A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production

Plant Journal

Volumn 60, Issue 2, 2009, Pages 292-302

  Moerkercke, Alex Van ^a   Schauvinhold, Ines ^b   Pichersky, Eran ^b   Haring, Michel A ^a   Schuurink, Robert C ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

oxidation; 3 ketoacyl CoA thiolase; Benzenoids; Benzoic acid; Floral volatiles; Petunia

Indexed keywords

ACETYL COENZYME A ACYLTRANSFERASE; BENZOIC ACID; COMPLEMENTARY DNA; ESSENTIAL OIL; PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; ENZYMOLOGY; FLOWER; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PEROXISOME; PETUNIA; TRANSGENIC PLANT;

ACETYL-COA C-ACYLTRANSFERASE; BENZOIC ACID; DNA, COMPLEMENTARY; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; MOLECULAR SEQUENCE DATA; OILS, VOLATILE; PEROXISOMES; PETUNIA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA, PLANT;

PETUNIA; PETUNIA X HYBRIDA;

EID: 70349854538     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03953.x     Document Type: Article

References (54)

1. Abd El-Mawla, A.M. Beerhues, L. (2002) Benzoic acid biosynthesis in cell cultures of Hypericum androsaemum. Planta, 214, 727 733.
2. Afitlhile, M.M., Fukushige, H., Nishimura, M. Hildebrand, D.F. (2005) A defect in glyoxysomal fatty acid beta-oxidation reduces jasmonic acid accumulation in Arabidopsis. Plant Physiol. Biochem. 43, 603 609.
3. Angenent, G.C., Busscher, M., Franken, J., Mol, J.N. van Tunen, A.J. (1992) Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant Cell, 4, 983 993.
4. Beuerle, T. Pichersky, E. (2002) Purification and characterization of benzoate:coenzyme A ligase from Clarkia breweri. Arch. Biochem. Biophys. 400, 258 264.
5. Boatright, J., Negre, F., Chen, X., Kish, C.M., Wood, B., Peel, G., Orlova, I., Gang, D., Rhodes, D. Dudareva, N. (2004) Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135, 1993 2011.
6. Burns, K.L., Gelbaum, L.T., Sullards, M.C., Bostwick, D.E. May, S.W. (2005) Iso-coenzyme A. J. Biol. Chem. 280, 16550 16558.
7. Carrie, C., Murcha, M.W., Millar, A.H., Smith, S.M. Whelan, J. (2007) Nine 3-ketoacyl-CoA thiolases (KATs) and acetoacetyl-CoA thiolases (ACATs) encoded by five genes in Arabidopsis thaliana are targeted either to peroxisomes or cytosol but not to mitochondria. Plant Mol. Biol. 63, 97 108.
8. Dexter, R., Qualley, A., Kish, C.M., Ma, C.J., Koeduka, T., Nagegowda, D.A., Dudareva, N., Pichersky, E. Clark, D. (2007) Characterization of a petunia acetyltransferase involved in the biosynthesis of the floral volatile isoeugenol. Plant J. 49, 265 275.
9. Dexter, R.J., Verdonk, J.C., Underwood, B.A., Shibuya, K., Schmelz, E.A. Clark, D.G. (2008) Tissue-specific PhBPBT expression is differentially regulated in response to endogenous ethylene. J. Exp. Bot. 59, 609 618.
10. van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P., Pereira, A. Stiekema, W.J. (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res. 4, 288 290.
11. Footitt, S., Slocombe, S.P., 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 2922.
12. Germain, V., Rylott, E.L., Larson, T.R., Sherson, S.M., Bechtold, N., Carde, J.P., Bryce, J.H., Graham, I.A. Smith, S.M. (2001) Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid beta-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J. 28, 1 12.
13. Gietl, C. (1990) Glyoxysomal malate dehydrogenase from watermelon is synthesized with an amino-terminal transit peptide. Proc. Natl Acad. Sci. USA, 87, 5773 5777.
14. Hayashi, M., Toriyama, K., Kondo, M. Nishimura, M. (1998) 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid beta-oxidation. Plant Cell, 10, 183 195.
15. Hertweck, C., Jarvis, A.P., Xiang, L., Moore, B.S. Oldham, N.J. (2001) A mechanism of benzoic acid biosynthesis in plants and bacteria that mirrors fatty acid beta-oxidation. Chembiochem 2, 784 786.
16. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science 227, 1229 1231.
17. Ibdah, M., Chen, Y.T., Wilkerson, C.G. Pichersky, E. (2009) An aldehyde oxidase in developing seeds of Arabidopsis thaliana converts benzaldehyde to benzoic acid. Plant Physiol. 150, 416 423.
18. Jarvis, A.P., Schaaf, O. Oldham, N.J. (2000) 3-Hydroxy-3-phenylpropanoic acid is an intermediate in the biosynthesis of benzoic acid and salicylic acid but benzaldehyde is not. Planta, 212, 119 126.
19. Johnson, T.L. Olsen, L.J. (2003) Import of the peroxisomal targeting signal type 2 protein 3-ketoacyl-coenzyme a thiolase into glyoxysomes. Plant Physiol. 133, 1991 1999.
20. Kaminaga, Y., Schnepp, J., Peel, G. et al. (2006) Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J. Biol. Chem. 281, 23357 23366.
21. Karimi, M., Inze, D. Depicker, A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193 195.
22. Kliebenstein, D.J., D'Auria, J.C., Behere, A.S., Kim, J.H., Gunderson, K.L., Lee, G., Gershenzon, J., Last, R.L. Jander, G. (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J. 51, 1062 1076.
23. Koeduka, T., Fridman, E., Gang, D.R. et al. (2006) Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. Proc. Natl Acad. Sci. USA, 103, 10128 10133.
24. Koes, R., Verweij, W. Quattrocchio, F. (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10, 236 242.
25. Kolosova, N., Gorenstein, N., Kish, C.M. Dudareva, N. (2001a) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell, 13, 2333 2347.
26. Kolosova, N., Sherman, D., Karlson, D. Dudareva, N. (2001b) Cellular and subcellular localization of S-adenosyl-l-methionine:benzoic acid carboxyl methyltransferase, the enzyme responsible for biosynthesis of the volatile ester methylbenzoate in snapdragon flowers. Plant Physiol. 126, 956 964.
27. Kremers, G.J., Goedhart, J., van den Heuvel, D.J., Gerritsen, H.C. Gadella, T.W. Jr. (2007) Improved green and blue fluorescent proteins for expression in bacteria and mammalian cells. Biochemistry 46, 3775 3783.
28. Lange, P.R., Eastmond, P.J., Madagan, K. Graham, I.A. (2004) An Arabidopsis mutant disrupted in valine catabolism is also compromised in peroxisomal fatty acid beta-oxidation. FEBS Lett. 571, 147 153.
29. Long, M.C., Nagegowda, D.A., Kaminaga, Y., Ho, K.K., Kish, C.M., Schnepp, J., Sherman, D., Weiner, H., Rhodes, D. Dudareva, N. (2009) Involvement of snapdragon benzaldehyde dehydrogenase in benzoic acid biosynthesis. Plant J. 59, 256 265.
30. Loscher, R. Heide, L. (1994) Biosynthesis of p-hydroxybenzoate from p-coumarate and p-coumaroyl-coenzyme a in cell-free extracts of Lithospermum erythrorhizon cell cultures. Plant Physiol. 106, 271 279.
31. Negre, F., Kish, C.M., Boatright, J., Underwood, B., Shibuya, K., Wagner, C., Clark, D.G. Dudareva, N. (2003) Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers. Plant Cell, 15, 2992 3006.
32. Nelson, B.K., Cai, X. Nebenfuhr, A. (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126 1136.
33. Orlova, I., Marshall-Colon, A., Schnepp, J. et al. (2006) Reduction of benzenoid synthesis in petunia flowers reveals multiple pathways to benzoic acid and enhancement in auxin transport. Plant Cell, 18, 3458 3475.
34. Petriv, O.I., Tang, L., Titorenko, V.I. Rachubinski, R.A. (2004) A new definition for the consensus sequence of the peroxisome targeting signal type 2. J. Mol. Biol. 341, 119 134.
35. Pichersky, E. Dudareva, N. (2007) Scent engineering: toward the goal of controlling how flowers smell. Trends Biotechnol. 25, 105 110.
36. Podstolski, A., Havkin-Frenkel, D., Malinowski, J., Blount, J.W., Kourteva, G. Dixon, R.A. (2002) Unusual 4-hydroxybenzaldehyde synthase activity from tissue cultures of the vanilla orchid Vanilla planifolia. Phytochemistry 61, 611 620.
37. Reumann, S. (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 135, 783 800.
38. Ribnicky, D.M., Shulaev, V. Raskin, I. (1998) Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol. 118, 565 572.
39. Schnitzler, J.P., Madlung, J., Rose, A. Seitz, H.U. (1992) Biosynthesis of p-hydroxybenzoic acid in elicitor-treated carrot cell cultures. Planta, 188, 594 600.
40. Schuurink, R.C., Haring, M.A. Clark, D.G. (2006) Regulation of volatile benzenoid biosynthesis in petunia flowers. Trends Plant Sci. 11, 20 25.
41. Shang, Y., Schwinn, K.E., Bennett, M.J., Hunter, D.A., Waugh, T.L., Pathirana, N.N., Brummell, D.A., Jameson, P.E. Davies, K.M. (2007) Methods for transient assay of gene function in floral tissues. Plant Methods, 3, 1.
42. Stuurman, J., Hoballah, M.E., Broger, L., Moore, J., Basten, C. Kuhlemeier, C. (2004) Dissection of floral pollination syndromes in Petunia. Genetics, 168, 1585 1599.
43. Tilton, G.B., Shockey, J.M. Browse, J. (2004) Biochemical and molecular characterization of ACH2, an acyl-CoA thioesterase from Arabidopsis thaliana. J. Biol. Chem. 279, 7487 7494.
44. Underwood, B.A., Tieman, D.M., Shibuya, K., Dexter, R.J., Loucas, H.M., Simkin, A.J., Sims, C.A., Schmelz, E.A., Klee, H.J. Clark, D.G. (2005) Ethylene-regulated floral volatile synthesis in petunia corollas. Plant Physiol. 138, 255 266.
45. Verdonk, J.C., de Vos, C.H.R., Verhoeven, H.A., Haring, M.A., van Tunen, A.J. Schuurink, R.C. (2003) Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry 62, 997 1008.
46. Verdonk, J.C., Haring, M.A., van Tunen, A.J. Schuurink, R.C. (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell, 17, 1612 1624.
47. Verdonk, J.C., Haring, M.A., van Tunen, A.J. Schuurink, R.C. (2006) Targeted transcriptomics to elucidate the regulation of benzenoid synthesis in Petunia hybrida. In Floriculture, Ornamental and Plant Biotechnology (Teixara da Silva, J.A., ed.). UK : Global Science Books, pp. 326 338.
48. Vermeer, J.E., Thole, J.M., Goedhart, J., Nielsen, E., Munnik, T. Gadella, T.W. Jr. (2008) Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant J. 57, 356 372.
49. + P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat. Cell Biol. 10, 1456 1462.
50. Wildermuth, M.C. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562 565.
51. Wildermuth, M.C. (2006) Variations on a theme: synthesis and modification of plant benzoic acids. Curr. Opin. Plant Biol. 9, 288 296.
52. Xiang, L. Moore, B.S. (2003) Characterization of benzoyl coenzyme a biosynthesis genes in the enterocin-producing bacterium "Streptomyces maritimus". J. Bacteriol. 185, 399 404.
53. Zhang, K. Zuo, Y.G. (2004) GC-MS determination of flavonoids and phenolic and benzoic acids in human plasma after consumption of cranberry juice. J. Agric. Food. Chem. 52, 222 227.
54. Zolman, B.K., Monroe-Augustus, M., Thompson, B., Hawes, J.W., Krukenberg, K.A., Matsuda, S.P. Bartel, B. (2001) Chy1, an Arabidopsis mutant with impaired beta-oxidation, is defective in a peroxisomal beta-hydroxyisobutyryl-CoA hydrolase. J. Biol. Chem. 276, 31037 31046.