Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination

Plant Cell

Volumn 17, Issue 7, 2005, Pages 2037-2048

  Pracharoenwattana, Itsara ^a   Cornah, Johanna E ^a,b   Smith, Steven M ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; FATTY ACIDS; OXIDATION; SEED; SYNTHESIS (CHEMICAL);

CARBON TRANSFER; FATTY ACID RESPIRATION; PEROXISOMES; SEED GERMINATION;

ENZYMES;

CATALYSTS; ENZYMES; FATTY ACIDS; GERMINATION; OXIDATION; SEEDS; SYNTHESIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CUCURBITA PEPO;

ACETYLCARNITINE; CITRATE SYNTHASE; CITRIC ACID; FATTY ACID; PLANT DNA; SUCROSE; TRIACYLGLYCEROL;

ARABIDOPSIS; ARTICLE; CELL RESPIRATION; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOCHONDRION; MUTATION; PEROXISOME; PHYSIOLOGY; PLANT SEED; SEEDLING;

ACETYLCARNITINE; ARABIDOPSIS; CELL RESPIRATION; CITRATE (SI)-SYNTHASE; CITRIC ACID; DNA, PLANT; FATTY ACIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GERMINATION; MITOCHONDRIA; MUTATION; PEROXISOMES; SEEDLING; SEEDS; SUCROSE; TRIGLYCERIDES;

EID: 33644802667     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.031856     Document Type: Article

References (47)

1. Adham, A.R., Zolman, B.K., Millius, A., and Bartel, B. (2005). Mutations in Arabidopsis acyl-CoA oxidase genes reveal distinct and overlapping roles in beta-oxidation. Plant J. 41, 859-874.
2. Alonso, J.M., al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
3. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R., and Gorlach, J. (2001). Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13, 1499-1510.
4. Bradford, M.M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 72, 248-254.
5. Browse, J., McCourt, P.J., and Somerville, C.R. (1986). Fatty-acid composition of leaf lipids determined after combined digestion and fatty-acid methyl-ester formation from fresh tissue. Anal. Biochem. 152, 141-145.
6. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
7. Cornah, J.E., Germain, V., Ward, J.L., Beale, M.H., and Smith, S.M. (2004). Lipid utilization, gluconeogenesis, and seedling growth in Arabidopsis mutants lacking the glyoxylate cycle enzyme malate synthase. J. Biol. Chem. 279, 42916-42923.
8. Cornah, J.E., and Smith, S.M. (2002). Synthesis and function of glyoxylate cycle enzymes. In Plant Peroxisomes, A. Baker and I.A. Graham, eds (London: Kluwer Academic Publishers), pp. 57-101.
9. Courtois-Verniquet, F., and Douce, R. (1993). Lack of aconitase in glyoxysomes and peroxisomes. Biochem. J. 294, 103-107.
10. De Bellis, L., Hayashi, M., Biagi, P.P., Haranishimura, I., Alpi, A., and Nishimura, M. (1994). Immunological analysis of aconitase in pumpkin cotyledons: The absence of aconitase in glyoxysomes. Physiol. Plant. 90, 757-762.
11. Dieuaide, M., Brouquisse, R., Pradet, A., and Raymond, P. (1992). Increased fatty acid β-oxidation after glucose starvation in maize root tips. Plant Physiol. 99, 595-600.
12. Eastmond, P.J., Germain, V., Lange, P.R., Bryce, J.H., Smith, S.M., and Graham, I.A. (2000). Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc. Natl. Acad. Sci. USA 97, 5669-5674.
13. Eastmond, P.J., and Graham, I.A. (2001). Re-examining the role of glyoxylate cycle in oilseeds. Trends Plant Sci. 6, 72-77.
14. Eccleston, V.S., and Ohlrogge, J.B. (1998). Expression of lauroyl-acyl carrier protein thioesterase in Brassica napus seeds induces pathways for both fatty acid oxidation and biosynthesis and implies a set point for triacylglycerol accumulation. Plant Cell 10, 613-622.
15. Elgersma, Y., Van Roermund, C.W.T., Wanders, R.J.A., and Tabak, H.F. (1995). Peroxisomal and mitochondrial carnitine acetyltransferases of Saccharomyces cerevisiae are encoded by a single gene. EMBO J. 14, 3472-3479.
16. Footitt, S., Slocombe, S.P., Larner, V., Kurup, S., Wu, Y., Larson, T., Graham, I., Baker, A., and Holdsworth, M. (2002). Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 21, 2912-2922.
17. Fulda, M., Schnurr, J., Abbadi, A., Heinz, E., and Browse, J. (2004). Peroxisomal acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16, 394-405.
18. Germain, V., Rylott, E.L., Larson, T.R., Sherson, S.M., Bechtold, N., Carde, J.P., Bryce, J.H., Graham, I.A., and Smith, S.M. (2001). Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid β-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J. 28, 1-12.
19. Hayashi, M., De Bellis, L., Alpi, A., and Nishimura, M. (1995). Cytosolic aconitase participates in the glyoxylate cycle in etiolated pumpkin cotyledons. Plant Cell Physiol. 36, 669-680.
20. Hayashi, M., Masahiro, A., Kato, A., Kondo, M., and Nishimura, M. (1996). Transport of chimeric proteins that contain a carboxy-terminal targeting signal into plant microbodies. Plant J. 10, 225-234.
21. Hayashi, M., Nito, K., Takei-Hoshi, R., Yagi, M., Kondo, M., Suenaga, A., Yamaya, T., and Nishimura, M. (2002). Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid β-oxidation. Plant Cell Physiol. 43, 1-11.
22. Hayashi, M., Toriyama, K., Kondo, M., and Nishimura, M. (1998). 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid β-oxidation. Plant Cell 10, 183-195.
23. Heazlewood, J.L., Tonti-Filippini, J.S., Gout, A.M., Day, D.A., Whelan, J., and Millar, A.H. (2004). Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16, 241-256.
24. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: A versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
25. Hooks, M.A. (2002). Molecular biology, enzymology, and physiology of β-oxidation. In Plant Peroxisomes, A. Baker and I.A. Graham, eds (London: Kluwer Academic Publishers), pp. 19-55.
26. Hooks, M.A., Bode, K., and Couée, I. (1995). Regulation of acyl-CoA oxidases in maize seedlings. Phytochemistry 40, 657-660.
27. Kato, A., Hayashi, M., Kondo, M., and Nishimura, M. (1996). Targeting and processing of a chimeric protein with the N-terminal presequence of the precursor to glyoxysomal citrate synthase. Plant Cell 8, 1601-1611.
28. Kato, A., Hayashi, M., Mori, H., and Nishimura, M. (1995). Molecular characterization of a glyoxysomal citrate synthase that is synthesized as a precursor of higher molecular mass in pumpkin. Plant Mol. Biol. 27, 377-390.
29. Koncz, C., and Schell, J. (1986). The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
30. Krysan, P.J., Young, J.C., and Sussman, M.R. (1999). T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11, 2283-2290.
31. Kunau, W.H., Dommes, V., and Schulz, H. (1995). β-Oxidation of fatty acids in mitochondria, peroxisomes and bacteria: A century of continued progress. Prog. Lipid Res. 34, 267-342.
32. Lawand, S., Dorne, A.J., Long, D., Coupland, G., Mache, R., and Carol, P. (2002). Arabidopsis A BOUT DE SOUFFLE, which is homologous with mammalian carnitine acyl carrier, is required for postembryonic growth in the light. Plant Cell 14, 2161-2173.
33. Lee, J.G., Cho, S.P., Lee, H.S., Lee, C.H., Bae, K.S., and Maeng, P.J. (2000). Identification of a cryptic N-terminal signal in Saccharomyces cerevisiae peroxisomal citrate synthase that functions in both peroxisomal and mitochondrial targeting. J. Biochem. (Tokyo) 128, 1059-1072.
34. Lin, Y., Cluette-Brown, J.E., and Goodman, H.M. (2004). The peroxisome deficient Arabidopsis mutant sse1 exhibits impaired fatty acid synthesis. Plant Physiol. 135, 814-827.
35. Mettler, I.J., and Beevers, H. (1980). Oxidation of NADH in glyoxysomes by a malate-aspartate shuttle. Plant Physiol. 66, 555-560.
36. Picault, N., Palmieri, L., Pisano, I., Hodges, M., and Palmieri, F. (2002). Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria. Bacterial expression, reconstitution, functional characterization, and tissue distribution. J. Biol. Chem. 277, 24204-24211.
37. Raymond, P., Spiteri, A., Dieuaide, M., Gerhardt, B., and Pradet, A. (1992). Peroxisomal β-oxidation of fatty acids and citrate formation by a particulate fraction from early germinating sunflower seeds. Plant Physiol. Biochem. 30, 153-161.
38. Richmond, T., and Bleecker, A.B. (1999). A defect in β-oxidation causes abnormal inflorescence development in Arabidopsis. Plant Cell 11, 1911-1924.
39. Russell, L., Larner, V., Kurup, S., Bougourd, S., and Holdsworth, M. (2000). The Arabidopsis COMATOSE locus regulates germination potential. Development 127, 3759-3767.
40. Rylott, E.L., Rogers, C.A., Gilday, A.D., Edgell, T., Larson, T.R., and Graham, I.A. (2003). Arabidopsis mutants in short- and medium-chain acyl-CoA oxidase activities accumulate acyl-CoAs and reveal that fatty acid β-oxidation is essential for embryo development. J. Biol. Chem. 278, 21370-21377.
41. Schnarrenberger, C., Fitting, K.H., Tetour, M., and Zehler, H. (1980). Inactivation of the glyoxysomal citrate synthase from caster bean endosperm by 5,5′-dithio-bis(2-nitrobenzoic acid) (DTNB). Protoplasma 103, 299-307.
42. Seki, M., et al. (2002). Functional annotation of a full-length Arabidopsis cDNA collection. Science 296, 141-145.
43. Sessions, A., et al. (2002). A high-throughput Arabidopsis reverse genetics system. Plant Cell 14, 2985-2994.
44. Sherson, S.M., Hemmann, G., Wallace, G., Forbes, S., Germain, V., Stadler, R., Bechtold, N., Sauer, N., and Smith, S.M. (2000). Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. Plant J. 24, 849-857.
45. van Roermund, C.W.T., Elgersma, Y., Singh, N., Wanders, R.J.A., and Tabak, H.F. (1995). The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J. 14, 3480-3486.
46. van Roermund, C.W.T., Hettema, E.H., van den Berg, M., Tabak, H.F., and Wanders, R.J.A. (1999). Molecular characterisation of carnitine-dependent transport of acetyl-CoA from peroxisomes to mitochondria in Saccharomyces cerevisiae and identification of a plasma membrane carnitine transporter, Agp2p. EMBO J. 18, 5843-5852.
47. Zolman, B.K., Silva, I.D., and Bartel, B. (2001). The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. Plant Physiol. 127, 1266-1278.