Biosynthesis, function and metabolic engineering of plant volatile organic compounds

New Phytologist

Volumn 198, Issue 1, 2013, Pages 16-32

  Dudareva, Natalia ^a   Klempien, Antje ^a   Muhlemann, Joëlle K ^a   Kaplan, Ian ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Agriculture; Floral scent; Genetic modification; Plant biodiversity; Plant defense; Pollination; Volatile secondary metabolites

Indexed keywords

FATTY ACID; VOLATILE ORGANIC COMPOUND;

BIOLOGICAL PRODUCTION; CROP PLANT; ENZYME ACTIVITY; FUNCTIONAL ROLE; METABOLISM; PATHOGEN; PHYTOCHEMISTRY; PLANT DEFENSE; POLLINATOR; SECONDARY METABOLITE; SEED DISPERSAL; VOLATILE ORGANIC COMPOUND;

BIOSYNTHESIS; CHEMISTRY; METABOLIC ENGINEERING; METABOLISM; PLANT; REVIEW; VOLATILIZATION;

FATTY ACIDS; METABOLIC ENGINEERING; PLANTS; VOLATILE ORGANIC COMPOUNDS; VOLATILIZATION;

EID: 84874206168     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12145     Document Type: Review

References (188)

1. Adam K-P, Thiel R, Zapp J. 1999. Incorporation of 1-[1-13C]deoxy-d-xylulose in chamomile sesquiterpenes. Archives of Biochemistry and Biophysics 369: 127-132.
2. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FW, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ. 2003. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15: 2866-2884.
3. Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun ZK, Jongsma MA, Schwab W, Bouwmeester HJ. 2004. Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16: 3110-3131.
4. Aharoni A, Jongsma M, Kim T-Y, Ri M-B, Giri A, Verstappen F, Schwab W, Bouwmeester H. 2006. Metabolic engineering of terpenoid biosynthesis in plants. Phytochemistry Reviews 5: 49-58.
5. Ahumada I, Cairo A, Hemmerlin A, Gonzalez V, Pateraki I, Bach TJ, Rodriguez-Concepcion M, Campos N, Boronat A. 2008. Characterisation of the gene family encoding acetoacetyl-CoA thiolase in Arabidopsis. Functional Plant Biology 35: 1100-1111.
6. Ali JG, Alborn HT, Campos-Herrera R, Kaplan F, Duncan LW, Rodriguez-Saona C, Koppenhofer AM, Stelinski LL. 2012. Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. PLoS ONE 7: e38146.
7. Andriotis VM, Kruger NJ, Pike MJ, Smith AM. 2010. Plastidial glycolysis in developing Arabidopsis embryos. New Phytologist 185: 649-662.
8. Arimura G, Kost C, Boland W. 2005. Herbivore-induced indirect plant defences. Biochimica et Biophysica Acta 1734: 91-111.
9. Arimura G-I, Ozawa R, Kugimiya S, Takabayashi J, Bohlmann J. 2004. Herbivore-induced defense response in a model legume. Two-spotted spider mites induce emission of (E)-β-ocimene and transcript accumulation of (E)-β-ocimene synthase in Lotus japonicus. Plant Physiology 135: 1976-1983.
10. Arpaia S, De Cristofaro A, Guerrieri E, Bossi S, Cellini F, Di Leo GM, Germinara GS, Iodice L, Maffei ME, Petrozza A et al. 2011. Foraging activity of bumblebees (Bombus terrestris L.) on Bt-expressing eggplants. Arthropod-Plant Interactions 5: 255-261.
11. Ashman TL. 2000. Pollinator selectivity and its implication for the evolution of dioecy and sexual dimorphism. Ecology 85: 2577-2591.
12. Aubourg S, Lecharny A, Bohlmann J. 2002. Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Molecular Genetics and Genomics 267: 730-745.
13. Ayasse M, Stokl J, Francke W. 2011. Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry 72: 1667-1677.
14. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA. 2006. Volatile signaling in plant-plant interactions: "Talking trees" in the genomics era. Science 311: 812-815.
15. Bang BG, Cobb S. 1968. Size of olfactory bulb in 108 species of birds. Auk 85: 55-61.
16. Bayer RG, Stael S, Csaszar E, Teige M. 2011. Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11: 1287-1299.
17. Beck HC, Hansen AM, Lauritsen FR. 2002. Metabolite production and kinetics of branched-chain aldehyde oxidation in Staphylococcus xylosus. Enzyme and Microbial Technology 31: 94-101.
18. Bedon F, Bomal C, Caron S, Levasseur C, Boyle B, Mansfield SD, Schmidt A, Gershenzon J, Grima-Pettenati J, Séguin A et al. 2010. Subgroup 4 R2R3-MYBs in conifer trees: gene family expansion and contribution to the isoprenoid- and flavonoid-oriented responses. Journal of Experimental Botany 61: 3847-3864.
19. Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen FWA, Bouwmeester HJ, Aharoni A. 2004. Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiology 135: 1865-1878.
20. Ben Zvi MM, Negre-Zakharov F, Masci T, Ovadis M, Shklarman E, Ben-Meir H, Tzfira T, Dudareva N, Vainstein A. 2008. Interlinking showy traits: Co-engineering of scent and colour biosynthesis in flowers. Plant Biotechnology Journal 6: 403-415.
21. Bick JA, Lange BM. 2003. Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Archives of Biochemistry and Biophysics 415: 146-154.
22. Bleeker PM, Spyropoulou EA, Diergaarde PJ, Volpin H, De Both MT, Zerbe P, Bohlmann J, Falara V, Matsuba Y, Pichersky E et al. 2011. RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Molecular Biology 77: 323-336.
23. Boatright J, Negre F, Chen XL, Kish CM, Wood B, Peel G, Orlova I, Gang D, Rhodes D, Dudareva N. 2004. Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiology 135: 1993-2011.
24. Bohlmann J, Meyer-Gauen G, Croteau R. 1998. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proceedings of the National Academy of Sciences, USA 95: 4126-4133.
25. Borges RM, Bessiere JM, Hossaert-McKey M. 2008. The chemical ecology of seed dispersal in monoecious and dioecious figs. Functional Ecology 22: 484-493.
26. Cane DE 1999. Sesquiterpene biosynthesis: cyclization mechanisms. In: Cane DD, ed. Comprehensive natural products chemistry: isoprenoids including carotenoids and steroids. Amsterdam, the Netherlands: Elsevier, 155-200.
27. Cheng A-X, Xiang C-Y, Li J-X, Yang C-Q, Hu W-L, Wang L-J, Lou Y-G, Chen X-Y. 2007. The rice (E)-β-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 68: 1632-1641.
28. Colquhoun TA, Kim JY, Wedde AE, Levin LA, Schmitt KC, Schuurink RC, Clark DG. 2011. PhMYB4 fine-tunes the floral volatile signature of Petunia × hybrida through PhC4H. Journal of Experimental Botany 62: 1133-1143.
29. Colquhoun TA, Verdonk JC, Schimmel BC, Tieman DM, Underwood BA, Clark DG. 2010. Petunia floral volatile benzenoid/phenylpropanoid genes are regulated in a similar manner. Phytochemistry 71: 158-167.
30. D'Auria JC. 2006. Acyltransferases in plants: a good time to be BAHD. Current Opinion In Plant Biology 9: 331-340.
31. D'Auria JC, Chen F, Pichersky E, John TR. 2003. The SABATH family of MTs in Arabidopsis thaliana and other plant species. In: Romeo JT, ed. Recent advances in phytochemistry, vol. 37, Amsterdam, the Netherlands: Elsevier, 253-283.
32. D'Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J. 2007. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant Journal 49: 194-207.
33. Davidovich-Rikanati R, Lewinsohn E, Bar E, Iijima Y, Pichersky E, Sitrit Y. 2008. Overexpression of the lemon basil alpha-zingiberene synthase gene increases both mono- and sesquiterpene contents in tomato fruit. Plant Journal 56: 228-238.
34. Davidovich-Rikanati R, Sitrit Y, Tadmor Y, Iijima Y, Bilenko N, Bar E, Carmona B, Fallik E, Dudai N, Simon JE et al. 2007. Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway. Nature Biotechnology 25: 899-901.
35. Degenhardt J, Hiltpold I, Kollner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ. 2009a. Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proceedings of the National Academy of Sciences, USA 106: 13213-13218.
36. Degenhardt J, Köllner TG, Gershenzon J. 2009b. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70: 1621-1637.
37. Dexter R, Qualley A, Kish CM, Ma CJ, Koeduka T, Nagegowda DA, Dudareva N, Pichersky E, Clark D. 2007. Characterization of a petunia acetyltransferase involved in the biosynthesis of the floral volatile isoeugenol. Plant Journal 49: 265-275.
38. Dickinson JR, Harrison SJ, Dickinson JA, Hewlins MJ. 2000. An investigation of the metabolism of isoleucine to active amyl alcohol in Saccharomyces cerevisiae. Journal of Biological Chemistry 275: 10937-10942.
39. Dobson HEM. 1994. Floral volatiles in insect biology. In: Bernays EA, ed. Insect-plant interactions. Boca Raton, FL, USA: CRC Press, 47-81.
40. Dobson HEM. 2006. Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E, eds. Biology of floral scent. Boca Raton, FL, USA: CRC Press, 147-198.
41. van Doorn WG, Woltering EJ. 2008. Physiology and molecular biology of petal senescence. Journal of Experimental Botany 59: 453-480.
42. Dotterl S, Jurgens A. 2005. Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides? Plant Systematics and Evolution 255: 99-109.
43. Dotterl S, Jurgens A, Seifert K, Laube T, Weissbecker B, Schutz S. 2006. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytologist 169: 707-718.
44. Dotterl S, Wolfe LM, Jurgens A. 2005. Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66: 203-213.
45. Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J. 2005. The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proceedings of the National Academy of Sciences, USA 102: 933-938.
46. Dudareva N, Murfitt LM, Mann CJ, Gorenstein N, Kolosova N, Kish CM, Bonham C, Wood K. 2000. Developmental regulation of methyl benzoate biosynthesis and emission in snapdragon flowers. Plant Cell 12: 949-961.
47. Dudareva N, Negre F, Nagegowda DA, Orlova I. 2006. Plant volatiles: recent advances and future perspectives. Critical Reviews in Plant Sciences 25: 417-440.
48. Dudareva N, Pichersky E, Gershenzon J. 2004. Biochemistry of plant volatiles. Plant Physiology 135: 1893-1902.
49. Effmert U, Saschenbrecker S, Ross J, Negre F, Fraser CM, Noel JP, Dudareva N, Piechulla B. 2005. Floral benzenoid carboxyl methyltransferases: from in vitro to in planta function. Phytochemistry 66: 1211-1230.
50. Farhi M, Lavie O, Masci T, Hendel-Rahmanim K, Weiss D, Abeliovich H, Vainstein A. 2010. Identification of rose phenylacetaldehyde synthase by functional complementation in yeast. Plant Molecular Biology 72: 235-245.
51. Feussner I, Wasternack C. 2002. The lipoxygenase pathway. Annual review of plant biology 53: 275-297.
52. Flügge UI, Gao W. 2005. Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biology 7: 91-97.
53. Friis EM, Pedersen KR, Crane PR. 2006. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232: 251-293.
54. Furumoto T, Yamaguchi T, Ohshima-Ichie Y, Nakamura M, Tsuchida-Iwata Y, Shimamura M, Ohnishi J, Hata S, Gowik U, Westhoff P et al. 2011. A plastidial sodium-dependent pyruvate transporter. Nature 476: 472-475.
55. Gang DR, Lavid N, Zubieta C, Chen F, Beuerle T, Lewinsohn E, Noel JP, Pichersky E. 2002. Characterization of phenylpropene O-methyltransferases from sweet basil: facile change of substrate specificity and convergent evolution within a plant O-methyltransferase family. Plant Cell 14: 505-519.
56. Gardiner MA, Tuell JK, Isaacs R, Gibbs J, Ascher JS, Landis DA. 2010. Implications of three biofuel crops for beneficial arthropods in agricultural landscapes. Bioenergy Research 3: 6-19.
57. Gigot C, Ongena M, Fauconnier ML, Wathelet JP, Pd Jardin, Thonart P. 2010. The lipoxygenase metabolic pathway in plants: potential for industrial production of natural green leaf volatiles. Biotechnologie, Agronomie, Société et Environnement 14: 451-460.
58. Gonda I, Bar E, Portnoy V, Lev S, Burger J, Schaffer AA, Tadmor Y, Gepstein S, Giovannoni JJ, Katzir N et al. 2010. Branched-chain and aromatic amino acid catabolism into aroma volatiles in Cucumis melo L. Fruit. Journal of Experimental Botany 61: 1111-1123.
59. Gonzalez M, Gaete-Eastman C, Valdenegro M, Figueroa CR, Fuentes L, Herrera R, Moya-León MA. 2009. Aroma development during ripening of Fragaria chiloensis fruit and participation of an alcohol acyltransferase (FcAAT1) gene. Journal of Agricultural and Food Chemistry 57: 9123-9132.
60. Gouinguene SP, Turlings TC. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiology 129: 1296-1307.
61. Gruter C, Ratnieks FL. 2011. Flower constancy in insect pollinators: adaptive foraging behaviour or cognitive limitation? Communicative and Integrative Biology 4: 633-636.
62. Guirimand G, Guihur A, Phillips MA, Oudin A, Glevarec G, Melin C, Papon N, Clastre M, St-Pierre B, Rodriguez-Concepcion M et al. 2012. A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Molecular Biology 79: 443-459.
63. Gutensohn M, Klempien A, Kaminaga Y, Nagegowda DA, Negre-Zakharov F, Huh J-H, Luo H, Weizbauer R, Mengiste T, Tholl D et al. 2011. Role of aromatic aldehyde synthase in wounding/herbivory response and flower scent production in different Arabidopsis ecotypes. Plant Journal 66: 591-602.
64. Gutensohn M, Nagegowda DA, Dudareva N. 2013. Involvement of compartmentalization in monoterpene and sesquiterpene biosynthesis in plants. In: Bach TJ, Rohmer M, eds. Isoprenoid synthesis in plants and microorganisms. New York, NY, USA: Springer, 155-169.
65. Guterman I, Masci T, Chen XL, Negre F, Pichersky E, Dudareva N, Weiss D, Vainstein A. 2006. Generation of phenylpropanoid pathway-derived volatiles in transgenic plants: rose alcohol acetyltransferase produces phenylethyl acetate and benzyl acetate in petunia flowers. Plant Molecular Biology 60: 555-563.
66. Hammer KA, Carson CF, Riley TV. 2003. Antifungal activity of the components of Melaleuca alternifolia (tea tree) oil. Journal of Applied Microbiology 95: 853-860.
67. Hampel D, Mosandl A, Wüst M. 2005. Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. Phytochemistry 66: 305-311.
68. Hare JD. 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology 56: 161-180.
69. von Helversen O, Winkler L, Bestmann HJ. 2000. Sulphur-containing "Perfumes" attract flower-visiting bats. Journal of Comparative Physiology a-Sensory Neural and Behavioral Physiology 186: 143-153.
70. Hemmerlin A, Harwood JL, Bach TJ. 2012. A raison d'être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Progress in Lipid Research 51: 95-148.
71. Hemmerlin A, Hoeffler J-F, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M, Bach TJ. 2003. Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. Journal of Biological Chemistry 278: 26666-26676.
72. Henning JA, Teuber LR. 1992. Combined gas-chromatography-electroantennogram characterization of alfalfa floral volatiles recognized by honey bees (Hymenoptera, Apidae). Journal of Economic Entomology 85: 226-232.
73. Hiltpold I, Turlings TCJ. 2012. Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests and to improve crop yield. Journal of Chemical Ecology 38: 641-650.
74. Hodgkison R, Ayasse M, Kalko EK, Haberlein C, Schulz S, Mustapha WA, Zubaid A, Kunz TH. 2007. Chemical ecology of fruit bat foraging behavior in relation to the fruit odors of two species of paleotropical bat-dispersed figs (Ficus hispida and Ficus scortechinii). Journal of Chemical Ecology 33: 2097-2110.
75. Hong G-J, Xue X-Y, Mao Y-B, Wang L-J, Chen X-Y. 2012. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635-2648.
76. Hsieh MH, Chang CY, Hsu SJ, Chen JJ. 2008. Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in IspD and IspE albino mutants in Arabidopsis. Plant Molecular Biology 66: 663-673.
77. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D. 2012. The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytologist 193: 997-1008.
78. Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N et al. 2006. Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry 67: 1579-1589.
79. Jabalpurwala FA, Smoot JM, Rouseff RL. 2009. A comparison of citrus blossom volatiles. Phytochemistry 70: 1428-1434.
80. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N. 2010. Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Progress in Lipid Research 49: 128-158.
81. Junker RR, Gershenzon J, Unsicker SB. 2011. Floral odor bouquet loses its ant repellent properties after inhibition of terpene biosynthesis. Journal of Chemical Ecology 37: 1323-1331.
82. Kaminaga Y, Schnepp J, Peel G, Kish CM, Ben-Nissan G, Weiss D, Orlova I, Lavie O, Rhodes D, Wood K et al. 2006. Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. Journal of Biological Chemistry 281: 23357-23366.
83. Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC. 2004. Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiology 135: 483-495.
84. Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ. 2005. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309: 2070-2072.
85. Kessler A, Halitschke R, Poveda K. 2011. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92: 1769-1780.
86. Kessler D, Baldwin IT. 2007. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant Journal 49: 840-854.
87. Kessler D, Diezel C, Clark DG, Colquhoun TA, Baldwin IT. 2012. Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecology Letters. doi: 10.1111/ele.12038.
88. Kessler D, Gase K, Baldwin IT. 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321: 1200-1202.
89. Klahre U, Gurba A, Hermann K, Saxenhofer M, Bossolini E, Guerin PM, Kuhlemeier C. 2011. Pollinator choice in petunia depends on two major genetic loci for floral scent production. Current Biology 21: 730-739.
90. Klempien A, Kaminaga Y, Qualley A, Nagegowda DA, Widhalm JR, Orlova I, Shasany AK, Taguchi G, Kish CM, Cooper BR et al. 2012. Contribution of CoA ligases to benzenoid biosynthesis in petunia flowers. Plant Cell 24: 2015-2030.
91. Knudsen JT, Eriksson R, Gershenzon J, Stahl B. 2006. Diversity and distribution of floral scent. Botanical Review 72: 1-120.
92. Knudsen JT, Tollsten L, Groth I, Bergstrom G, Raguso RA. 2004. Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa. Botanical Journal of the Linnean Society 146: 191-199.
93. Koeduka T, Fridman E, Gang DR, Vassao DG, Jackson BL, Kish CM, Orlova I, Spassova SM, Lewis NG, Noel JP et al. 2006. Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. Proceedings of the National Academy of Sciences, USA 103: 10128-10133.
94. Koeduka T, Louie GV, Orlova I, Kish CM, Ibdah M, Wilkerson CG, Bowman ME, Baiga TJ, Noel JP, Dudareva N et al. 2008. The multiple phenylpropene synthases in both Clarkia breweri and Petunia hybrida represent two distinct protein lineages. Plant Journal 54: 362-374.
95. Kolosova N, Gorenstein N, Kish CM, Dudareva N. 2001. Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13: 2333-2347.
96. Kos M, Houshyani B, Overeem A-J, Bouwmeester HJ, Weldegergis BT, van Loon JJA, Dicke M, Vet LEM. 2013. Genetic engineering of plant volatile terpenoids: effects on a herbivore, a predator and a parasitoid. Pest Management Science 69: 302-311.
97. Lange BM, Rujan T, Martin W, Croteau R. 2000. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proceedings of the National Academy of Sciences, USA 97: 13172-13177.
98. Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M. 2003. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 100: 6866-6871.
99. Lavy M, Zuker A, Lewinsohn E, Larkov O, Ravid U, Vainstein A, Weiss D. 2002. Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene. Molecular Breeding 9: 103-111.
100. Lerdau M, Gray D. 2003. Ecology and evolution of light-dependent and light-independent phytogenic volatile organic carbon. New Phytologist 157: 199-211.
101. Lewinsohn E, Gijzen M. 2009. Phytochemical diversity: the sounds of silent metabolism. Plant Science 176: 161-169.
102. Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam K-H, Amar O, Lastochkin E, Larkov O, Ravid U et al. 2001. Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiology 127: 1256-1265.
103. Long MC, Nagegowda DA, Kaminaga Y, Ho KK, Kish CM, Schnepp J, Sherman D, Weiner H, Rhodes D, Dudareva N. 2009. Involvement of snapdragon benzaldehyde dehydrogenase in benzoic acid biosynthesis. Plant Journal 59: 256-265.
104. Losey JE, Vaughan M. 2006. The economic value of ecological services provided by insects. BioScience 56: 311-323.
105. Lu S, Xu R, Jia J-W, Pang J, Matsuda SPT, Chen X-Y. 2002. Cloning and functional characterization of a β-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiology 130: 477-486.
106. Lucker J, Bouwmeester HJ, Schwab W, Blaas J, van der Plas LH, Verhoeven HA. 2001. Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-β-D-glucopyranoside. Plant Journal 27: 315-324.
107. Lucker J, Schwab W, van Hautum B, Blaas J, van der Plas LH, Bouwmeester HJ, Verhoeven HA. 2004. Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiology 134: 510-519.
108. Lucker J, Verhoeven HA, van der Plas LH, Bouwmeester HJ. 2006. Molecular engineering of floral scent. In: Dudareva N, Pichersky E, eds. Biology of floral scent. Boca Raton, FL, USA: CRC Press, 321-337.
109. Maeda H, Dudareva N. 2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual review of plant biology 63: 73-105.
110. Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G, Cooper BR, Rhodes D, Pichersky E, Dudareva N. 2010. RNAi suppression of arogenate dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in petunia petals. Plant Cell 22: 832-849.
111. Majetic CJ, Raguso RA, Ashman TL. 2009. The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. Functional Ecology 23: 480-487.
112. Marino P, Raguso RA, Goffinet B. 2009. The ecology and evolution of fly dispersed dungmosses (family Splachnaceae): manipulating insect behaviour through odour and visual clues. Symbiosis 47: 61-76.
113. Martin DM, Gershenzon J, Bohlmann J. 2003. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of norway spruce. Plant Physiology 132: 1586-1599.
114. McConkey ME, Gershenzon J, Croteau RB. 2000. Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiology 122: 215-224.
115. McGarvey DJ, Croteau R. 1995. Terpenoid metabolism. Plant Cell 7: 1015-1026.
116. Morse A, Kevan P, Shipp L, Khosla S, McGarvey B. 2012. The impact of greenhouse tomato (Solanales: Solanaceae) floral volatiles on bumble bee (Hymenoptera: Apidae) pollination. Environmental Entomology 41: 855-864.
117. Muhlemann JK, Maeda H, Chang CY, San Miguel P, Baxter I, Cooper B, Perera MA, Nikolau BJ, Vitek O, Morgan JA et al. 2012. Developmental changes in the metabolic network of snapdragon flowers. PLoS ONE 7: e40381.
118. Muhlemann JK, Waelti MO, Widmer A, Schiestl FP. 2006. Postpollination changes in floral odor in Silene latifolia: adaptive mechanisms for seed-predator avoidance? Journal of Chemical Ecology 32: 1855-1860.
119. Mumm R, Dicke M. 2010. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Canadian Journal of Zoology-Revue Canadienne De Zoologie 88: 628-667.
120. 13C-labelled glycine in cultured cells of liverworts, Heteroscyphus planus and Lophocolea heterophylla. Journal of the Chemical Society-Perkin Transactions 1: 261-267.
121. Nagegowda DA, Gutensohn M, Wilkerson CG, Dudareva N. 2008. Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. Plant Journal 55: 224-239.
122. Nakamura A, Shimada H, Masuda T, Ohta H, Takamiya K. 2001. Two distinct isopentenyl diphosphate isomerases in cytosol and plastid are differentially induced by environmental stresses in tobacco. FEBS Letters 506: 61-64.
123. Negre F, Kish CM, Boatright J, Underwood B, Shibuya K, Wagner C, Clark DG, Dudareva N. 2003. Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers. Plant Cell 15: 2992-3006.
124. Oliver DJ, Nikolau BJ, Wurtele ES. 2009. Acetyl-CoA-Life at the metabolic nexus. Plant Science 176: 597-601.
125. Orlova I, Marshall-Colon A, Schnepp J, Wood B, Varbanova M, Fridman E, Blakeslee JJ, Peer WA, Murphy AS, Rhodes D 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.
126. Orlova I, Nagegowda DA, Kish CM, Gutensohn M, Maeda H, Varbanova M, Fridman E, Yamaguchi S, Hanada A, Kamiya Y et al. 2009. The small subunit of snapdragon geranyl diphosphate synthase modifies the chain length specificity of tobacco geranylgeranyl diphosphate synthase in planta. Plant Cell 21: 4002-4017.
127. Parachnowitsch AL, Raguso RA, Kessler A. 2012. Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytologist 195: 667-675.
128. Pareja M, Qvarfordt E, Webster B, Mayon P, Pickett J, Birkett M, Glinwood R. 2012. Herbivory by a phloem-feeding insect inhibits floral volatile production. PLoS ONE 7: e31971.
129. Pichersky E, Noel JP, Dudareva N. 2006. Biosynthesis of plant volatiles: nature's diversity and ingenuity. Science 311: 808-811.
130. Pulido P, Perello C, Rodriguez-Concepcion M. 2012. New insights into plant isoprenoid metabolism. Molecular Plant 5: 964-967.
131. Qualley AV, Widhalm JR, Adebesin F, Kish CM, Dudareva N. 2012. Completion of the core β-oxidative pathway of benzoic acid biosynthesis in plants. Proceedings of the National Academy of Sciences, USA 109: 16383-16388.
132. Raguso RA. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution, and Systematics 39: 549-569.
133. Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N, Philippe RN, Aeschliman D, White R, Huber D et al. 2006. Genomics of hybrid poplar (Populus trichocarpa × deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Molecular Ecology 15: 1275-1297.
134. Razal RA, Ellis S, Singh S, Lewis NG, Towers GHN. 1996. Nitrogen recycling in phenylpropanoid metabolism. Phytochemistry 41: 31-35.
135. Reineccius G. 2006. Flavor chemistry and technology. Boca Raton, FL, USA: CRC Press.
136. Reumann S, Babujee L, Ma CJ, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Lüder F, Weckwerth W, Jahn O. 2007. Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19: 3170-3193.
137. Rieseberg LH, Willis JH. 2007. Plant speciation. Science 317: 910-914.
138. Rodriguez-Saona C, Vorsa N, Singh AP, Johnson-Cicalese J, Szendrei Z, Mescher MC, Frost CJ. 2011. Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. Journal of Experimental Botany 62: 2633-2644.
139. Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, Laupitz R, Gräwert T, Amslinger S, Eisenreich W, Bacher A et al. 2003. The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proceedings of the National Academy of Sciences, USA 100: 1586-1591.
140. Sallaud C, Rontein D, Onillon S, Jabes F, Duffe P, Giacalone C, Thoraval S, Escoffier C, Herbette G, Leonhardt N et al. 2009. A novel pathway for sesquiterpene biosynthesis from Z, Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21: 301-317.
141. Schiestl FP. 2005. On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92: 255-264.
142. Schiestl FP, Ayasse M. 2001. Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 126: 531-534.
143. Schiestl FP, Huber FK, Gomez JM. 2011. Phenotypic selection on floral scent: trade-off between attraction and deterrence? Evolutionary Ecology 25: 237-248.
144. Schilmiller AL, Schauvinhold I, Larson M, Xu R, Charbonneau AL, Schmidt A, Wilkerson C, Last RL, Pichersky E. 2009. Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proceedings of the National Academy of Sciences, USA 106: 10865-10870.
145. Schluter PM, Xu S, Gagliardini V, Whittle E, Shanklin J, Grossniklaus U, Schiestl FP. 2011. Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids. Proceedings of the National Academy of Sciences, USA 108: 5696-56701.
146. Shalit M, Shafir S, Larkov O, Bar E, Kaslassi D, Adam Z, Zamir D, Vainstein A, Weiss D, Ravid U et al. 2004. Volatile compounds emitted by rose cultivars: fragrance perception by man and honeybees. Israel Journal of Plant Sciences 52: 245-255.
147. Simkin AJ, Guirimand G, Papon N, Courdavault V, Thabet I, Ginis O, Bouzid S, Giglioli-Guivarc'h N, Clastre M. 2011. Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta. Planta 234: 903-914.
148. Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ. 2004. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant Journal 40: 882-892.
149. Song M, Kim D, Lee S. 2005. Isolation and characterization of a jasmonic acid carboxyl methyltransferase gene from hot pepper (Capsicum annuum L.). Journal of Plant Biology 48: 292-297.
150. Spitzer-Rimon B, Marhevka E, Barkai O, Marton I, Edelbaum O, Masci T, Prathapani N-K, Shklarman E, Ovadis M, Vainstein A. 2010. EOBII, a gene encoding a flower-specific regulator of phenylpropanoid volatiles' biosynthesis in petunia. Plant Cell 22: 1961-1976.
151. Staudt M, Bertin N. 1998. Light and temperature dependence of the emission of cyclic and acyclic monoterpenes from holm oak (Quercus ilex L.) leaves. Plant, Cell & Environment 21: 385-395.
152. Tamiru A, Bruce TJA, Woodcock CM, Caulfield JC, Midega CAO, Ogol CKPO, Mayon P, Birkett MA, Pickett JA, Khan ZR. 2011. Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters 14: 1075-1083.
153. Tavaria FK, Dahl S, Carballo FJ, Malcata FX. 2002. Amino acid catabolism and generation of volatiles by lactic acid bacteria. Journal of Dairy Science 85: 2462-2470.
154. Theis N. 2006. Fragrance of canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. Journal of Chemical Ecology 32: 917-927.
155. Theis N, Adler LS. 2012. Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93: 430-435.
156. Theis N, Lerdau M, Raguso RA. 2007. The challenge of attracting pollinators while evading floral herbivores: patterns of fragrance emission in Cirsium arvense and Cirsium repandum (asteraceae). International Journal of Plant Sciences 168: 587-601.
157. Tholl D. 2006. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Current Opinion In Plant Biology 9: 297-304.
158. Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E. 2005. Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant Journal 42: 757-771.
159. Tholl D, Sohrabi R, Huh J-H, Lee S. 2011. The biochemistry of homoterpenes - common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry 72: 1635-1646.
160. Tieman DM, Loucas HM, Kim JY, Clark DG, Klee HJ. 2007. Tomato phenylacetaldehyde reductases catalyze the last step in the synthesis of the aroma volatile 2-phenylethanol. Phytochemistry 68: 2660-2669.
161. Tieman DM, Taylor MG, Schauer N, Fernie AR, Hanson AD, Klee HJ. 2006. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proceedings of the National Academy of Sciences, USA 103: 8287-8292.
162. Togni PHB, Laumann RA, Medeiros MA, Sujii ER. 2010. Odour masking of tomato volatiles by coriander volatiles in host plant selection of Bemisia tabaci biotype b. Entomologia Experimentalis et Applicata 136: 164-173.
163. Tzin V, Galili G. 2010. The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book 8: e0132.
164. Tzin V, Malitsky S, Ben Zvi MM, Bedair M, Sumner L, Aharoni A, Galili G. 2012. Expression of a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway in arabidopsis elucidates potential metabolic bottlenecks between primary and secondary metabolism. New Phytologist 194: 430-439.
165. Underwood BA, Tieman DM, Shibuya K, Dexter RJ, Loucas HM, Simkin AJ, Sims CA, Schmelz EA, Klee HJ, Clark DG. 2005. Ethylene-regulated floral volatile synthesis in petunia corollas. Plant Physiology 138: 255-266.
166. Unsicker SB, Kunert G, Gershenzon J. 2009. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Current Opinion In Plant Biology 12: 479-485.
167. Van Moerkercke A, Galvan-Ampudia CS, Verdonk JC, Haring MA, Schuurink RC. 2012. Regulators of floral fragrance production and their target genes in petunia are not exclusively active in the epidermal cells of petals. Journal of Experimental Botany 63: 3157-3171.
168. Van Moerkercke A, Schauvinhold I, Pichersky E, Haring MA, Schuurink RC. 2009. A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production. Plant Journal 60: 292-302.
169. Van Moerkercke A, Haring MA, Schuurink RC. 2011. The transcription factor emission of benzenoids II activates the MYB ODORANT1 promoter at a MYB binding site specific for fragrant petunias. Plant Journal 67: 917-928.
170. Vassao DG, Gang DR, Koeduka T, Jackson B, Pichersky E, Davin LB, Lewis NG. 2006. Chavicol formation in sweet basil (Ocimum basilicum): cleavage of an esterified C9 hydroxyl group with NAD(P)H-dependent reduction. Organic and Biomolecular Chemistry 4: 2733-2744.
171. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC. 2005. ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17: 1612-1624.
172. Vickers CE, Gershenzon J, Lerdau MT, Loreto F. 2009. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nature Chemical Biology 5: 283-291.
173. Vogel JT, Tan B-C, McCarty DR, Klee HJ. 2008. The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. Journal of Biological Chemistry 283: 11364-11373.
174. Waelti MO, Muhlemann JK, Widmer A, Schiestl FP. 2008. Floral odour and reproductive isolation in two species of Silene. Journal of Evolutionary Biology 21: 111-121.
175. Ward JL, Baker JM, Llewellyn AM, Hawkins ND, Beale MH. 2011. Metabolomic analysis of Arabidopsis reveals hemiterpenoid glycosides as products of a nitrate ion-regulated, carbon flux overflow. Proceedings of the National Academy of Sciences, USA 108: 10762-10767.
176. Winterhalter P, Rouseff R. 2001. Carotenoid-derived aroma compounds: an introduction. In: Winterhalter P, Rouseff R, eds. Carotenoid-derived aroma compounds. Washington, DC, USA: American Chemical Society, 1-17.
177. Wise ML, Croteau R 1999. Monoterpene biosynthesis. In: Cane DD, ed. Comprehensive natural products chemistry: isoprenoids including carotenoids and steroids. Amsterdam, the Netherlands: Elsevier, 97-153.
178. Wolfe LM. 2002. Why alien invaders succeed: support for the escape-from-enemy hypothesis. American Naturalist 160: 705-711.
179. Wright GA, Lutmerding A, Dudareva N, Smith BH. 2005. Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera). Journal of Comparative Physiology A - Neuroethology, Sensory, Neural, and Behavioral Physiology 191: 105-114.
180. Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappell J. 2006. Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nature biotechnology 24: 1441-1447.
181. Xiao Y, Wang Q, Erb M, Turlings TC, Ge L, Hu L, Li J, Han X, Zhang T, Lu J et al. 2012. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecology Letters 15: 1130-1139.
182. Xu S, Schluter PM, Grossniklaus U, Schiestl FP. 2012. The genetic basis of pollinator adaptation in a sexually deceptive orchid. PLoS Genetics 8: e1002889.
183. Young AM, Severson DW. 1994. Comparative analysis of steam distilled floral oils of cacao cultivars (Theobroma cacao L., Sterculiaceae) and attraction of flying insects - implications for a Theobroma pollination syndrome. Journal of Chemical Ecology 20: 2687-2703.
184. Youngsteadt E, Nojima S, Haberlein C, Schulz S, Schal C. 2008. Seed odor mediates an obligate ant-plant mutualism in amazonian rainforests. Proceedings of the National Academy of Sciences, USA 105: 4571-4575.
185. Zebelo SA, Maffei ME. 2012. Signal transduction in plant-insect interactions: from membrane potential variations to metabolomics. In: Volkov AG, ed. Plant electrophysiology. Berlin & Heidelberg Germany: Springer, 143-172.
186. Zebelo SA, Matsui K, Ozawa R, Maffei ME. 2012. Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Science 196: 93-100.
187. Zuker A, Tzfira T, Ben-Meir H, Ovadis M, Shklarman E, Itzhaki H, Forkmann G, Martens S, Neta-Sharir I, Weiss D et al. 2002. Modification of flower color and fragrance by antisense suppression of the flavanone 3-hydroxylase gene. Molecular Breeding 9: 33-41.
188. Zvi MM, Shklarman E, Masci T, Kalev H, Debener T, Shafir S, Ovadis M, Vainstein A. 2012. PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers. New Phytologist 195: 335-345.