Lipoate-protein ligase and octanoyltransferase are essential for protein lipoylation in mitochondria of arabidopsis

Plant Physiology

Volumn 165, Issue 3, 2014, Pages 978-990

  Ewald, Ralph ^a   Hoffmann, Christiane ^b   Florian, Alexandra ^c   Neuhaus, Ekkehard ^b   Fernie, Alisdair R ^c   Bauwe, Hermann ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903650266     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.238311     Document Type: Article

References (61)

1. Allary M, Lu JZQ, Zhu L, Prigge ST (2007) Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Mol Microbiol 63: 1331-1344
2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
3. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15: 330-336
4. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
6. Chen S, Hofius D, Sonnewald U, Börnke F (2003) Temporal and spatial control of gene silencing in transgenic plants by inducible expression of double-stranded RNA. Plant J 36: 731-740
7. Christensen QH, Cronan JE (2009) The Thermoplasma acidophilum LplA-LplB complex defines a new class of bipartite lipoate-protein ligases. J Biol Chem 284: 21317-21326
8. Christensen QH, Martin N, Mansilla MC, de Mendoza D, Cronan JE (2011) A novel amidotransferase required for lipoic acid cofactor assembly in Bacillus subtilis. Mol Microbiol 80: 350-363
9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
10. Douce R, Bourguignon J, Neuburger M, Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6: 167-176
11. Engel N, van den Daele K, Kolukisaoglu U, Morgenthal K, Weckwerth W, Pärnik T, Keerberg O, Bauwe H (2007) Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions. Plant Physiol 144: 1328-1335
12. Ewald R, Hoffmann C, Neuhaus E, Bauwe H (2014) Two redundant octanoyltransferases and one obligatory lipoyl synthase provide proteinlipoylation autonomy to plastids of Arabidopsis. Plant Biol (Stuttg) 16: 35-42
13. Ewald R, Kolukisaoglu U, Bauwe U, Mikkat S, 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: 41-48
14. Fernie AR, Aharoni A, Willmitzer L, Stitt M, Tohge T, Kopka J, Carroll AJ, Saito K, Fraser PD, DeLuca V (2011) Recommendations for reporting metabolite data. Plant Cell 23: 2477-2482
15. Fujiwara K, Takeuchi S, Okamura-Ikeda K, Motokawa Y (2001) Purification, characterization, and cDNA cloning of lipoate-activating enzyme from bovine liver. J Biol Chem 276: 28819-28823
16. Fujiwara K, Toma S, Okamura-Ikeda K, Motokawa Y, Nakagawa A, Taniguchi H (2005) Crystal structure of lipoate-protein ligase A from Escherichia coli: Determination of the lipoic acid-binding site. J Biol Chem 280: 33645-33651
17. Gueguen V, Macherel D, Jaquinod M, Douce R, Bourguignon J (2000) Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J Biol Chem 275: 5016-5025
18. Hasse D, Mikkat S, Hagemann M, Bauwe H (2009) Alternative splicing produces an H-protein with better substrate properties for the P-protein of glycine decarboxylase. FEBS J 276: 6985-6991
19. Hermes FA, Cronan JE (2013) The role of the Saccharomyces cerevisiae lipoate protein ligase homologue, Lip3, in lipoic acid synthesis. Yeast 30: 415-427
20. Jordan SW, Cronan JE Jr (2003) The Escherichia coli lipB gene encodes lipoyl (octanoyl)-acyl carrier protein:protein transferase. J Bacteriol 185: 1582-1589
21. Kang SG, Jeong HK, Lee E, Natarajan S (2007) Characterization of a lipoate-protein ligase A gene of rice (Oryza sativa L.). Gene 393: 53-61
22. Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37: 300-311
23. Keech O, Dizengremel P, Gardeström P (2005) Preparation of leaf mitochondria from Arabidopsis thaliana. Physiol Plant 124: 403-409
24. Kim DJ, Kim KH, Lee HH, Lee SJ, Ha JY, Yoon HJ, Suh SW (2005) Crystal structure of lipoate-protein ligase A bound with the activated intermediate: insights into interaction with lipoyl domains. J Biol Chem 280: 38081-38089
25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
26. Lernmark U, Gardeström P (1994) Distribution of pyruvate dehydrogenase complex activities between chloroplasts and mitochondria from leaves of different species. Plant Physiol 106: 1633-1638
27. Lin M, Behal R, Oliver DJ (2003) Disruption of plE2, the gene for the E2 subunit of the plastid pyruvate dehydrogenase complex, in Arabidopsis causes an early embryo lethal phenotype. Plant Mol Biol 52: 865-872
28. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1: 387-396
29. Martin N, Christensen QH, Mansilla MC, Cronan JE, de Mendoza D (2011) A novel two-gene requirement for the octanoyltransfer reaction of Bacillus subtilis lipoic acid biosynthesis. Mol Microbiol 80: 335-349
30. Masterson C, Wood C (2000) Mitochondrial b-oxidation of fatty acids in higher plants. Physiol Plant 109: 217-224
31. Masterson C, Wood C (2009) Influence of mitochondrial b-oxidation on early pea seedling development. New Phytol 181: 832-842
32. Mooney BP, Miernyk JA, Randall DD (2002) The complex fate of a-ketoacids. Annu Rev Plant Biol 53: 357-375
33. Morikawa T, Yasuno R, Wada H (2001) Do mammalian cells synthesize lipoic acid? Identification of a mouse cDNA encoding a lipoic acid synthase located in mitochondria. FEBS Lett 498: 16-21
34. Morris TW, Reed KE, Cronan JE Jr (1995) Lipoic acid metabolism in Escherichia coli: the lplA and lipB genes define redundant pathways for ligation of lipoyl groups to apoprotein. J Bacteriol 177: 1-10
35. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957-970
36. Ohlrogge JB, Kuhn DN, Stumpf PK (1979) Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Proc Natl Acad Sci USA 76: 1194-1198
37. Perham RN (2000) Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu Rev Biochem 69: 961-1004
38. Posner MG, Upadhyay A, Bagby S, Hough DW, Danson MJ (2009) A unique lipoylation system in the Archaea: lipoylation in Thermoplasma acidophilum requires two proteins. FEBS J 276: 4012-4022
39. Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152: 1501-1513
40. Schonauer MS, Kastaniotis AJ, Kursu VAS, Hiltunen JK, Dieckmann CL (2009) Lipoic acid synthesis and attachment in yeast mitochondria. J Biol Chem 284: 23234-23242
41. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994
42. Shimakata T, Stumpf PK (1982) Isolation and function of spinach leaf betaketoacyl-[acyl-carrier-protein] synthases. Proc Natl Acad Sci USA 79: 5808-5812
43. Shockey JM, FuldaMS, Browse J (2003) Arabidopsis contains a large superfamily of acyl-activating enzymes: phylogenetic and biochemical analysis reveals a new class of acyl-coenzyme A synthetases. Plant Physiol 132: 1065-1076
44. Soreze Y, Boutron A, Habarou F, Barnerias C, Nonnenmacher L, Delpech H, Mamoune A, Chrétien D, Hubert L, Bole-Feysot C, et al (2013)Mutations in human lipoyltransferase gene LIPT1 cause a Leigh disease with secondary deficiency for pyruvate and alpha-ketoglutarate dehydrogenase. Orphanet J Rare Dis 8: 192
45. Souza CdeA, Barbazuk B, Ralph SG, Bohlmann J, Hamberger B, Douglas CJ (2008) Genome-wide analysis of a land plant-specific acyl:coenzyme A synthetase (ACS) gene family in Arabidopsis, poplar, rice and Physcomitrella. New Phytol 179: 987-1003
46. Spalding MD, Prigge ST (2010) Lipoic acid metabolism in microbial pathogens. Microbiol Mol Biol Rev 74: 200-228
47. Studart-Guimarães C, Fait A, Nunes-Nesi A, Carrari F, Usadel B, Fernie AR (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the g-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol 145: 626-639
48. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15: 462-470
49. Taylor NL, Day DA, Millar AH (2002) Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J Biol Chem 277: 42663-42668
50. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-Northerns, expression angling, and promoter analyses. Plant J 43: 153-163
51. Tsunoda JN, Yasunobu KT (1967) Mammalian lipoic acid activating enzyme. Arch Biochem Biophys 118: 395-401
52. Wada H, Shintani D, Ohlrogge J (1997) Why do mitochondria synthesize fatty acids? Evidence for involvement in lipoic acid production. Proc Natl Acad Sci USA 94: 1591-1596
53. Wada M, Yasuno R, Jordan SW, Cronan JE Jr, Wada H (2001a) Lipoic acid metabolism in Arabidopsis thaliana: cloning and characterization of a cDNA encoding lipoyltransferase. Plant Cell Physiol 42: 650-656
54. Wada M, Yasuno R, Wada H (2001b) Identification of an Arabidopsis cDNA encoding a lipoyltransferase located in plastids. FEBS Lett 506: 286-290
55. Wendt UK, Wenderoth I, Tegeler A, Von Schaewen A (2000) Molecular characterization of a novel glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). Plant J 23: 723-733
56. Witkowski A, Joshi AK, Smith S (2007) Coupling of the de novo fatty acid biosynthesis and lipoylation pathways in mammalian mitochondria. J Biol Chem 282: 14178-14185
57. Wittig I, Braun HP, Schägger H (2006) Blue native PAGE. Nat Protoc 1: 418-428
58. Yasuno R, von Wettstein-Knowles P, Wada H (2004) Identification and molecular characterization of the b-ketoacyl-[acyl carrier protein] synthase component of the Arabidopsis mitochondrial fatty acid synthase. J Biol Chem 279: 8242-8251
59. Yasuno R, Wada H (1998) Biosynthesis of lipoic acid in Arabidopsis: cloning and characterization of the cDNA for lipoic acid synthase. Plant Physiol 118: 935-943
60. Yasuno R, Wada H (2002) The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. FEBS Lett 517: 110-114
61. Zhao X, Miller JR, Jiang Y, Marletta MA, Cronan JE (2003) Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol 10: 1293-1302