGoogle Scholar
  16. Gerbling H, Gerhardt B (1988) Carnitine-acyltransferase activity of mitochondria from mung-bean hypocotyls. Planta 174:90–93CrossRefPubMedGoogle Scholar
  17. Gooding JM, Shayeghi M, Saggerson ED (2004) Membrane transport of fatty acylcarnitine and free l-carnitine by rat liver microsomes. Eur J Biochem 271:954–961CrossRefPubMedGoogle Scholar
  18. Graham IA, Eastmond PJ (2002) Pathways of straight and branched chain fatty acid catabolism in higher plants. Prog Lipid Res 41:156–181CrossRefPubMedGoogle Scholar
  19. Gutierrez L, Mongelard G, Floková K, Pacurar DI, Novák O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kim S, Yamaoka Y, Ono H, Kim H, Shim D, Maeshima M, Martinoia E, Cahoon EB, Nishida I, Lee Y (2013) AtABCA9 transporter supplies fatty acids for lipid synthesis to the endoplasmic reticulum. Proc Natl Acad Sci USA 110:773–778CrossRefPubMedPubMedCentralGoogle Scholar
  21. Koo AJ, Ohlrogge JB, Pollard M (2004) On the export of fatty acids from the chloroplast. J Biol Chem 279:16101–16110CrossRefPubMedGoogle Scholar
  22. 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 85:4143–4147CrossRefPubMedPubMedCentralGoogle Scholar
  23. Li N, Gügel 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:e1002053CrossRefPubMedPubMedCentralGoogle Scholar
  24. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, Debono A, Durrett TP, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2013) Acyl-lipid metabolism. Arabidopsis Book 11:e0161CrossRefPubMedPubMedCentralGoogle Scholar
  25. Masterson C, Wood C (2000) Pea chloroplast carnitine acetyltransferase. Proc Biol Sci 267:1–6CrossRefPubMedPubMedCentralGoogle Scholar
  26. Masterson C, Wood C (2009) Influence of mitochondrial beta-oxidation on early pea seedling development. New Phytol 181:832–842CrossRefPubMedGoogle Scholar
  27. McLaren I, Wood C, Jalil MNH, Yong BCS, Thomas DR (1985) Carnitine acyltransferases in chloroplasts of Pisum sativum L. Planta 163:197–200CrossRefPubMedGoogle Scholar
  28. McNeil PH, Thomas DR (1975) Carnitine content of pea seedling cotyledons. Phytochemistry 14:2335–2336CrossRefGoogle Scholar
  29. McNeil PH, Thomas DR (1976) The effect of carnitine on palmitate oxidation by pea cotyledon mitochondria. J Exp Bot 27:1163–1179CrossRefGoogle Scholar
  30. Nameth B, Dinka SJ, Chatfield SP, Morris A, English J, Lewis D, Oro R, Raizada MN (2013) The shoot regeneration capacity of excised Arabidopsis cotyledons is established during the initial hours after injury and is modulated by a complex genetic network of light signaling. Plant, Cell Environ 36:68–86CrossRefGoogle Scholar
  31. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970CrossRefPubMedPubMedCentralGoogle Scholar
  32. Panter RA, Mudd JB (1969) Carnitine levels in some higher plants. FEBS Lett 5:169–170CrossRefPubMedGoogle Scholar
  33. Ramsay RR, Zammit VA (2004) Carnitine acyltransferases and their influence on CoA pools in health and disease. Mol Aspects Med 25:475–493CrossRefPubMedGoogle Scholar
  34. Ramsay RR, Gandour RD, Van Der Leij FR (2001) Molecular enzymology of carnitine transfer and transport. Biochem Biophys Acta Protein Struct Mol Enzymol 1546:21–43CrossRefGoogle Scholar
  35. Running MP (2014) The role of lipid post-translational modification in plant developmental processes. Front Plant Sci 5:50CrossRefPubMedPubMedCentralGoogle Scholar
  36. Salas JJ, Ohlrogge JB (2002) Characterization of substrate specificity of plant FatA and FatB acyl-ACP thioesterases. Arch Biochem Biophys 403:25–34CrossRefPubMedGoogle Scholar
  37. Schwabedissen-Gerbling H, Gerhardt B (1995) Purification and characterization of carnitine acyltransferase from higher plant mitochondria. Phytochemistry 39:36–43CrossRefGoogle Scholar
  38. Shockey JM, Fulda MS, Browse J (2002) Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol 129:1710–1722CrossRefPubMedPubMedCentralGoogle Scholar
  39. Sierra AY, Gratacós E, Carrasco P, Clotet J, Ureña J, Serra D, Asins G, Hegardt FG, Casals N (2008) CPT1c is localized in endoplasmic reticulum of neurons and has carnitine palmitoyltransferase activity. J Biol Chem 283:6878–6885CrossRefPubMedGoogle Scholar
  40. Steiber A, Kerner J, Hoppel CL (2004) Carnitine: a nutritional, biosynthetic, and functional perspective. Mol Aspects Med 25:455–473CrossRefPubMedGoogle Scholar
  41. Stephens FB, Constantin-Teodosiu D, Greenhaff PL (2007) New insights concerning the role of carnitine in the regulation of fuel metabolism in skeletal muscle. J Physiol 581:431–444CrossRefPubMedPubMedCentralGoogle Scholar
  42. ter Veld F, Primassin S, Hoffmann L, Mayatepek E, Spiekerkoetter U (2009) Corresponding increase in long-chain acyl-CoA and acylcarnitine after exercise in muscle from VLCAD mice. J Lipid Res 50:1556–1562CrossRefPubMedPubMedCentralGoogle Scholar
  43. Thomas DR, Wood C (1986) The two β-oxidation sites in pea cotyledons carnitine palmitoyltransferase: location and function in pea mitochondria. Planta 168:261–266PubMedGoogle Scholar
  44. Tjellström H, Yang Z, Allen DK, Ohlrogge JB (2012) Rapid kinetic labeling of Arabidopsis cell suspension cultures: implications for models of lipid export from plastids. Plant Physiol 158:601–611CrossRefPubMedPubMedCentralGoogle Scholar
  45. van Roermund CW, Waterham HR, Ijlst L, Wanders RJ (2003) Fatty acid metabolism in Saccharomyces cerevisiae. Cell Mol Life Sci 60:1838–1851CrossRefPubMedGoogle Scholar
  46. Vrkoslav V, Cvačka J (2012) Identification of the double-bond position in fatty acid methyl esters by liquid chromatography/atmospheric pressure chemical ionisation mass spectrometry. J Chromatogr A 1259:244–250CrossRefPubMedGoogle Scholar
  47. Wang Z, Benning C (2012) Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochem Soc Trans 40:457–463CrossRefPubMedGoogle Scholar
  48. Washington L, Cook GA, Mansbach CM 2nd (2003) Inhibition of carnitine palmitoyltransferase in the rat small intestine reduces export of triacylglycerol into the lymph. J Lipid Res 44:1395–1403CrossRefPubMedGoogle Scholar
  49. Wood C, Jalil MNH, Ariffin A, Yong BCS, Thomas DR (1983) Carnitine short-chain acyltransferases in pea mitochondria. Planta 158:175–178CrossRefPubMedGoogle Scholar
  50. Wood C, Jalil MNH, McLaren I, Yong BCS, Ariffin A, McNeil PH, Burgess N, Thomas DR (1984) Carnitine long-chain acyltransferase and oxidation of palmitate, palmitoyl CoA and palmitoylcarnitine by pea mitochondria preparations. Planta 161:255–260CrossRefPubMedGoogle Scholar
  51. Zammit VA, Ramsay RR, Bonomini M, Arduini A (2009) Carnitine, mitochondrial function and therapy. Adv Drug Deliv Rev 61:1353–1362CrossRefPubMedGoogle Scholar
  52. 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 64:1048–1058CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Phuong-Jean Nguyen
    • 1
  • Sonia Rippa
    • 1
  • Yannick Rossez
    • 1
  • Yolande Perrin
    • 1
    Email author
  1. 1.Génie Enzymatique et Cellulaire, FRE 3580 CNRS, Centre de recherche RoyallieuSorbonne Universités, Université de Technologie de CompiègneCompiègne CedexFrance

Personalised recommendations