Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants

Plant Cell

Volumn 15, Issue 12, 2003, Pages 2866-2884

  Aharoni, Asaph ^a   Giri, Ashok P ^a,c   Deuerlein, Stephan ^b   Griepink, Frans ^a   De Kogel, Willem Jan ^a   Verstappen, Francel W A ^a   Verhoeven, Harrie A ^a   Jongsma, Maarten A ^a   Schwab, Wilfried ^b,d   Bouwmeester, Harro J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c NATIONAL CHEMICAL LABORATORY   (India)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOLS; BIOSYNTHESIS; ENVIRONMENTAL IMPACT; ENZYMES; HYDROCARBONS; METABOLISM;

DIURNAL EMISSION PATTERN;

PLANTS (BOTANY);

APHIDIDAE; ARABIDOPSIS; MYZUS; MYZUS PERSICAE;

EID: 10744226660     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.016253     Document Type: Article

References (62)

1. Adam, K.P., and Zapp, J. (1998). Biosynthesis of the isoprene units of chamomile sesquiterpenes. Phytochemistry 48, 953-959.
2. Aharoni, A., et al. (2000). Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12, 647-661.
3. 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.
4. Behr, D., Wahlberg, I., Nishida, T., and Enzell, C.R. (1978). Tobacco chemistry. 45. (2E,6S)-2,6-dimethyl-2,7-octadiene-1,6-diol, a new monoterpenoid from Greek tobacco. Acta Chem. Scand. B 32, 228-234.
5. Bohlmann, J., Martin, D., Oldham, N.J., and Gershenzon, J. (2000). Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization, and functional expression of a myrcene/(E)-β-ocimene synthase. Arch. Biochem. Biophys. 375, 261-269.
6. Bohlmann, J., Meyer, G.G., and Croteau, R.B. (1998). Plant terpenoid synthases: Molecular biology and phylogenetic analysis. Proc. Natl. Acad. Sci. USA 95, 4126-4133.
7. Bohlmann, J., Phillips, M., Ramachandiran, V., Katoh, S., and Croteau, R.B. (1999). cDNA cloning, characterisation, and functional expression of four new monoterpene synthase members of the Tpsd gene family from grand fir (Abies grandis). Arch. Biochem. Biophys. 368, 232-243.
8. Bouwmeester, H.J., Kodde, J., Verstappen, F.W.A., Altug, I.G., de Kraker, J.W., and Wallaart, T.E. (2002). Isolation and characterization of two germacrene A synthase cDNA clones from chicory. Plant Physiol. 129, 134-144.
9. Bouwmeester, H.J., Verstappen, F.W.A., Posthumus, M.A., and Dicke, M. (1999). Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean: The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol. 121, 173-180.
10. Busch, M., Seuter, A., and Hain, R. (2002). Functional analysis of the early steps of carotenoid biosynthesis in tobacco. Plant Physiol. 128, 439-453.
11. Chappell, J., Wolf, F., Proulx, J., Cuellar, R., and Saunders, C. (1995). Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for isoprenoid biosynthesis in plants? Plant Physiol. 109, 1337-1343.
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, 481-494.
13. 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.
14. Colby, S.M., Crock, J., Dowdle, R.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. Cunillera, N., Boronat, A., and Ferrer, A. (1997). The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J. Biol. Chem. 272, 15381-15388.
16. Degenhardt, J., Gershenzon, J., Baldwin, I.T., and Kessler, A. (2003). Attracting friends to feast on foes: Engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr. Opin. Biotechnol. 14, 169-176.
17. de Kraker, J.W., Franssen, M.C.R., De Groot, A., Koenig, W.A., and Bouwmeester, H.J. (1998). (+)-Germacrene A biosynthesis: The committed step in the biosynthesis of bitter sesquiterpene lactones in chicory. Plant Physiol. 117, 1381-1392.
18. 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.
19. Fäldt, J., Arimura, G., Gershenzon, J., Takabayashi, J., and Bohlmann, J. (2003). Functional identification of AtTPS03 as (E)-β-ocimene synthase: A monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana. Planta 216, 745-751.
20. Fraser, P.D., Pinto, M.E.S., Holloway, D.E., and Bramley, P.M. (2000). Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J. 24, 551-558.
21. Fray, R.G., Wallace, A., Fraser, P.D., Valero, D., Hedden, P., Bramley, P.M., and Grierson, D. (1995). Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. Plant J. 8, 693-701.
22. Gols, R., Posthumus, M.A., and Dicke, M. (1999). Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis. Entomol. Exp. Appl. 93, 77-86.
23. Hedtke, B., Meixner, M., Gillandt, S., Richter, E., Borner, T., and Weihe, A. (1999). Green fluorescent protein as a marker to investigate targeting of organellar RNA polymerases of higher plants in vivo. Plant J. 17, 557-561.
24. Hohn, T.M., and Ohlrogge, J.B. (1991). Expression of a fungal sesquiterpene cyclase gene in transgenic tobacco. Plant Physiol. 97, 460-462.
25. Hollander, M., and Wolfe, D.A. (1973). Nonparametric Statistical Methods (New York: Wiley).
26. Hori, M. (1998). Repellency of rosemary oil against Myzus persicae in a laboratory and in a screenhouse. J. Chem. Ecol. 24, 1425-1432.
27. Kubo, I., Muroi, H., and Himejima, M. (1993). Antibacterial activity against Streptococcus mutans of mate tea flavor components. J. Agric. Food Chem. 41, 107-111.
28. Lange, M.B., Wildung, M.R., Stauber, E.J., Sanchez, C., Pouchnik, D., and Croteau, R.B. (2000). Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc. Natl. Acad. Sci. USA 97, 2934-2939.
29. Lavy, M., Zuker, A., Lewinsohn, E., Larkov, O., Ravid, U., Vainstein, A., and Weiss, D. (2002). Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene. Mol. Breed. 9, 103-111.
30. Lewinsohn, E., et al. (2001). Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol. 127, 1256-1265.
31. Lichtenthaler, H.K. (2000). Non-mevalonate isoprenoid biosynthesis: Enzymes, genes and inhibitors. Biochem. Soc. Trans. 28, 785-789.
32. Lücker, J., Bouwmeester, H.J., Schwab, W., Blaas, J., van der Plas, L.H.W., and Verhoeven, H.A. (2001). Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-β-D- glucopyranoside. Plant J. 27, 315-324.
33. Lücker, J., El-Tamer, M.K., Schwab, W., Verstappen, F.W.A., van der Plas, L.H.W., Bouwmeester, H.J., and Verhoeven, H.A. (2002). Monoterpene biosynthesis in lemon (Citrus limon): cDNA isolation and functional analysis of four monoterpene synthases. Eur. J. Biochem. 269, 3160-3171.
34. Mahmoud, S.S., and Croteau, R.B. (2002). Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci. 7, 366-373.
35. Marsch-Martinez, N., Greco, R., van Arkel, G., Herrera-Estrella, L., and Pereira, A. (2002). Activation tagging using the En-I maize transposon system in Arabidopsis. Plant Physiol. 129, 1544-1556.
36. Masferrer, A., Arro, M., Manzano, D., Schaller, H., Fernandez-Busquets, X., Moncalean, P., Fernandez, B., Cunillera, N., Boronat, A., and Ferrer, A. (2002). Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J. 30, 123-132.
37. McCaskill, D., and Croteau, R.B. (1998). Some caveats for bioengineering terpenoid metabolism in plants. Trends Biotechnol. 16, 349-355.
38. McConkey, M.E., Gershenzon, J., and Croteau, R.B. (2000). Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiol. 122, 215-223.
39. 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.
40. Muller, P., Lorber, P., and Haley, B. (1968). Volatile growth inhibitors produced by Salvia leucophylla: Effect on seedling growth and respiration. Bull. Torrey Bot. Club 95, 415-422.
41. Negrutiu, I., Shillito, R., Potrykus, I., Biasini, G., and Sala, F. (1987). Hybrid genes in the analysis of transformation conditions. Plant Mol. Biol. 8, 363-373.
42. Paulsen, H., Le-Nguyen, B., Sinnwell, V., and Seehofer, F. (1985). Synthesis of glycosides of mono-, sesqui- and diterpene alcohols. Liebigs Ann. Chem. 8, 1513-1536.
43. Peeters, N.M., Chapron, A., Giritch, A., Grandjean, O., Lancelin, D., Lhomme, T., Vivrel, A., and Small, I. (2000). Duplication and quadruplication of Arabidopsis thaliana cysteinyl- and asaparaginyl-tRNA synthetase genes of organellar origin. J. Mol. Evol. 50, 413-423.
44. Pereira, A., and Aarts, M.G.M. (1998). Transposon tagging with the En-I system. In Arabidopsis Protocols, J.S.J. Martinez-Zapater, ed (Totowa, NJ: Humana Press), pp. 329-338.
45. Phillips, M.A., and Croteau, R.B. (1999). Resin-based defenses in conifers. Trends Plant Sci. 4, 184-190.
46. Pichersky, E., and Gershenzon, J. (2002). The formation and function of plant volatiles: Perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 5, 237-243.
47. Raguso, R.A., Light, D.M., and Pickersky, E. (1996). Electroantennogram responses of Hyles lineata (Sphingidae:Lepidoptera) to volatile compounds from Clarkia breweri (Onagraceae) and other moth-pollinated flowers. J. Chem. Ecol. 22, 1735-1766.
48. Raguso, R.A., and Pichersky, E. (1999). A day in the life of a linalool molecule: Chemical communication in a plant-pollinator system. Part 1. Linalool biosynthesis in flowering plants. Plant Species Biol. 14, 95-120.
49. Rodriguez-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.
50. Schnurr, J.A., and Guerra, D.J. (2000). The CaMV-35S promoter is sensitive to shortened photoperiod in transgenic tobacco. Plant Cell Rep. 19, 279-282.
51. Shah, F.H., and Cha, T.S. (2000). A mesocarp- and species-specific cDNA clone from oil palm encodes for sesquiterpene synthase. Plant Sci. 154, 153-160.
52. Shen, B., Zheng, Z., Dooner, H.K., Shen, B.Z., and Zheng, Z.W. (2000). A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. Proc. Natl. Acad. Sci. USA 97, 14807-14812.
53. Snape, J.W., and Lawrence, M.J. (1971). The breeding system of Arabidopsis thaliana. Heredity 27, 299-302.
54. Vainstein, A., Lewinsohn, E., Pichersky, E., and Weiss, D. (2001). Floral fragrance: New inroads into an old commodity. Plant Physiol. 127, 1383-1389.
55. Van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P., Pereira, A., and Stiekema, W.J. (1995). pBINPLUS: An improved plant transformation vector based on pBIN19. Transgenic Res. 4, 288-290.
56. Van Poecke, R.M.P., and Dicke, M. (2002). Induced parasitoid attraction by Arabidopsis thaliana: Involvement of the octadecanoid and the salicylic acid pathway. J. Exp. Bot. 53, 1793-1799.
57. Van Poecke, R.M.P., Posthumus, M.A., and Dicke, M. (2001). Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: Chemical, behavioral, and gene-expression analysis. J. Chem. Ecol. 27, 1911-1928.
58. Verhoeven, H., Beuerle, T., and Schwab, W. (1997). Solid-phase microextraction: Artefact formation and its avoidance. Chromatographia 46, 63-66.
59. Wallaart, T.E., Bouwmeester, H.J., Hille, J., Poppinga, L., and Maijers, N.C.A. (2001). Amorpha-4,11-diene synthase: Cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin. Planta 212, 460-465.
60. Weidenhamer, J.D., Macias, F.A., Fischer, N.H., and Williamson, G.B. (1993). Just how insoluble are monoterpenes? J. Chem. Ecol. 19, 1799-1807.
61. Wise, M.L., Savage, T.J., Katahira, E., and Croteau, R.B. (1998). Monoterpene synthases from common sage (Salvia officinalis): cDNA isolation, characterization, and functional expression of (+)-sabinene synthase, 1,8-cineole synthase, and (+)-bornyl diphosphate synthase. J. Biol. Chem. 273, 14891-14899.
62. Zook, M., Hohn, T., Bonnen, A., Tsuji, J., and Hammerschmidt, R. (1996). Characterization of novel sesquiterpenoid biosynthesis in tobacco expressing a fungal sesquiterpene synthase. Plant Physiol. 112, 311-318.