The small subunit of snapdragon geranyl diphosphate synthase modifies the chain length specificity of tobacco geranylgeranyl diphosphate synthase in planta

Plant Cell

Volumn 21, Issue 12, 2009, Pages 4002-4017

  Orlova, Irina ^a   Nagegowda, Dinesh A ^a,b   Kish, Christine M ^a   Gutensohn, Michael ^a   Maeda, Hiroshi ^a   Varbanova, Marina ^b   Fridman, Eyal ^b   Yamaguchi, Shinjiro ^c   Hanada, Atsushi ^c   Kamiya, Yuji ^c   Krichevsky, Alexander ^d   Citovsky, Vitaly ^d   Pichersky, Eran ^b   Dudareva, Natalia ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c RIKEN   (Japan)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRRHINUM; ANTIRRHINUM MAJUS; NICOTIANA TABACUM;

EID: 75649145887     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.071282     Document Type: Article

References (73)

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., Ri, M., Giri, A.P., Verstappen, F. W., Schwab, W., and Bouwmeester, H.J. (2006). Metabolic engineering of terpenoid biosynthesis in plants. Phytochem. Rev. 5: 49-58.
5. Ament, K., Van Schie, C.C., Bouwmeester, H.J., Haring, M.A., and Schuurink, R.C. (2006). Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E,E)-4,8,12-trimethyltrideca1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta 224: 1197-1208.
6. Bick, J.A., and Lange, B.M. (2003). Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch. Biochem. Biophys. 415: 146-154.
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. Bouvier, F., Suire, C., d'Harlingue, A., Backhaus, R.A., and Camara, B. (2000). Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J. 24: 241-252.
9. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72: 248-254.
10. Burke, C.C., and Croteau, R. (2002a). Interactions with the small subunit of geranyl diphosphate synthase modifies the chain length specificity of geranylgeranyl diphosphate synthase to produce geranyl diphosphate. J. Biol. Chem. 277: 3141-3149.
11. Burke, C.C., and Croteau, R. (2002b). Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch. Biochem. Biophys. 405: 130-136.
12. Burke, C.C., Wildung, M.R., and Croteau, R. (1999). Geranyl diphosphate synthase: Cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc. Natl. Acad. Sci. USA 96: 13062-13067.
13. Citovsky, V., Gafni, Y., and Tzfira, T. (2008). Localizing protein-protein interactions by bimolecular fluorescence complementation in planta. Methods 45: 196-206.
14. Cordoba, E., Salmi, M., and León, P. (2009). Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J. Exp. Bot. 60: 2933-2943.
15. Croteau, R.B., Davis, E.M., Ringer, K.L., and Wildung, M.R. (2005). (-)-Menthol biosynthesis and molecular genetics. Naturwissenschaften 92: 562-577.
16. Croteau, R., and Purkett, P.T. (1989). Geranyl pyrophosphate synthase: Characterization of the enzyme and evidence that this chainlength specific prenyltransferase is associated with monoterpene biosynthesis in sage (Salvia officinalis). Arch. Biochem. Biophys. 271: 524-535.
17. Cseke, L., Dudareva, N., and Pichersky, E. (1998). Structure and evolution of linalool synthase. Mol. Biol. Evol. 15: 1491-1498.
18. Curtis, I.S., Davey, M.R., and Power, J.B. (1995). Leaf disk transformation. Methods Mol. Biol. 44: 59-70.
19. Donath, J., and Boland, W. (1995). Biosynthesis of acyclic homoterpenes: Enzyme selectivity and absolute configuration of the nerolidol precursor. Phytochemistry 39: 785-790.
20. 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.
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 methyl benzoate biosynthesis and emission in snapdragon flowers. Plant Cell 12: 949-961.
22. Eckenrode, V.K., Arnold, J., and Meagher, R.B. (1985). Comparison of the nucleotide sequence of soybean 18S rRNA with the sequences of the other small-subunit rRNA. J. Mol. Evol. 21: 259-269.
23. Estévez, J.M., Cantero, A., Reindl, A., Reichler, S., and León, P. (2001).1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem. 276: 22901-22909.
24. Gershenzon, J., and Dudareva, N. (2007). The function of terpene natural products in the natural world. Nat. Chem. Biol. 3: 408-414.
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, M. Wink, ed (Boca Raton, FL: CRC Press), pp. 222-299.
26. Goldberg, R.B. (1988). Plants: Novel developmental processes. Science 240: 1460-1467.
27. Hampel, D., Mosandl, A., and Wüst, M. (2005a). Biosynthesis of monoand sesquiterpenes in carrot roots and leaves (Daucus carota L.): Metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. Phytochemistry 66: 305-311.
28. Hampel, D., Mosandl, A., and Wüst, M. (2005b). Induction of de novo volatile terpene biosynthesis via cytosolic and plastidial pathways by methyl jasmonate in foliage of Vitis vinifera L. J. Agric. Food Chem. 53: 2652-2657.
29. Hemmerlin, A., Hoeffler, 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 plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J. Biol. Chem. 278: 26666-26676.
30. Kang, F., and Rawsthorne, S. (1994). Starch and fatty acid synthesis in plastids from developing embryos of oilseed rape (Brassica napus L.). Plant J. 6: 795-805.
31. Koeduka, T., Orlova, I., Baiga, T.J., Noel, J.P., Dudareva, N., and Pichersky, E. (2009). The lack of floral synthesis and emission of isoeugenol in Petunia axillaris subsp. parodii is due to a mutation in the isoeugenol synthase gene. Plant J. 58: 961-969.
32. Koltunow, A.M., Truettner, J., Cox, K.H., Wallroth, M., and Goldberg, R.B. (1990). Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2: 1201-1224.
33. Koyama, T., and Ogura, K. (1999). Isopentenyl diphosphate isomerase and prenyltransferases. In Comprehensive Natural Product Chemistry: Isoprenoids Including Carotenoids and Steroids, Vol. 2, D.E. Cane, ed (Oxford, UK: Pergamon Press), pp. 69-96.
34. Kuzuyama, T., Shimizu, T., Takahashi, S., and Seto, H. (1998). Fosmidomycin, a specific inhibitor of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett. 39: 7913-7916.
35. Laule, O., Furholz, A., Chang, H.-S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., and Lange, B.M. (2003). Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100: 6866-6871.
36. Lee, K.H., Kim, D.H., Lee, S.W., Kim, Z.H., and Hwang, I. (2002). In vivo import experiments in protoplasts reveal the importance of the overall context but not specific amino acid residues of the transit peptide during import into chloroplasts. Mol. Cells 14: 388-397.
37. Lee, L.-Y., and Gelvin, S.B. (2008). T-DNA binary vectors and systems. Plant Physiol. 146: 325-332.
38. 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.
39. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol. 148: 350-382.
40. Ling, Y., Li, Z.H., Miranda, K., Oldfield, E., and Moreno, S.N. (2007). The farnesyl-diphosphate/geranylgeranyl-diphosphate synthase of Toxoplasma gondii is a bifunctional enzyme and a molecular target of bisphosphonates. J. Biol. Chem. 282: 30804-30816.
41. Lücker, J., Bouwmeester, H.J., Schwab, W., Blaas, J., van der Plas, L.H., and Verhoeven, H.A. (2001). Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-beta-D-glucopyranoside. Plant J. 27: 315-324.
42. Lücker, J., Schwab, W., van Hautum, B., Blaas, J., van der Plas, L.H., Bouwmeester, H.J., and Verhoeven, H.A. (2004). Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiol. 134: 510-519.
43. Martin, D.M., Gershenzon, J., and Bohlmann, J. (2003). Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol. 132: 1586-1599.
44. McCaskill, D., and Croteau, R. (1995). Isoprenoid synthesis in peppermint (Mentha x piperita): Development of a model system for measuring flux of intermediates through the mevalonic acid pathway in plants. Biochem. Soc. Trans. 23: 290S.
45. McGarvey, D.J., and Croteau, R. (1995). Terpenoid metabolism. Plant Cell 7: 1015-1026.
46. Nagegowda, D.A., Gutensohn, M., Wilkerson, C.G., and Dudareva, N. (2008). Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. Plant J. 55: 224-239.
47. Narita, K., Ohnuma, S., and Nishino, T. (1999). Protein design of geranyl diphosphate synthase. Structural features that define the product specificities of prenyltransferases. J. Biochem. 126: 566-571.
48. 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.
49. Okada, K., Saito, T., Nakagawa, T., Kawamukai, M., and Kamiya, Y. (2000). Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol. 122: 1045-1056.
50. Orlova, I., Marshall-Colón, A., Schnepp, J., Wood, B., Varbanova, M., Fridman, E., Blakeslee, J.J., Peer, W.A., Murphy, A.S., Rhodes, D., Pichersky, E., and Dudareva, N. (2006). Reduction of benzenoid synthesis in petunia flowers reveals multiple pathways to benzoic acid and enhancement in auxin transport. Plant Cell 18: 3458-3475.
51. Otsuka, M., Kenmoku, H., Ogawa, M., Okada, K., Mitsuhashi, W., Sassa, T., Kamiya, Y., Toyomasu, T., and Yamaguchi, S. (2004). Emission of ent-kaurene, a diterpenoid hydrocarbon precursor for gibberellins, into the headspace from plants. Plant Cell Physiol. 45: 1129-1138.
52. Pateraki, I., and Kanellis, A.K. (2008). Isolation and functional analysis of two Cistus creticus cDNAs encoding geranylgeranyl diphosphate synthase. Phytochemistry 69: 1641-1652.
53. Phillips, M.A., D'Auria, J.C., Gershenzon, J., and Pichersky, E. (2008). The Arabidopsis thaliana type 1 isopentenyl diphosphate isomerase are targeted to multiple subcellular compartments and gave overlapping functions in isoprenoid biosynthesis. Plant Cell 20: 677-696.
54. Phillips, M.A., Walter, M.H., Ralph, S.G., Dabrowska, P., Luck, K., Urós, E.M., Boland, W., Strack, D., Rodríguez-Concepción, M., Bohlmann, J., and Gershenzon, J. (2007). Functional identification and differential expression of 1-deoxy-D-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol. Biol. 65: 243-257.
55. Rodríguez-Concepción, 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.
56. 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.
57. Sapir-Mir, M., Mett, A., Belausov, E., Tal-Meshulam, S., Frydman, A., Gidoni, D., and Eyal, Y. (2008). Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol. 148: 1219-1228.
58. Schilmiller, A.L., Schauvinhold, I., Larson, M., Xu, R., Charbonneau, A.L., Schmidt, A., Wilkerson, C., Last, R.L., and Pichersky, E. (2009). Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proc. Natl. Acad. Sci. USA 106: 10865-10870.
59. Schmidt, A., and Gershenzon, J. (2008). Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 96: 49-57.
60. 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.
61. Sheen, J. (2002). A transient expression assay using Arabidopsis mesophyll protoplasts. Available at http://genetics.mgh.harvard.edu/ sheenweb/
62. 2H labeling studies. Phytochemistry 60: 13-20.
63. Takahashi, S., Kuzuyama, T., Watanabe, H., and Seto, H. (1998). A 1-deoxy-d-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-d-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc. Natl. Acad. Sci. USA 95: 9879-9884.
64. Tholl, D., Croteau, R., and Gershenzon, J. (2001). Partial purification and characterization of the short-chain prenyltransferases, geranyl diphosphate synthase and farnesyl diphosphate synthase, from Abies grandis (grand fir). Arch. Biochem. Biophys. 386: 233-242.
65. 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.
66. van Schie, C.C.N., Ament, K., Schmidt, A., Lange, T., Haring, M.A., and Schuurink, R.C. (2007). Geranyl diphosphate synthase is required for biosynthesis of gibberellins. Plant J. 52: 752-762.
67. Varbanova, M., et al. (2007). Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19: 32-45.
68. Wagner, K.H., and Elmadfa, I. (2003). Biological relevance of terpenoids: Overview focusing on mono-, di and tetraterpenes. Ann. Nutr. Metab. 47: 95-106.
69. Wang, G., and Dixon, R.A. (2009). Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc. Natl. Acad. Sci. USA 106: 9914-9919.
70. Wang, K., and Ohnuma, S.-I. (1999). Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. Trends Biochem. Sci. 24: 445-451.
71. Wildung, M.R., and Croteau, R.B. (2005). Genetic engineering of peppermint for improved essential oil composition and yield. Transgenic Res. 14: 365-372.
72. Wise, M.L., and Croteau, R. (1999). Monoterpene biosynthesis. In Comprehensive Natural Product Chemistry: Isoprenoids Including Carotenoids and Steroids, Vol. 2, D.E. Cane, ed (Oxford, UK: Pergamon Press), pp. 97-153.
73. 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.