Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers

Plant Journal

Volumn 55, Issue 2, 2008, Pages 224-239

  Nagegowda, Dinesh A ^a   Gutensohn, Michael ^b   Wilkerson, Curtis G ^c   Dudareva, Natalia ^a  

^a PURDUE UNIVERSITY   (United States)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Floral volatiles; Linalool; Nerolidol; Snapdragon; Terpene synthases

Indexed keywords

ANTIRRHINUM;

LINALOOL; NEROLIDOL; SESQUITERPENE; TERPENE; TERPENE SYNTHASE; TRANSFERASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANTIRRHINUM; ARTICLE; CHEMISTRY; ENZYMOLOGY; FLOWER; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY;

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; ANTIRRHINUM; FLOWERS; MOLECULAR SEQUENCE DATA; MONOTERPENES; PHYLOGENY; PLANT PROTEINS; SESQUITERPENES;

EID: 55249088798     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03496.x     Document Type: Article

References (66)

1. Aharoni, A., Giri, A.P., Deuerlein, S., Griepink, F., de Kogel, W.J., Verstappen, F.W., Verhoeven, H.A., Jongsma, M.A., Schwab, W. and Bouwmeester, H.J. (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell, 15, 2866-2884.
2. Aharoni, A., Giri, A.P., Verstappen, F.W., Bertea, C.M., Sevenier, R., Sun, Z., Jongsma, M.A., Schwab, W. and Bouwmeester, H.J. (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell, 16, 3110-3131.
3. Aharoni, A., Jongsma, M.A. and Bouwmeester, H.J. (2005) Volatile science? Metabolic engineering of terpenoids in plants Trends Plant Sci. 10, 594-602.
4. Aharoni, A., Jongsma, M.A., Kim, T.Y., Ri, M.B., Giri, A.P., Verstappen, W.A., Schwab, W. and Bouwmeester, H.J. (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochem. Rev. 5, 49-58.
5. Aubourg, S., Lecharny, A. and Bohlmann, J. (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol. Genet. Genomics, 267, 730-745.
6. Bey, M., Stuber, K., Fellenberg, K., Schwarz-Sommer, Z., Sommer, H., Saedler, H. and Zachgo, S. (2004) Characterization of Antirrhinum petal development and identification of target genes of the class B MADS box gene DEFICIENS. Plant Cell, 16, 3197-3215.
7. Boatright, J., Negre, F., Chen, X., Kish, C.M., Wood, B., Peel, G., Orlova, I., Gang, D., Rhodes, D. and Dudareva, N. (2004) Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135, 1993-2011.
8. Bohlmann, J., Crock, J., Jetter, R. and Croteau, R.B. (1998a) Terpenoid-based defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). Proc. Natl Acad. Sci. USA, 95, 6756-6761.
9. Bohlmann, J., Meyer-Gauen, G. and Croteau, R. (1998b) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc. Natl Acad. Sci. USA, 95, 4126-4133.
10. Bradford, M.M. (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.
11. Cane, D.E. (1999) Sesquiterpene biosynthesis: cyclization mechanisms. In Comprehensive Natural Products Chemistry, Vol. 2, Isoprenoids Including Carotenoids and Steroids (Cane, D.D., ed.). Amsterdam: Elsevier, pp. 155-200.
12. Chen, F., Tholl, D., D'auria, J.C., Farooq, A., Pichersky, E. and Gershenzon, J. (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell, 15, 1-15.
13. Chen, H., Wilkerson, C.G., Kuchar, J.A., Phinney, B.S. and Howe, G.A. (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc. Natl Acad. Sci. USA, 102, 19237-19242.
14. Colby, S.M., Crock, J., Dowdle-Rizzo, B., Lemaux, P.G. and Croteau, R. (1998) Germacrene C synthase from Lycopersicon esculentum cv. VFNT cherry tomato: cDNA isolation, characterization, and bacterial expression of the multiple product sesquiterpene cyclase. Proc. Natl Acad. Sci. USA, 95, 2216-2221.
15. Crock, J., Wildung, M. and Croteau, R. (1997) Isolation and bacterial expression of a sesquiterpene synthase cDNA clone from peppermint (Mentha x piperita, L.) that produces the aphid alarm pheromone (E)-β-farnesene. Proc. Natl Acad. Sci. USA, 94, 12833-12838.
16. Crowell, A.L., Williams, D.C., Davis, E.M., Wildung, M.R. and Croteau, R. (2002) Molecular cloning and characterization of a new linalool synthase. Arch. Biochem. Biophys. 405, 112-121.
17. Donath, J. and Boland, W. (1995) Biosynthesis of acyclic homoterpenes - enzyme selectivity and absolute configuration of the nerolidol precursor. Phytochemistry, 39, 785-790.
18. Dudareva, N. and Pichersky, E. (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol. 122, 627-633.
19. Dudareva, N., Cseke, L., Blanc, V.M. and Pichersky, E. (1996) Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell, 8, 1137-1148.
20. Dudareva, N., D'Auria, J.C., Nam, K.H., Raguso, R.A. and Pichersky, E. (1998) Acetyl-CoA:benzyl alcohol acetyltransferase: an enzyme involved in floral scent production in Clarkia breweri. Plant J. 14, 297-304.
21. Dudareva, N., Murfitt, L.M., Mann, C.J., Gorenstein, N., Kolosova, N., Kish, C.M., Bonham, C. and Wood, K. (2000) Developmental regulation of methylbenzoate biosynthesis and emission in snapdragon flowers. Plant Cell, 12, 949-961.
22. Dudareva, N., Martin, D., Kish, C.M., Kolosova, N., Gorenstein, N., Fäldt, J., Miller, B. and Bohlmann, J. (2003) (E)-β-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell, 15, 1227-1241.
23. Dudareva, N., Andersson, S., Orlova, I., Gatto, N., Reichelt, M., Rhodes, D., Boland, W. and Gershenzon, J. (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc. Natl Acad. Sci. USA, 102, 933-938.
24. Dudareva, N., Negre, F., Nagegowda, D.A. and Orlova, I. (2006) Plant volatiles: recent advances and future perspectives. Crit. Rev. Plant Sci. 25, 417-440.
25. Gershenzon, J. and Kreis, W. (1999) Biochemistry of terpenoids: monoterpenes, sesquiterpenes, diterpenes, sterols, cardiac glycosides and steroid saponins. In Biochemistry of Plant Secondary Metabolism (Wink, M., ed.). Boca Raton, FL: CRC Press, pp. 222-299.
26. Green, S., Friel, E.N., Matich, A., Beuning, L.L., Cooney, J.M., Rowan, D.D. and Macrae, E. (2007) Unusual features of a recombinant apple alpha-farnesene synthase. Phytochemistry, 68, 176-188.
27. 2H labeling studies. J. Agric. Food. Chem. 54, 1473-1478.
28. Hemmerlin, A., Hoeffer, J.F., Meyer, O., Tritsch, D., Kagan, I.A., Grosdemange-Billiard, C., Rohmer, M. and Bach, T.J. (2003) Cross-talk between the cytosolic mevalonate and the plastidal methylerythrito phosphate pathways in tobacco bright yellow-2 cells. J. Biol. Chem. 278, 26666-26676.
29. Hemmerlin, A., Tritsch, D., Hartmann, M., Pacaud, K., Hoeffler, J.F., van Dorsselaer, A., Rohmer, M. and Bach, T.J. (2006) A cytosolic Arabidopsis D-xylulose kinase catalyzes the phosphorylation of 1-deoxy-D-xylulose into a precursor of the plastidial isoprenoid pathway. Plant Physiol. 142, 441-457.
30. Iijima, Y., Davidovich-Rikanati, R., Fridman, E., Gang, D.R., Bar, E., Lewinsohn, E. and Pichersky, E. (2004) The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physiol. 136, 3724-3736.
31. Jia, J.W., Crock, J., Lu, S., Croteau, R. and Chen, X.Y. (1999) (3R)-Linalool synthase from Artemisia annua L.: cDNA isolation, characterization, and wound induction. Arch. Biochem. Biophys. 372, 143-149.
32. 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.
33. Kang, F. and Rawsthorne, S. (1994) Starch and fatty acid synthesis in plastids from developing embryos of oilseed rape. Plant J. 6, 795-805.
34. Knudsen, J.T. and Gershenzon, J. (2006) The chemical diversity of floral scent. In Biology of Floral Scent (Dudareva, N. and Pichersky, E., eds). Boca Raton [u.a.]: Taylor & Francis, pp. 27-52.
35. Kohlstaedt, L. (2006) TCA precipitation of proteins. Available at: http://biology.berkeley.edu/crl/mass-spec/TCA-precipitation-of-proteins.pdf.
36. Kollner, T.G., Schnee, C., Gershenzon, J. and Degenhardt, J. (2004) The variability of sesquiterpenes cultivars is controlled by allelic emitted from two Zea mays variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell, 16, 1115-1131.
37. Kolosova, N., Gorenstein, N., Kish, C.M. and Dudareva, N. (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell, 13, 2333-2347.
38. Koyama, T. and Ogura, K. (1999) Isopentenyl diphosphate isomerase and prenyltransferases. In Comprehensive Natural Product Chemistry, Vol. 2 (Barton, D. and Nakanishi, K., eds). Oxford: Elsevier Science Ltd, pp. 69-96.
39. Laule, O., Furholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W. and Lange, M. (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 100, 6866-6871.
40. Lichtenthaler, H.K. (1999) The 1-deoxy-D-xylulose-5- phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 47-65.
41. Martin, D.M., Fäldt, J. and Bohlmann, J. (2004) Functional characterization of nine Norway spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol. 135, 1908-1927.
42. McCaskill, D. and Croteau, R. (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha x piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta, 197, 49-56.
43. McGarvey, D.J. and Croteau, R. (1995) Terpenoid metabolism. Plant Cell, 7, 1015-1026.
44. Mercke, P., Crock, J., Croteau, R.B. and Brodelius, P.E. (1999) Cloning, expression, and characterization of epi-cedrol synthase, a sesquiterpene cyclase from Artemisia annua L. Arch. Biochem. Biophys. 369, 213-222.
45. Murfitt, L.M., Kolosova, N., Mann, C.J. and Dudareva, N. (2000) Purification and characterization of S-adenosyl-L-methionine: benzoic acid carboxyl methyltransferase, the enzyme responsible for biosynthesis of the volatile ester methyl benzoate in flowers of Antirrhinum majus. Arch. Biochem. Biophys. 382, 145-151.
46. Negre, F., Kolosova, N., Knoll, J., Kish, C.M. and Dudareva, N. (2002) Novel S-adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme responsible for biosynthesis of methylsalicylate and methylbenzoate, is not involved in floral scent production in snapdragon flowers. Arch. Biochem. Biophys. 406, 261-270.
47. Newman, J.D. and Chappell, J. (1999) Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. Crit. Rev. Biochem. Mol. Biol. 34, 95-106.
48. Ogura, K. and Koyama, T. (1998) Enzymatic aspects of isoprenoid chain elongation. Chem. Rev. 98, 1263-1276.
49. Pechous, S.W. and Whitaker, B.D. (2004) Cloning and functional expression of an (E,E)-a-farnesene synthase cDNA from peel tissue of apple fruit. Planta, 219, 84-94.
50. Perkins, D.N., Pappin, D.J., Creasy, D.M. and Cottrell, J.S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis, 20, 3551-3567.
51. Pichersky, E., Lewinsohn, E. and Croteau, R. (1995) Purification and characterization of S-linalool synthase, an enzyme involved in the production of floral scent in Clarkia breweri. Arch. Biochem. Biophys. 316, 803-807.
52. Poulter, C.D. and Rilling, H.C. (1981) Prenyl transferases and isomerase. In Biosynthesis of Isoprenoid Compounds, Vol. 1 (Porter, J.W. and Spurgeon, S.L., eds). New York, NY: John Wiley and Sons, pp. 162-209.
53. Rodriguez-Concepcion, M. and Boronat, A. (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130, 1079-1089.
54. Rohmer, M. (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat. Prod. Rep. 16, 565-574.
55. van Schie, C.C., Haring, M.A. and Schuurink, R.C. (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol. Biol. 64, 251-263.
56. Schnee, C., Köllner, T.G., Gershenzon, J. and Degenhardt, J. (2002) The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-beta-farnesene, (E)-nerolidol, and (E,E)-farnesol after herbivore damage. Plant Physiol. 130, 2049-2060.
57. Schuhr, C.A., Radykewicz, T., Sagner, S., Latzel, C., Zenk, M.H., Arigoni, D., Bacher, A., Rohdich, F. and Eisenreich, W. (2003) Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy. Phytochem. Rev. 2, 3-16.
58. Sheen, J. (2002) A transient expression assay using Arabidopsis mesophyll protoplasts. Available at http://genetics.mgh. harvard.edu/sheenweb/.
59. Smith, R.G., Gauthier, D.A., Dennis, D.T. and Turpin, D.H. (1992) Malate and pyruvate dehydrogenase-dependent fatty acid synthesis in leucoplasts from developing castor endosperm. Plant Physiol. 98, 1233-1238.
60. Steele, C.L., Crock, J., Bohlmann, J. and Croteau, R. (1998) Sesquiterpene synthases from grand fir (Abies grandis): comparison of constitutive and wound-induced activities, and cDNA isolation, characterization, and bacterial expression of δ-selinene synthase and γ-synthase. J. Biol. Chem. 273, 2078-2089.
61. Tholl, D. (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr. Opin. Plant Biol. 9, 297-304.
62. Tholl, D., Kish, C.M., Orlova, I., Sherman, D., Gershenzon, J., Pichersky, E. and Dudareva, N. (2004) Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell, 16, 977-992.
63. Tholl, D., Chen, F., Petri, J., Gershenzon, J. and Pichersky, E. (2005) Two sesquiterpene synthses are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J. 42, 757-771.
64. Williams, D.C., McGarvey, D.J., Katahira, E.J. and Croteau, R. (1998) Truncation of limonene synthase preprotein provides a fully active 'pseudomature' form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair. Biochemistry, 37, 12213-12220.
65. Wise, M.L. and Croteau, R. (1999) Monoterpene biosynthesis. In Comprehensive Natural Products Chemistry, Vol 2, Isoprenoids Including Carotenoids and Steroids (Cane, D.D., ed.). Amsterdam: Elsevier Science, pp. 97-153.
66. Wu, S., Schalk, M., Clark, A., Miles, R.B., Coates, R. and Chappell, J. (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat. Biotechnol. 24, 1441-1447.