Two redundant octanoyltransferases and one obligatory lipoyl synthase provide protein-lipoylation autonomy to plastids of Arabidopsis

Plant Biology

Volumn 16, Issue 1, 2014, Pages 35-42

  Ewald, R ^a   Hoffmann, C ^b   Neuhaus, E ^b   Bauwe, H ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Arabidopsis; Lipoyl synthase; Octanoyltransferase; Protein lipoylation

Indexed keywords

DICOTYLEDON; ENZYME ACTIVITY; PLASTID; PROTEIN;

ARABIDOPSIS;

ACYLTRANSFERASE; LIGASE; LIP2 LIPOYLTRANSFERASE, ARABIDOPSIS; VEGETABLE PROTEIN;

ARABIDOPSIS; ENZYMOLOGY; ESCHERICHIA COLI; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PLASTID;

ACYLTRANSFERASES; ARABIDOPSIS; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; LIGASES; PLANT PROTEINS; PLASTIDS;

EID: 84890988080     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12028     Document Type: Article

References (45)

1. Allary M., Lu J.Z.Q., Zhu L.Q., Prigge S.T. (2007) Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Molecular Microbiology, 63, 1331-1344.
2. Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., Gadrinab C., Heller C., Jeske A., Koesema E., Meyers C.C., Parker H., Prednis L., Ansari Y., Choy N., Deen H., Geralt M., Hazari N., Hom E., Karnes M., Mulholland C., Ndubaku R., Schmidt I., Guzman P., Aguilar-Henonin L., Schmid M., Weigel D., Carter D.E., Marchand T., Risseeuw E., Brogden D., Zeko A., Crosby W.L., Berry C.C., Ecker J.R. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
3. Booker S.J. (2004) Unraveling the pathway of lipoic acid biosynthesis. Chemistry and Biology, 11, 10-12.
4. Bradford M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248-254.
5. Christensen Q.H., Cronan J.E. (2010) Lipoic acid synthesis: a new family of octanoyltransferases generally annotated as lipoate protein ligases. Biochemistry, 49, 10024-10036.
6. Cicchillo R.M., Booker S.J. (2005) Mechanistic investigations of lipoic acid biosynthesis in Escherichia coli: Both sulfur atoms in lipoic acid are contributed by the same lipoyl synthase polypeptide. Journal of the American Chemical Society, 127, 2860-2861.
7. Cicchillo R.M., Iwig D.F., Jones A.D., Nesbitt N.M., Baleanu-Gogonea C., Souder M.G., Tu L., Booker S.J. (2004) Lipoyl synthase requires two equivalents of S-adenosyl-L-methionine to synthesize one equivalent of lipoic acid. Biochemistry, 43, 6378-6386.
8. Douce R., Bourguignon J., Neuburger M., Rebeille F. (2001) The glycine decarboxylase system: a fascinating complex. Trends in Plant Science, 6, 167-176.
9. Emanuelsson O., Nielsen H., von Heijne G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science, 8, 978-984.
10. Ewald R., Kolukisaoglu Ü., 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 Physiology, 145, 41-48.
11. Fujiwara K., Okamura-Ikeda K., Motokawa Y. (1994) Purification and characterization of lipoyl-AMP:N-ε-lysine lipoyltransferase from bovine liver mitochondria. Journal of Biological Chemistry, 269, 16605-16609.
12. Fujiwara K., Takeuchi S., Okamura-Ikeda K., Motokawa Y. (2001) Purification, characterization, and cDNA cloning of lipoate-activating enzyme from bovine liver. Journal of Biological Chemistry, 276, 28819-28823.
13. Gueguen V., Macherel D., Jaquinod M., Douce R., Bourguignon J. (2000) Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. Journal of Biological Chemistry, 275, 5016-5025.
14. Hayden M.A., Huang I., Bussiere D.E., Ashley G.W. (1992) The biosynthesis of lipoic acid. Cloning of lip, a lipoate biosynthetic locus of Escherichia coli. Journal of Biological Chemistry, 267, 9512-9515.
15. Hermes F.A.M., Cronan J.E. (2009) Scavenging of cytosolic octanoic acid by mutant LplA lipoate ligases allows growth of Escherichia coli strains lacking the LipB octanoyltransferase of lipoic acid synthesis. Journal of Bacteriology, 191, 6796-6803.
16. Hiltunen J.K., Autio K.J., Schonauer M.S., Kursu V.A.S., Dieckmann C.L., Kastaniotis A.J. (2010) Mitochondrial fatty acid synthesis and respiration. Biochimica et Biophysica Acta, 1797, 1195-1202.
17. Jordan S.W., Cronan J.E. Jr (2003) The Escherichia coli lipB gene encodes lipoyl (octanoyl)-acyl carrier protein:protein transferase. Journal of Bacteriology, 185, 1582-1589.
18. Kang S.G., Jeong H.K., Lee E., Natarajan S. (2007) Characterization of a lipoate-protein ligase A gene of rice (Oryza sativa L.). Gene, 393, 53-61.
19. Kleinboelting N., Huep G., Kloetgen A., Viehoever P., Weisshaar B. (2012) GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database. Nucleic Acids Research, 40, D1211-D1215.
20. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
21. Lernmark U., Gardeström P. (1994) Distribution of pyruvate dehydrogenase complex activities between chloroplasts and mitochondria from leaves of different species. Plant Physiology, 106, 1633-1638.
22. Lin M., Behal R., Oliver D.J. (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 Molecular Biology, 52, 865-872.
23. Mooney B.P., Miernyk J.A., Randall D.D. (2002) The complex fate of α-ketoacids. Annual Review of Plant Biology, 53, 357-375.
24. Morris T.W., Reed K.E., Cronan J.E. Jr (1994) Identification of the gene encoding lipoate-protein ligase A of Escherichia coli. Molecular cloning and characterization of the lplA gene and gene product. Journal of Biological Chemistry, 269, 16091-16100.
25. Morris T.W., Reed K.E., Cronan J.E. Jr (1995) Lipoic acid metabolism in Escherichia coli: the lplA and lipB genes define redundant pathways for ligation of lipoyl groups to apoprotein. Journal of Bacteriology, 177, 1-10.
26. Navari-Izzo F., Quartacci M.F., Sgherri C. (2002) Lipoic acid: a unique antioxidant in the detoxification of activated oxygen species. Plant Physiology and Biochemistry, 40, 463-470.
27. Ohlrogge J.B., Jaworski J.G. (1997) Regulation of fatty acid synthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 109-136.
28. Ohlrogge J.B., Kuhn D.N., Stumpf P.K. (1979) Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Proceedings of the National Academy of Sciences USA, 76, 1194-1198.
29. Perham R.N. (2000) Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annual Review of Biochemistry, 69, 961-1004.
30. Posner M.G., Upadhyay A., Bagby S., Hough D.W., Danson M.J. (2009) A unique lipoylation system in the Archaea: lipoylation in Thermoplasma acidophilum requires two proteins. FEBS Journal, 276, 4012-4022.
31. Ramaswamy A.V., Maurelli A.T. (2010) Chlamydia trachomatis serovar L2 can utilize exogenous lipoic acid through the action of the lipoic acid ligase LplA1. Journal of Bacteriology, 192, 6172-6181.
32. Randall D.D., Miernyk J.A., Fang T.K., Budde R.J., Schuller K.A. (1989) Regulation of the pyruvate dehydrogenase complexes in plants. Annals of the New York Academy of Sciences, 573, 192-205.
33. Rébeillé F., Alban C., Bourguignon J., Ravanel S., Douce R. (2007) The role of plant mitochondria in the biosynthesis of coenzymes. Photosynthesis Research, 92, 149-162.
34. Salvi D., Rolland N., Joyard J., Ferro M. (2008) Purification and proteomic analysis of chloroplasts and their sub-organellar compartments. In: Pflieger D., Rossier J. (Eds), Organelle proteomics. Humana Press, Totowa, NJ, USA, pp. 19-36.
35. Schonauer M.S., Kastaniotis A.J., Kursu V.A.S., Hiltunen J.K., Dieckmann C.L. (2009) Lipoic acid synthesis and attachment in yeast mitochondria. Journal of Biological Chemistry, 284, 23234-23242.
36. Spalding M.D., Prigge S.T. (2010) Lipoic acid metabolism in microbial pathogens. Microbiology and Molecular Biology Reviews, 74, 200-228.
37. Wada H., Shintani D., Ohlrogge J. (1997) Why do mitochondria synthesize fatty acids? Evidence for involvement in lipoic acid production. Proceedings of the National Academy of Sciences USA, 94, 1591-1596.
38. Wada M., Yasuno R., Jordan S.W., Cronan J.E., Wada H. (2001a) Lipoic acid metabolism in Arabidopsis thaliana: cloning and characterization of a cDNA encoding lipoyltransferase. Plant and Cell Physiology, 42, 650-656.
39. Wada M., Yasuno R., Wada H. (2001b) Identification of an Arabidopsis cDNA encoding a lipoyltransferase located in plastids. FEBS Letters, 506, 286-290.
40. Wendt U.K., Wenderoth I., Tegeler A., Von Schaewen A. (2000) Molecular characterization of a novel glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). The Plant Journal, 23, 723-733.
41. Yasuno R., Wada H. (1998) Biosynthesis of lipoic acid in Arabidopsis: cloning and characterization of the cDNA for lipoic acid synthase. Plant Physiology, 118, 935-943.
42. Yasuno R., Wada H. (2002) The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. FEBS Letters, 517, 110-114.
43. Yasuno R., von Wettstein-Knowles P., Wada H. (2004) Identification and molecular characterization of the β-ketoacyl-[acyl carrier protein] synthase component of the Arabidopsis mitochondrial fatty acid synthase. Journal of Biological Chemistry, 279, 8242-8251.
44. Zhao X., Miller J.R., Jiang Y., Marletta M.A., Cronan J.E. (2003) Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chemistry and Biology, 10, 1293-1302.
45. Zhao X., Miller J.R., Cronan J.E. (2005) The reaction of LipB, the octanoyl-[acyl carrier protein]:protein N-octanoyltransferase of lipoic acid synthesis, proceeds through an acyl-enzyme intermediate. Biochemistry, 44, 16737-16746.