Terpenoid biosynthesis in trichomes-current status and future opportunities

Plant Biotechnology Journal

Volumn 11, Issue 1, 2013, Pages 2-22

  Markus Lange, B ^a   Turner, Glenn W ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Engineering; Glandular trichome; Terpenoid

Indexed keywords

ESSENTIAL OIL; PLANT EXTRACT; TERPENE;

BIOSYNTHESIS; BIOTECHNOLOGY; METABOLISM; PLANT CELL; PLANT EPIDERMIS; REVIEW; ULTRASTRUCTURE;

BIOTECHNOLOGY; OILS, VOLATILE; PLANT CELLS; PLANT EPIDERMIS; PLANT EXTRACTS; TERPENES;

EID: 84871677371     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2012.00737.x     Document Type: Review

References (212)

1. Amme, S., Rutten, T., Melzer, M., Sonsmann, G., Vissers, J.P.C., Schlesier, B. and Mock, H.P. (2005) A proteome defines protective functions of tobacco leaf trichomes. Proteomics, 5, 2508-2518.
2. Ascensão, L., Marques, N. and Pais, M.S. (1997) Peltate glandular trichomes of Leonotis leonotis leaves: ultrastructure and histochemical characterization of secretions. Int. J. Plant Sci. 158, 249-258.
3. Ascensão, L., Mota, L. and Castro, M.deM. (1999) Glandular trichomes on the leaves and flowers of Plectranthus ornatus: morphology, distribution and histochemistry. Ann. Bot. 84, 437-447.
4. Awai, K., Xu, C., Lu, B. and Benning, C. (2006) Lipid trafficking between the endoplasmic reticulum and the chloroplast. Biochem. Soc. Trans. 34, 395-398.
5. van Bakel, H., Stout, J.M., Cote, A.G., Tallon, C.M., Sharpe, A.G., Hughes, T.R. and Page, J.E. (2011) The draft genome and transcriptome of Cannabis sativa. Genome Biol. 12, R102.
6. Balkunde, R., Pesch, M. and Hülskamp, M. (2010) Trichome patterning in Arabidopsis thaliana: from genetic to molecular models. Curr. Top. Dev. Biol. 91, 299-321.
7. Behnke, H.D. (1984) Plant trichomes - structure and ultrastructure: general terminology, taxonomic applications, and aspects of trichome-bacteria interactions in the leaf tips of Dioscorea. In Biology and Chemistry of Plant Trichomes (Rodriguez, E., Healey, P.L. and Meta, I., eds), pp. 1-21. New York, NY: Plenum Press.
8. Bell, J.M. and Curtis, J.D. (1985) Development and ultrastructure of foliar glands of Comptonia peregrina (Myricaceae). Bot. Gaz. 146, 288-292.
9. Bennett, M.H., Mansfield, J.W., Lewis, M.J. and Beale, M.H. (2002) Cloning and expression of sesquiterpene synthase genes from lettuce (Lactuca sativa L.). Phytochemistry 60, 255-261.
10. Benning, C. (2008) A role for lipid trafficking in chloroplast biogenesis. Prog. Lipid Res. 47, 381-389.
11. Bertea, C.M., Schalk, M., Karp, F., Maffei, M. and Croteau, R. (2001) Demonstration that menthofuran synthase of mint (Mentha) is a cytochrome P450 monooxygenase: cloning, functional expression, and characterization of the responsible gene. Arch. Biochem. Biophys. 390, 279-286.
12. Bertea, C.M., Voster, A., Verstappen, F.W.A., Maffei, M., Beekwilder, J. and Bouwmeester, H.J. (2006) Isoprenoid biosynthesis in Artemisia annua: cloning and heterologous expression of a germacrene A synthase from a glandular trichome cDNA library. Arch. Biochem. Biophys. 446, 3012.
13. Besser, K., Harper, A., Welsby, N., Schauvinhold, I., Slocombe, S., Li, Y., Dixon, R.A. and Broun, P. (2009) Divergent evolution of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiol. 149, 499-514.
14. Black, V.H., Sanjay, A., van Leyen, K., Lauring, B. and Kreibich, G. (2005) Cholesterol and steroid synthesizing smooth endoplasmic reticulum of adrenocortical cells contains high levels of proteins associated with the translocation channel. Endocrinology, 146, 4234-4249.
15. Bleeker, P.M., Spyropoulou, E.A., Diergaarde, P.J., Volpin, H., De Both, M.T.J., Zerbe, P., Bohlmann, J., Falara, V., Matsuba, Y., Pichersky, E., Haring, M.A. and Schuurink, R.C. (2011) RNA-seq discovery, functional characterization, and compartmentation of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Mol. Biol. 77, 323-336.
16. Bourett, T.M., Howard, R.J., O'Keefe, D.P. and Hallahan, D.L. (1994) Gland development on leaf surfaces of Nepeta racemosa. Int. J. Plant Sci. 155, 623-632.
17. Bouvier, F., Rahier, A. and Camara, B. (2005) Biogenesis, molecular regulation and function of plant isoprenoids. Prog. Lipid Res. 44, 357-429.
18. Bouwmeester, H.J., Kodde, J., Verstappen, F.W., 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.
19. Burke, C. and Croteau, R. (1999) Geranyl pyrophosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch. Biochem. Biophys. 405, 130-136.
20. Cai, Y., Jia, J.W., Crock, J., Lin, Z.X. and Croteau, R. (2002) A cDNA clone for beta-caryophyllene synthase from Artemisia annua. Phytochemistry, 61, 523-529.
21. Cardé, J.P. (1984) Leucoplasts: a distinct kind of organelles lacking typical 70S ribosomes and free thylakoids. Eur. J. Cell Biol. 34, 18-26.
22. Carpenter, K.J. (2006) Specialized structures in the leaf epidermis of basal angiosperms: morphology, distribution, and homology. Am. J. Bot. 93, 665-681.
23. Carson, C.F. and Hammer, K.A. (2011) Chemistry and bioactivity of essential oils. In Lipids and Essential Oils as Antimicrobial Agents (Thormar, H., ed.), pp. 203-238. Chichester, UK: John Wiley & Sons.
24. Chang, Y.J., Song, S.H., Park, S.H. and Kim, S.U. (2000) Amorpha-4, 11-diene synthase of Artemisia annua: cDNA isolation and bacterial expression of a terpene synthase involved in artemisinin biosynthesis. Arch. Biochem. Biophys. 383, 178-184.
25. Charon, J., Launay, J. and Cardé, J.P. (1987) Spatial organization and volume density of leucoplasts in pine secretory cells. Protoplasma, 138, 45-53.
26. Chatzopoulou, F.M., Marks, A.M., Argiriou, A., Degenhardt, J. and Kenellis, A.K. (2010) EST analysis and annotation of transcripts derived from a trichome-specific cDNA library from Salvia fruticosa. Plant Cell Rep. 29, 523-534.
27. Chauveau, O., Eggers, L., Raquin, C., Silverio, A., Brown, S., Couloux, A., Cruaund, C., Kaltchuk-Santos, E., Yockteng, R., Souza-Chies, T.T. and Nadot, S. (2011) Evolution of oil producing trichomes in Sisyrinchium (Iridaceae): insights from the first comprehensive phylogenetic analysis of the genus. Ann. Bot. 107, 1287-1312.
28. Cheniclet, C. and Cardé, J.P. (1985) Presence of leucoplasts in secretory cells and of monoterpenes in the essential oil: a correlative study. Israel J. Bot. 34, 219-238.
29. Colby, S.M., Alonso, W.R., Katahira, E., McGarvey, D.J. and Croteau, R. (1993) 4S-Limonene synthase from the oil glands of spearmint (Mentha spicata): cDNA isolation, characterization and bacterial expression of the catalytically active monoterpene cyclase. J. Biol. Chem. 268, 23016-23024.
30. 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. U.S.A. 95, 2216-2221.
31. Colson, M., Pupier, R. and Perrin, A. (1993) Étude biomathématique du nombre de glandes peltées des feuilles de Mentha × piperita. Can. J. Bot. 71, 1202-1211.
32. Cristani, M., D'Arrigo, M., Mandalari, G., Castelli, F., Sarpietro, M.G, Micieli, D., Venuti, V., Bisignano, G., Saija, A. and Trombetta, D. (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J. Agric. Food Chem. 55, 6300-6308.
33. Crock, J., Wildung, M. and Croteau, R. (1997) Isolation and bacterial expression of a sesquiterpene synthase cDNA clone from peppermint (Mentha × piperita, L.) that produces the aphid alarm pheromone (E)-beta-farnesene. Proc. Natl. Acad. Sci. U.S.A. 94, 12833-12838.
34. Crocoll, C., Asbach, J., Novak, J., Gershenzon, J. and Degenhardt, J. (2010) Terpene synthases of oregano (Origanum vulgare L.) and their roles in the pathway and regulation of terpene biosynthesis. Plant Mol. Biol. 73, 587-603.
35. Croteau, R. and Winters, J.N. (1982) Demonstration of the intercellular compartmentation of l-menthone metabolism in peppermint (Mentha × piperita) leaves. Plant Physiol. 69, 975-977.
36. Croteau, R.B., Davis, E.M., Ringer, K.L. and Wildung, M.R. (2005) (-)-Menthol biosynthesis and molecular genetics. Naturwissenschaften 92, 562-577.
37. Crowell, A., 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.
38. Cui, H., Zhang, S.T., Yang, H.J., Hao, J. and Wang, X.J. (2011) Gene expression profile analysis of tobacco leaf trichomes. BMC Plant Biol. 11, 76.
39. 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.
40. van Cutsem, E., Simonart, G., Degand, H., Faber, A.M., Morsomme, P. and Boutry, M. (2011) Gel-based and gel-free proteomic analysis of Nicotiana tabacum trichomes identifies proteins involved in secondary metabolism and in the (a)biotic stress response. Proteomics 11, 440-454.
41. Davis, E.M. and Croteau, R. (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Top. Curr. Chem. 209, 53-95.
42. Davis, E.M., Ringer, K.L., McConkey, M.E. and Croteau, R. (2005) Monoterpene metabolism. Cloning, expression, and characterization of menthone reductases from peppermint. Plant Physiol. 137, 873-881.
43. Degenhardt, J., Köllner, T.G. and Gershenzon, J. (2009) Monoeterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry, 70, 1621-1637.
44. Deguerry, F., Pastore, L., Wu, S., Clark, A., Chappell, J. and Schalk, M. (2006) The diverse sesquiterpene profile of patchouli, Pogostemon cablin, is correlated with a limited number of sesquiterpene synthases. Arch. Biochem. Biophys. 454, 123-136.
45. Dell, B. and McComb, A.J. (1978) Plant resins - their formation, secretion and possible functions. Adv. Bot. Res. 6, 278-316.
46. Demissie, Z.A., Sarker, L.S. and Mahmoud, S.S. (2010) Cloning and functional characterization of beta-phellandrene synthase from Lavandula angustifolia. Planta, 233, 685-696.
47. Duke, S.O. and Paul, R.N. (1993) Development and fine structure of the glandular trichomes of Artemisia annua L. Int. J. Plant Sci. 154, 107-118.
48. Dung, J.K.S., Schroeder, B.K. and Johnson, D.A. (2010) Evaluation of Verticillium wilt resistance in Mentha arvensis and M. longifolia genotypes. Plant Dis. 94, 1255-1260.
49. Durkee, L.T., Baird, C.W. and Cohen, P.F. (1984) Light and electron microscopy of the resin glands of Passiflora foetida (Passifloraceae). Am. J. Bot. 71, 596-602.
50. Eisenreich, W, Schwarz, M., Cartayrade, A., Arigoni, D., Zenk, M.H. and Bacher, A. (1998) The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem. Biol. 5, R221-R233.
51. Ennajdaoui, H., Vachon, G., Giacalone, C., Besse, I., Sallaud, C., Herzog, M. and Tissier, A. (2010) Trichome specific expression of the tobacco (Nicotiana sylvestris) cembratrien-ol synthase genes is controlled by both activating and repressing cis-regions. Plant Mol. Biol. 73, 673-685.
52. Eshed, Y. and Zamir, D. (1994) A genomic library of Lycopersicon pennellii in L. esculentum: a tool for fine mapping of genes. Euphytica, 79, 175-179.
53. Eshed, Y. and Zamir, D. (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics, 141, 1147-1162.
54. Fahn, A. (1979) Secretory Tissues in Plants, London, UK: Academic Press.
55. Fahn, A. (1988) Secretory tissues in vascular plants. New Phytol. 108, 229-257.
56. Falara, V., Fotopoulos, V., Margaritis, T., Anastasaki, T., Pteraki, I., Bosabilidis, A.M., Kafetzopoulos, D., Demetzos, C., Pichersky, E. and Kenellis, A.K. (2008) Transcriptome analysis approaches for the isolation of trichome-specific genes from the medicinal plant Cistus creticus subsp. Creticus. Plant Mol. Biol. 68, 633-651.
57. Falara, V., Pichersky, E. and Kenellis, A.K. (2010) A copalyl-8-ol pyrophosphate synthase from the Angiosperm Cistus creticus subsp. Creticus is a putative key enzyme for the formation of pharmacologically active, oxygen-containing labdane-type diterpenes. Plant Physiol. 154, 301-310.
58. Falara, V., Akhtar, T.A., Nguyen, T.T.H., Spyropoulou, E.A., Bleeker, P.M., Schauvinhold, I., Matsuba, Y., Bonini, M.E., Schilmiller, A.L., Last, R.L., Schuurink, R.C. and Pichersky, E. (2011) The tomato terpene synthase gene family. Plant Physiol. 157, 770-789.
59. Fei, Z., Tang, X., Alba, R.M., White, J.A., Ronning, C.M., Martin, G.B., Tanksley, S.D. and Giovannoni, J.J. (2004) Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J. 40, 47-59.
60. Gang, D.R., Wang, J., Dudareva, N., Nam, K.H., Simon, J.E., Lewinsohn, E. and Pichersky, E. (2001) An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol. 125, 539-555.
61. Gershenzon, J., Duffy, M., Karp, F. and Croteau, R. (1987) Mechanized techniques for the selective extraction of enzymes from plant epidermal glands. Anal. Biochem. 163, 159-164.
62. Gershenzon, J., Maffei, M. and Croteau, R. (1989) Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiol. 89, 1351-1357.
63. Gershenzon, J., McCaskill, D., Rajaonarivony, J.I.M., Mihaliak, C., Karp, F. and Croteau, R. (1992) Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Anal. Biochem. 200, 130-138.
64. Gershenzon, J., McConkey, M.E. and Croteau, R. (2000) Regulation of monoterpene accumulation in leaves of peppermint (Mentha × piperita L.). Plant Physiol. 122, 205-214.
65. Gleizes, M., Pauly, G., Cardé, J.-P., Marpeau, A. and Bernarddagan, C. (1983) Monoterpene hydrocarbon biosynthesis by isolated leukoplasts of Citrofortunella mitis. Planta, 159, 373-381.
66. Gonzales-Vigil, E., Hufnagel, D.E., Kim, J., Last, R.L. and Barry, C.S. (2012) Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites. Plant J. (in press), doi: 10.1111/j.1365-313X.2012.05040.x.
67. Göpfert, J., Heil, N., Conrad, J. and Spring, O. (2005) Cytological development and sesquiterpene lactone secretion in capitates glandular trichomes of sunflower. Plant Biol. 7, 148-155.
68. Göpfert, J.C., MacNevin, G., Ro, D.K. and Spring, O. (2009) Identification, functional characterization and developmental regulation of sesquiterpene synthases from sunflower capitate glandular trichomes. BMC Plant Biol. 9, 86.
69. Göpfert, J., Bülow, A.K. and Spring, O. (2010) Identification and functional characterization of a new sunflower germacrene A synthase (HaGAS3). Nat. Prod. Commun. 5, 709-715.
70. Graham, I.A., Besser, K., Blumer, S., Branigan, C.A., Czechowski, T., Elias, L., Guterman, I., Harvey, D., Isaac, P.G., Khan, A.M., Larson, T.R., Li, Y., Pawson, T., Penfield, T., Rae, A.M., Rathbone, D.A., Reid, S., Ross, J., Smallwood, M.F., Segura, V., Townsend, T., Vyas, D., Winzer, T. and Bowles, D. (2010) The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science, 327, 328-331.
71. Grebe, M. (2012) The patterning of epidermal hairs in Arabidopsis - updated. Curr. Opin. Plant Biol. 15, 31-37.
72. Günnewich, N., Page, J.E., Köllner, T.G., Degenhardt, J. and Kutchan, T.M. (2007) Functional expression and characterization of trichome-specific (-)-limonene synthase and (+)-α-pinene synthase from Cannabis sativa. Nat. Prod. Commun. 2, 223-232.
73. Hammond, C.T. and Mahlberg, P.G. (1978) Ultrastrcutural development of capitate glandular hairs of Cannabis sativa L. (Cannabaceae). Am. J. Bot. 65, 140-151.
74. Hanlidou, E., Kokkini, A.M., Bosabalidis, A.M. and Bessière, J.M. (1991) Glandular trichomes and essential oil constituents of Calamintha menthifolia (Lamiaceae). Plant Syst. Evol. 177, 17-26.
75. Harada, E., Kim, J.A., Meyer, A.J., Hell, R., Clemens, S. and Choi, Y.E. (2010) Expression profiling of tobacco leaf trichomes identifies genes for biotic and abiotic stresses. Plant Cell Physiol. 51, 1627-1637.
76. Hashidoko, Y. and Urashima, M. (1994) Efficient preparation of browning-free glandular trichome tissues from the surface of leaves of Rosa rugosa Thunb. Plant Cell Physiol. 36, 127-132.
77. Hawes, C. (2005) Cell biology of the plant golgi apparatus. New Phytol. 165, 29-44.
78. Hawes, C. and Satiat-Jeunemaitre, B. (2005) The plant golgi apparatus - going with the flow. Biochim. Biophys. Acta 1744, 93-107.
79. Heinrich, G., Sawidis, T., Ingolic, E., Stabentheiner, E. and Pfeifhofer, H.W. (2010) Ultrastructure of glandular hairs of Sigesbeckia jorullensis Kunth (Asteraceae). Israel J. Plant Sci. 58, 297-308.
80. 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.
81. Hölscher, D.J., Williams, D.C., Wildung, M.R. and Croteau, R. (2003) A cDNA clone for 3-carene synthase from Salvia stenophylla. Phytochemistry, 62, 1081-1086.
82. Hosoi, M., Ito, M., Yagura, T., Adams, R.P. and Honda, G. (2004) cDNA isolation and functional expression of myrcene synthase from Perilla frutescens. Biol. Pharm. Bull. 27, 1979-1985.
83. Hristozov, D., Costa, F.B. and Gasteiger, J. (2007) Sesquiterpene lactone-based classification of the family Asteraceae using neural networks and k-nearest neighbors. J. Chem. Inf. Model. 47, 9-19.
84. Hua, L. and Matsuda, S.P.T. (1999) The molecular cloning of 8-epicedrol synthase from Artemisia annua. Arch. Biochem. Biophys. 369, 208-212.
85. Iijima, Y., Gang, D.R., Fridman, E., Lewinsohn, E. and Pichersky, E. (2004a) Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol. 134, 370-379.
86. Iijima, Y., Davidoviach-Rikanti, R., Fridman, E., Gang, D.R., Bar, E., Lewinsohn, E. and Pichersky, E. (2004b) 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.
87. Iijima, Y., Wang, G., Fridman, E. and Pichersky, E. (2006) Analysis of the enzymatic formation of citral in the glands of sweet basil. Arch. Biochem. Biophys. 448, 141-149.
88. Ikezawa, N., Göpfert, J., Nguyen, D.T., Kim, S.U., O'Maille, P.E., Spring, O. and Ro, D.K. (2011) Lettuce costunolide synthase (CYP71BL2) and its homolog (CYP71BL1) from sunflower catalyze distinct regio- and stereoselective hydroxylations in sesquiterpene lactone metabolism. J. Biol. Chem. 286, 21601-21611.
89. Ito, M. and Honda, G. (2007) Geraniol synthases from Perilla and their taxonomical significance. Phytochemistry, 68, 446-453.
90. 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.
91. Kampranis, S.C., Ionnidis, D., Purvis, A., Mahrez, W., Ninga, E., Katerelos, N.A., Anssour, S., Dunwell, J.M., Degenhardt, J., Makris, A.M., Goodenough, P.W. and Johnson, C.B. (2007) Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Plant Cell, 19, 1994-2005.
92. Krings, M., Kellogg, D.W., Kerp, H. and Taylor, T.N. (2003) Trichomes of the seed fern Blanzyopteris praedentata: implications for plant-insect interactions in the Late Carboniferous. Bot. J. Linn. Soc. 141, 133-149.
93. Landmann, C., Fink, B., Festner, M., Dregus, M., Engel, K.H. and Schwab, W. (2007) Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Arch. Biochem. Biophys. 465, 417-429.
94. Lane, A., Broecklemann, A., Woronuk, G.N., Sarker, L. and Mahmoud, S.S. (2010) A genomics resource for investigating regulation of essential oil production in Lavandula angustifolia. Planta, 231, 835-845.
95. Lange, B.M. and Croteau, R. (1999a) Isoprenoid biosynthesis via a mevalonate-independent pathway in plants: cloning and heterologous expression of 1-deoxyxylulose-5-phosphate reductoisomerase from peppermint. Arch. Biochem. Biophys. 365, 170-174.
96. Lange, B.M. and Croteau, R. (1999b) Isopentenyl pyrophosphate biosynthesis via a mevalonate-independent pathway: isopentenyl monophosphate kinase catalyzes the terminal enzymatic step. Proc. Natl. Acad. Sci. U.S.A. 96, 13714-13719.
97. Lange, B.M., Wildung, M.R., McCaskill, D. and Croteau, R. (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 2100-2104.
98. Lange, B.M., Wildung, M.R., Stauber, E.J., Sanchez, C., Pouchnik, D. and Croteau, R. (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc. Natl. Acad. Sci. U.S.A. 97, 2934-2939.
99. Lange, B.M., Rios-Estepa, R. and Turner, G.W. (2010) Production of terpenes and terpenoids in glandular trichome-bearing plants. PCT patent application WO/2010/111571.
100. Lange, B.M., Mahmoud, S.S., Wildung, M.R., Turner, G.W., Davis, E.M., Lange, I., Baker, R.C., Boydston, R.A. and Croteau, R.B. (2011) Improving peppermint essential oil yield and composition by metabolic engineering. Proc. Natl. Acad. Sci. U.S.A. 108, 16944-16949.
101. Levin, T. (2004) Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol. 14, 483-490.
102. Levin, T. and Loewen, C. (2006) Inter-organelle membrane contact sites: through a glass, darkly. Curr. Opin. Cell Biol. 18, 371-378.
103. Liu, B., Wang, H., Du, Z., Li, G. and Ye, H. (2011) Metabolic engineering of artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep. 30, 689-694.
104. Lu, S., Xu, R., Jia, J.W., Pang, J., Matsuda, S.P.T. and Chen, X.Y. (2002) Cloning and functional characterization of a β-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiol. 130, 477-486.
105. Lücker, J., Schwab, W., Franssen, M.C.R., van der Plas, L.H.W., Bouwmeester, H.J. and Verhoeven, H.A. (2004) Metabolic engineering of monoterpene biosynthesis: two-step production of (+)-transisopiperitenol by tobacco. Plant J.39, 135-145.
106. Lupien, S., Karp, F., Wildung, M. and Croteau, R. (1999) Regiospecific cytochrome P450 limonene hydroxylases from mint (Mentha) species: cDNA isolation, characterization, and functional expression of (-)-4S-limonene-3-hydroxylase and (-)-4S-limonene-6-hydroxylase. Arch. Biochem. Biophys. 368, 181-192.
107. Machado, S.R., Gregorio, E.A. and Gumarães, E. (2006) Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure and secretion in relation to function. Ann. Bot. 97, 357-369.
108. Maffei, M., Chialva, F. and Sacco, T. (1989) Glandular trichomes and essential oils in developing peppermint leaves. New Phytol. 111, 707-716.
109. Mahmoud, S.S. and Croteau, R.B. (2001) Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc. Natl. Acad. Sci. U.S.A. 98, 8915-8920.
110. Mahmoud, S.S., Williams, M. and Croteau, R. (2004) Cosuppression of limonene-3-hydroxylase in peppermint promotes accumulation of limonene in the essential oil. Phytochemistry, 65, 547-554.
111. Majdi, M., Liu, Q., Karinzadeh, G., Malboobi, M.A., Beekwilder, J., Cankar, K., de Vos, R., Todorović, S., Simonović, A. and Bouwmeester, H. (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry, 72, 1739-1750.
112. 9-tretrahydrocannabinol biosynthesis in Cannabis sativa. J. Exp. Bot. 60, 3715-3726.
113. Maruyama, T., Ito, M., Kiuchi, F. and Honda, G. (2001) Molecular cloning, functional expression and characterization of d-limonene synthase from Schizonepeta tenuifolia. Biol. Pharm. Bull. 24, 373-377.
114. Maruyama, T., Saeki, D., Ito, M. and Honda, G. (2002) Molecular cloning, functional expression and characterization of d-limonene synthase from Agastache rugosa. Biol. Pharm. Bull. 25, 661-665.
115. Masumoto, N., Korin, M. and Ito, M. (2010) Geraniol and linalool synthases from wild species of perilla. Phytochemistry, 71, 1068-1075.
116. Mau, C.J., Karp, F., Ito, M., Honda, G. and Croteau, R.B. (2010) A candidate cDNA clone for (-)-limonene 7-hydroxylase from Perilla frutescens. Phytochemistry, 71, 373-379.
117. McCaskill, D. and Croteau, R. (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha × piperita) rely exclusively on plastid-derived isopentenyl pyrophosphate. Planta, 197, 49-56.
118. McCaskill, D., Gershenzon, J. and Croteau, R. (1992) Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha × piperita L.). Planta, 187, 445-454.
119. McConkey, M.E., Gershenzon, J. and Croteau, R.B. (2000) Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiol. 122, 215-224.
120. McDowell, E.T., Kapetyn, J., Schmidt, A., Li, C., Kang, J.H., Descour, A., Shi, F., Larson, M., Schilmiller, A., An, L., Jones, A.D., Pichersky, E., Soderlund, C.A. and Gang, D.A. (2011) Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol. 155, 524-539.
121. Menin, B., Comino, C., Protis, E., Moglia, A., Cankar, K., Bouwmeester, H.J., Lanteri, S. and Beekwilder, J. (2012) Genetic mapping and characterization of the globe artichoke (+)-germacrene A synthase gene, encoding the first dedicated enzyme for biosynthesis of the bitter sesquiterpene lactone cynaropicrin. Plant Sci. 190, 1-8.
122. Mercke, P., Crock, J., Croteau, R. and Brodelius, P.E. (1999) Cloning, expression and characterization of epi-cedrol synthase, a sesquiterpene cyclase from Artemisia annua. Arch. Biochem. Biophys. 369, 213-222.
123. Mercke, P., Bengtsson, M., Bouwmeester, H.J., Posthumus, M.A. and Brodelius, P.E. (2000) Molecular cloning, expression, and characterization of amorpha-4, 11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L. Arch. Biochem. Biophys. 381, 173-180.
124. Metcalfe, C.R. and Chalk, L. (1950) Lists of families in which certain diagnostic features occur. In Anatomy of the Dicotyledons, 1st edn, Vol.2, pp. 1326-1354. Oxford, UK: Clarendon Press.
125. Metcalfe, C.R. and Chalk, L. (1979) Lists of families in which certain diagnostic features occur. In Anatomy of the Dicotyledons, 2nd edn, Vol. 1, pp. 190-221. Oxford, UK: Clarendon Press.
126. Monforte, A.J. and Tanksley, S.D. (2000) Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon habrochaites genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome, 43, 803-813.
127. Nagel, J., Culley, L.K., Lu, Y., Liu, E., Matthews, P.D., Stevens, J.F. and Page, J.E. (2008) EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell, 20, 186-200.
128. Napp-Zinn, K. (1966) Anatomie des Blattes. Teil 1, Blattanatomie der Gymnospermen. In Handbuch der Pflanzenanatomie, Vol. 8, Part 1, (Tischler, G. and Pascher, A., eds), Berlin, Germany: Gebrüder̈ Borntraeger.
129. Nguyen, D.T., Göpfert, J., Ikezawa, N., Macnevin, G., Kathiresan, M., Conrad, J., Spring, O. and Ro, D.K. (2010) Biochemical conservation and evolution of germacrene A oxidase in Asteraceae. J. Biol. Chem. 28, 16588-16598.
130. Nielsen, M.T., Akers, C.P., Järlfors, U.E., Wagner, G.J. and Berger, S. (1991) Comparative ultrastructural features of secreting and nonsecreting glandular trichomes of two genotypes of Nicotiana tabacum L. Bot. Gaz. 152, 13-22.
131. Ogura, Y. (1972) Comparative anatomy of the vegetative organs of the pteridophytes. In Handbuch der Pflanzenanatomie, Vol. 7, Part 3, (Tischler, G. and Pascher, A, eds), Berlin, Germany: Gebrüder̈Borntraeger.
132. Okada, Y. and Ito, K. (2001) Cloning and analysis of valerophenone synthase gene expressed specifically in lupulin gland of hop (Humulus lupulus L.). Biosci. Biotechnol. Biochem. 65, 150-155.
133. Olofsson, L., Lundgren, A. and Brodelius, P.E. (2012) Trichome isolation with and without fixation using laser microdissection and pressure catapulting followed by RNA amplification: expression of genes of terpene metabolism in apical and sub-apical trichome cells of Artemisia annua L. Plant Sci. 183, 9-13.
134. Olsson, M.E., Olofsson, L.M., Lindahl, A.L., Lundgren, A., Brodelius, M. and Brodelius, P.E. (2009) Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70, 1123-1128.
135. Page, J.E. and Boubakir, Z. (2011) Aromatic prenyltransferase from Cannabis. PCT patent application WO/2011/017798.
136. Parsons, H.T., Christiansen, K., Knierim, B., Carroll, A., Ito, J., Batth, T.S., Smith-Moritz, A.M., Morrison, S., McInerney, P., Hadi, M.Z., Auer, M., Mukhopadhyay, A., Petzold, C.J., Scheller, H.V., Loqué, D. and Heazlewood, J.L. (2012) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol. 159, 12-26.
137. Pateraki, I. and Kanellis, A.K. (2008) Isolation and functional analysis of two Cistus creticus cDNAs encoding geranylgeranyl diphosphate synthase. Ohytochemistry 69, 1641-1652.
138. Pesch, M. and Hülskamp, M. (2009) One, two, three... models for trichome patterning in Arabidopsis? Curr. Opin. Plant Biol. 12, 587-592.
139. Picaud, S., Olofsson, L., Brodelius, M. and Brodelius, P.E. (2005) Expression, purification, and characterization of recombinant amorpha-4, 11-diene synthase from Artemisia annua L. Arch. Biochem. Biophys. 436, 215-226.
140. Polichuk, D.B., Zhang, Y., Reed, D.W., Schmidt, J.F. and Covello, P.S. (2010) A glandular trichome-specific monoterpene alcohol dehydrogenase from Artemisia annua. Phytochemistry 71, 1264-1269.
141. Potato Genome Sequencing Consortium (2011) Genome sequencing and analysis of the tuber crop potato. Nature, 475, 189-195.
142. Prosser, I., Phillips, A.L., Gittings, S., Lewis, M.J., Hooper, A.M., Pickett, J.A. and Beale, M.H. (2002) (+)-(10R)-Germacrene A synthase from goldenrod, Solidago canadensis; cDNA isolation, bacterial expression and functional analysis. Phytochemistry, 60, 691-702.
143. Prosser, I.M., Adams, R.J., Beale, M.H., Hawkins, N.D., Phillips, A.L., Pickett, J.A. and Field, L.M. (2006) Cloning and functional characterization of a cis-muuroladiene synthase from black peppermint (Mentha × piperita) and direct evidence for a chemotype unable to synthesise farnesene. Phytochemistry, 67, 1564-1572.
144. Raychaudhuri, S. and Prinz, W.A. (2010) The diverse functions of oxysterol-binding proteins. Annu. Rev. Cell Dev. Biol. 26, 157-177.
145. Rebers, M., Kaneta, T., Kawaide, H., Yamaguchi, S., Yang, Y.Y., Imai, R., Sekimoto, H. and Kamiya, Y. (1999) Regulation of gibberellin biosynthesis genes during flower and early fruit development of tomato. Plant J. 17, 241-250.
146. Ringer, K.L., McConkey, M.E., Davis, E.M., Rushing, G.W. and Croteau, R. (2003) Monoterpene double-bond reductases of the (-)-menthol biosynthetic pathway: isolation and characterization of cDNAs encoding (-)-isopiperitenone reductase and (+)-pulegone reductase of peppermint. Arch. Biochem. Biophys. 418, 80-92.
147. Ringer, K.L., Davis, E.M. and Croteau, R. (2005) Monoterpene metabolism. Cloning, expression, and characterization of (-)-isopiperitenol/(-)-carveol dehydrogenase of peppermint and spearmint. Plant Physiol. 137, 863-872.
148. Rios-Estepa, R., Turner, G.W., Lee, J.M., Croteau, R.B. and Lange, B.M. (2008) A systems biology approach identifies the biochemical mechanisms regulating monoterpenoid essential oil composition in peppermint. Proc. Natl. Acad. Sci. U.S.A. 105, 2818-2823.
149. Rios-Estepa, R., Turner, G.W., Lee, J.M., Croteau, R.B. and Lange, B.M. (2010) Mathematical modeling-guided evaluation of biochemical, developmental, environmental and genotypic determinants of essential oil composition and yield in peppermint leaves. Plant Physiol. 152, 2105-2119.
150. Ro, D.K., Paradise, E.M., Ouellet, M., Fisher, K.J., Newman, K.L., Ndungu, J.M., Ho, K.A., Eachus, R.A., Ham, T.S., Kirby, J., Chang, M.C., Withers, S.T., Shiba, Y., Sarpong, R. and Keasling, J.D. (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature, 440, 940-943.
151. Rydén, A.M., Ruyter-Spira, C., Quax, W.J., Osada, H., Muranaka, T., Kayser, O. and Bouwmeester, H. (2010) The molecular cloning of dihydroartemisinc aldehyde reductase and its implication in artemisinin biosynthesis in Artemisia annua. Planta, 76, 1778-1783.
152. Sallaud, C., Rontein, D., Onillon, S., Jabès, F., Duffé, P., Giacalone, C., Thoraval, S., Escoffier, C., Herbette, G., Leonhardt, N., Causse, M. and Tissier, A. (2009) A novel pathway for sesquiterpene biosynthesis from Z, Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell, 21, 301-317.
153. Sallaud, C., Giacalone, C., Töpfer, R., Goepfert, S., Bakaher, N., Rösti, S. and Tissier, A. (2012) Characterization of two genes for the biosynthesis of the labdane diterpene Z-abienol in tobacco (Nicotiana tabacum) glandular trichomes. Plant J. (in press), doi: 10.1111/j.1365-313X.2012.05068.x.
154. Sanmiya, K., Ueno, O., Matsuoka, M. and Yamamoto, N. (1999) Localization of farnesyl diphosphate synthase in chloroplasts. Plant Cell Physiol. 40, 348-354.
155. Schalk, M. and Croteau, R. (2000) A single amino acid substitution (F363I) converts the regiochemistry of the spearmint (-)-limonene hydroxylase from a C6- to a C3-hydroxylase. Proc. Natl. Acad. Sci. U.S.A. 97, 11948-11953.
156. Schilmiller, A.L., Last, R.L. and Pichersky, E. (2008) Harnessing plant trichome biochemistry for the production of useful compounds. Plant J. 54, 702-711.
157. Schilmiller, A., 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 pyrophosphate precursor rather than geranyl pyrophosphate. Proc. Natl. Acad. Sci. U.S.A. 106, 10865-10870.
158. Schilmiller, A., Shi, F., Kim, J., Charbonneau, A.L., Holmes, D., Jones, A.D. and Last, R.L. (2010) Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant J. 62, 391-403.
159. Schnepf, E. and Klasova, A. (1972) Zur Feinstruktur von Öl- und Flavon-Drüsen. Ber. Dtsch. Bot. Ges. 85, 249-258.
160. Schnepf, E. (1974) Gand cells. In Dynamic Aspects of Plant Ultrastructure (Robards, A.W. ed.), pp. 331-357. London, UK: McGraw-Hill.
161. Schnepf, E. (1993) Golgi apparatus and slime secretion in plants: the early implications and recent models of membrane traffic. Protoplasma 172, 3-11.
162. Sinclair, D., Zani, B., Donegan, S., Olliaro, P. and Garner, P. (2009) Artemisinin-based combination therapy for treating uncomplicated malaria. Cochrane Database Syst. Rev. 3, CD007483.
163. Sirikantaramas, S., Morimoto, S., Shoyama, Y., Ishikawa, Y., Wada, Y., Shoyama, Y. and Taura, F. (2004) The gene controlling marijuana psychoactivity. J. Biol. Chem. 279, 39767-39774.
164. Slone, J.H. and Kelsey, R.G. (1985) Isolation and purification of glandular secretory cells from Artemisia tridentata (ssp. Vaseyana) by percoll density gradient centrifugation. Am. J. Bot. 72, 1445-1451.
165. Spring, O., Bienert, U. and Klemt, V. (1987) Sesquiterpene lactones in glandular trichomes of sunflower leaves. J. Plant Physiol. 130, 433-439.
166. Staehelin, L.A. (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 11, 1151-1165.
167. Stevens, J.F. and Page, J.E. (2004) Xanthohumol and related prenylflavonoids from hops and beer: to your good health. Phytochemistry, 65, 1317-1330.
168. Swanson, E.S., Cunningham, W.P. and Holman, R.T. (1980) Ultrastructure of the glandular ovarian trichomes of Cypripedium calceolus and C. reginae (Orcadaceae). Am. J. Bot. 67, 784-789.
169. Tan, X., Wang, Q., Tian, B., Zhang, H., Lu, D. and Zhou, J. (2011) A Brassica napus lipase locates at the membrane contact sites involved in chloroplast development. PLoS ONE, 6, 1-9.
170. Taura, F., Sirikantaramas, S., Shoyama, Y., Yoshikai, K., Shoyama, Y. and Morimoto, S. (2007) Cannabidiolic acid synthase, the chemotype-determining enzyme in fiber-type Cannabis sativa. FEBS Lett. 581, 2929-2934.
171. Taura, F., Tanaka, S., Taguchi, C., Fukamizu, T., Tanaka, H., Shoyama, Y. and Morimoto, S. (2009) Characterization of olivetol synthase, a polyketide synthase putatively involved in cannabinoid biosynthetic pathway. FEBS Lett. 583, 2061-2066.
172. Teoh, K.H., Polichuk, D.R., Reed, D.W., Nowak, G. and Covello, P.S. (2006) Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett. 580, 1411-1416.
173. Teoh, K.H., Polichuk, D.R., Reed, D.W. and Covello, P.S. (2009) Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany, 87, 635-642.
174. Thabet, I., Guirimand, G., Courdavault, V., Papon, N., Godet, S., Dutilleul, C., Bouzid, S., Giglioli-Guivarc'h, N., Clastre, M. and Simkin, A.J. (2011) The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis. J. Plant Physiol. 168, 2110-2116.
175. 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 pyrophosphate synthases. Plant Cell, 16, 977-992.
176. Tissier, A. (2012a) Glandular trichomes: what comes after expressed sequence tags? Plant J. 70, 51-68.
177. Tissier, A. (2012b) Trichome specific expression: promoters and their applications. In Transgenic Plants - Advances and Limitations (Çiftçi, Y.O., ed.), pp. 353-378. Rijeka, Croatia: InTech Open Access Company.
178. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635-641.
179. Tomlinson, P.B. (1969) Commelinales-Zingiberales. In Anatomy of the Monocotyledons, Vol. 3 (Metcalfe, C.R. ed.), pp. 1-446. Oxford, UK: Clarendon Press.
180. Toulmay, A. and Prinz, W.A. (2011) Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr. Opin. Cell Biol. 23, 458-463.
181. Towler, M.J. and Weathers, P.J. (2007) Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. Plant Cell Rep. 26, 2129-2136.
182. Tsurumaru, Y., Sasaki, K., Miyawaki, T., Momma, T., Umemoto, N. and Yazaki, K. (2010) An aromatic prenyltransferase-like gene HIPT-1 preferentially expressed in lupulin glands of hop. Plant Biotechnol. 27, 199-204.
183. Tsurumaru, Y., Sasaki, K., Miyawaki, T., Uto, Y., Momma, T., Umemoto, N., Mommose, M. and Yazaki, K. (2012) HIPT-1, a membrane-bound prenyltransferase responsible for the biosynthesis of bitter acids in hops. Biochem. Biophys. Res. Commun. 417, 393-398.
184. Turina, A.V., Nolan, M.V., Zygadlo, J.A. and Perillo, M.A. (2006a) Natural terpenes: self-assembly and membrane partitioning. Biophys. Chem. 122, 101-113.
185. Turner, G.W. and Croteau, R. (2004) Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localization of geranyl pyrophosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol. 136, 4215-4227.
186. Turner, G., Gershenzon, J., Nielson, E.E., Froehlich, J.E. and Croteau, R. (1999) Limonene synthase, the enzyme responsible for monoterpene biosynthesis in peppermint, is localized to leucoplasts of oil gland secretory cells. Plant Physiol. 120, 879-886.
187. Turner, G.W., Gershenzon, J. and Croteau, R. (2000a) Distribution of peltate glandular trichomes on developing leaves of peppermint. Plant Physiol. 124, 655-664.
188. Turner, G.W., Gershenzon, J. and Croteau, R. (2000b) Development of peltate glandular trichomes of peppermint. Plant Physiol. 124, 665-679.
189. Turner, G.W., Davis, E.M. and Croteau, R.B. (2012) Immunocytochemical localization of short-chain family reductases involved in menthol biosynthesis in peppermint. Planta, 235, 1185-1195.
190. Uphof, J.C.T. (1962) Plant hairs In Handbuch der Pflanzenanatomie, Vol. 4, Part 5 (Tischler, G and Pascher, A., eds), pp. 1-206. Berlin, Germany: Gebrüder̈ Borntraeger.
191. Van der Hoeven, R.S., Monforte, A.J., Breeden, D., Tanksley, S.D. and Steffens, J.C. (2000) Genetic control and evolution of sesquiterpene biosynthesis in Lycopersicon esculentum and L. habrochaites. Plant Cell 12, 2283-2294.
192. Van Meer, G., Voelker, D.R. and Feigenson, G.W. (2008) Membrane lipid: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124.
193. Van Schie, C.C.N., Haring, M.A. and Schuurink, R.C. (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol. Biol. 64, 251-263.
194. Vihervaara, T., Jansen, M., Uronen, R.L. and Ohsaki, Y. (2011) Cytoplasmic oxysterol-binding proteins: sterol sensors of transporters? Chem. Phys. Lipids, 164, 443-450.
195. 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.
196. Wang, E. and Wagner, G.J. (2003) Elucidation of the functions of genes central to diterpene metabolism in tobacco trichomes using posttranscriptional gene silencing. Planta, 216, 686-691.
197. Wang, G., Tian, L., Aziz, N., Broun, P., Dai, X., He, J., King, A., Zhao, P.X. and Dixon, R.A. (2008) Terpene biosynthesis in glandular trichomes of hop. Plant Physiol. 148, 1254-1266.
198. Wang, W., Wang, Y., Zhang, Q., Qi, Y. and Guo, D. (2009) Global characterization of Artemisia annua glandular trichome transcriptome using 454 pyrosequencing. BMC Genomics, 10, 465.
199. Wang, Z., Xu, C. and Benning, C. (2012) TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J. 70, 614-623.
200. Warner, K.A., Rudall, P.J. and Frohlich, M.W. (2009) Environmental control of sepalness and petalness in perianth organs of waterlilies: a new mosaic theory for the evolutionary origin of a differentiated perianth. J. Exp. Bot. 60, 3559-3574.
201. Weathers, P.J., Arsenault, P.R., Covello, P.S., McMickle, A., Teoh, K.H. and Reed, D.W. (2011) Artemisinin production in Artemisia annua: studies in planta and results of a novel delivery method for treating malaria and other neglected diseases. Phytochem. Rev. 10, 173-183.
202. Werker, E. (2000) Trichome diversity and development. Adv. Bot. Res. 31, 1-35.
203. Wise, M.L., Savage, T.J., Katahira, E. and Croteau, R. (1998) Monoterpene synthases from common sage (Salvia officinalis). cRNA isolation, characterization, and functional expression of (+)-sabinene synthase, 1, 8-cineole synthase, and (+)-bornyl pyrophosphate synthase. J. Biol. Chem. 273, 14891-14899.
204. Wollenweber, E. and Schneider, H. (2000) Lipophilic exudates of Pteridaceae - chemistry and chemotaxonomy. Biochem. Syst. Ecol. 28, 751-777.
205. Wollenweber, E., Stevens, J.F., Icanic, M. and Deinzer, M.L. (1998) Acylphloroglucinols and flavonoid aglycones produced by external glands on the leaves of two Dryopteris ferns and Currania robertiana. Phytochemistry, 48, 931-939.
206. Xie, Z., Kapetyn, J. and Gang, D.R. (2008) A systems biology investigation of the MEP/terpenoid and shikimate/phenylpropanoid pathways points to multiple levels of metabolic control in sweet basil glandular trichomes. Plant J. 54, 349-361.
207. Xu, C., Fan, J., Cornish, A.J. and Benning, C. (2008) Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein. Plant Cell, 20, 2190-2204.
208. Yamaura, T., Tanaka, S. and Tabata, M. (1992) Localization of the biosynthesis and accumulation of monoterpenoids in glandular trichomes of thyme. Planta Med. 58, 153-158.
209. Yerger, E.H., Grazzini, R.A., Hesk, D., Cox-Foster, D.L., Craig, R. and Mumma, R.O. (1992) A rapid method for isolating glandular trichomes. Plant Physiol. 99, 1-7.
210. Yuba, A., Yazaki, K., Tabata, M., Honda, G. and Croteau, R.B. (1996) cDNA cloning, characterization, and functional expression of 4S-(-)-limonene synthase from Perilla frutescens. Arch. Biochem. Biophys. 332, 280-287.
211. Zhang, Y., Teoh, K.H., Reed, D.W. and Covello, P.S. (2008a) Molecular cloning and characterization of Dbr1, a 2-alkenal reductase from Artemisia annua. Botany, 87, 643-649.
212. Zhang, Y., Teoh, K.H., Reed, D.W., Maes, L., Goossens, A., Olson, D.J., Ross, A.R. and Covello, P.S. (2008b) The molecular cloning of artemisinic aldehyde Δ11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J. Biol. Chem. 283, 21501-21508.