, Volume 249, Issue 1, pp 71–93 | Cite as

Functional characterization and expression analysis of two terpene synthases involved in floral scent formation in Lilium ‘Siberia’

  • Farhat Abbas
  • Yanguo Ke
  • Rangcai YuEmail author
  • Yanping FanEmail author
Original Article
Part of the following topical collections:
  1. Terpenes and Isoprenoids


Main conclusion

Floral scent formation in Lilium ‘Siberia’ is mainly due to monoterpene presence in the floral profile. LoTPS1 and LoTPS3 are responsible for the formation of (±)-linalool and β-ocimene in Lilium ‘Siberia’.

Lilium ‘Siberia’ is a perennial herbaceous plant belonging to Liliaceae family, cultivated both as a cut flower and garden plant. The snowy white flower emits a pleasant aroma which is mainly caused by monoterpenes present in the floral volatile profile. Previously terpene synthase (TPS) genes have been isolated and characterized from various plant species but less have been identified from Liliaceae family. Here, two terpene synthase genes (LoTPS1 and LoTPS3), which are highly expressed in sepals and petals of Lilium ‘Siberia’ flower were functionally characterized recombinant LoTPS1 specifically catalyzes the formation of (Z)-β-ocimene and (±)-linalool as its main volatile compounds from geranyl pyrophosphate (GPP), whereas LoTPS3 is a promiscuous monoterpene synthase which utilizes both GPP and farnesyl pyrophosphate (FPP) as a substrate to generate (±)-linalool and cis-nerolidol, respectively. Transcript levels of both genes were prominent in flowering parts, especially in sepals and petals which are the main source of floral scent production. The gas chromatography–mass spectrometry (GC–MS) and quantitative real-time PCR analysis revealed that the compounds were emitted throughout the day, prominently during the daytime and lower levels at night following a strong circadian rhythm in their emission pattern. Regarding mechanical wounding, both genes showed considerable involvement in floral defense by inducing the emission of (Z)-β-ocimene and (±)-linalool, elevating the transcript accumulation of LoTPS1 and LoTPS3. Furthermore, the subcellular localization experiment revealed that LoTPS1 was localized in plastids, whilst LoTPS3 in mitochondria. Our findings on these two TPSs characterized from Lilium ‘Siberia’ provide new insights into molecular mechanisms of terpene biosynthesis in this species and also provide an opportunity for biotechnological modification of floral scent profile of Lilium.


Floral scent Linalool β-Ocimene Nerolidol Terpene synthases Lilium ‘Siberia’ 



Terpene synthase


Geranyl pyrophosphate


Farnesyl pyrophosphate


Gas chromatography–mass spectrometry


Isopentenyl pyrophosphate


Dimethylallyl pyrophosphate


Methylerythritol phosphate


Mevalonic acid


Geranylgeranyl diphosphate


Open reading frame


Quantitative real-time polymerase chain reaction


Green fluorescence protein


Monoterpene synthases


Terpene synthases


Gene ontology






Phenylmethanesulfonyl fluoride


Bovine serum albumin




Laser scanning confocal microscopy


Reverse transcription PCR


Decanoic acid



This work was supported in part by the Ministry of Education Program to Rangcai Yu: Promote Scientific Research and High-level Personnel Training of Cooperation with the American and Oceanica areas, International Cooperation of Science and Technology Research of Guangdong to Rangcai Yu (Grant no. 2009B050700038), and a Specialized Major Project of the Production-Study-Research Collaborative Innovation of Guangzhou Science and Information Bureau to Yanping Fan (Grant no. 156100058).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

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  1. Abbas F, Ke Y, Yu R, Yue Y, Amanullah S, Jahangir MM, Fan YP (2017) Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering. Planta 246:803–816Google Scholar
  2. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FW et al (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884Google Scholar
  3. Aharoni A, Giri AP, Verstappen FW, Bertea CM, Sevenier R, Sun Z et al (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131Google Scholar
  4. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602Google Scholar
  5. Arimura GI, 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 Physiol 135:1976–1983Google Scholar
  6. Arimura GI, Garms S, Maffei M, Bossi S, Schulze B, Leitner M et al (2008) Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta 227:453–464Google Scholar
  7. Aros D, Gonzalez V, Allemann RK, Müller CT, Rosati C, Rogers HJ (2012) Volatile emissions of scented Alstroemeria genotypes are dominated by terpenes, and a myrcene synthase gene is highly expressed in scented Alstroemeria flowers. J Exp Bot 63:2739–2752Google Scholar
  8. Bergougnoux V, Caissard JC, Jullien F, Magnard JL, Scalliet G, Cock JM et al (2007) Both the adaxial and abaxial epidermal layers of the rose petal emit volatile scent compounds. Planta 226:853–866Google Scholar
  9. Birkett MA, Campbell CA, Chamberlain K, Guerrieri E, Hick AJ, Martin JL et al (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97:9329–9334Google Scholar
  10. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133Google Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  12. Chang YT, Chu FH (2011) Molecular cloning and characterization of monoterpene synthases from Litsea cubeba (Lour.) Persoon. Tree Genet Genomes 7:835–844. Google Scholar
  13. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66:212–229Google Scholar
  14. Cheng S, Fu X, Mei X, Zhou Y, Du B, Watanabe N et al (2016) Regulation of biosynthesis and emission of volatile phenylpropanoids/benzenoids in petunia × hybrida flowers by multi-factors of circadian clock, light, and temperature. Plant Physiol Biochem 107:1–8Google Scholar
  15. Corley J (2007) Fragrances for natural and certified organic personal care products: the link between fragrance and health in personal care product development. Perfum Flavorist 32:24–28Google Scholar
  16. Crowell AL, Williams DC, Davis EM, Wildung MR, Croteau R (2002) Molecular cloning and characterization of a new linalool synthase. Arch Biochem Biophys 405:112–121Google Scholar
  17. Cseke L, Dudareva N, Pichersky E (1998) Structure and evolution of linalool synthase. Mol Biol Evol 15:1491–1498Google Scholar
  18. Cunillera N, Boronat A, Ferrer A (1997) The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 272:15381–15388Google Scholar
  19. Danner H, Boeckler GA, Irmisch S, Yuan JS, Chen F, Gershenzon J et al (2011) Four terpene synthases produce major compounds of the gypsy moth feeding-induced volatile blend of Populus trichocarpa. Phytochemistry 72:897–908Google Scholar
  20. Davis E, Croteau R (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Biosynthesis. Google Scholar
  21. Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637Google Scholar
  22. Delfine S, Csiky O, Seufert G, Loreto F (2000) Fumigation with exogenous monoterpenes of a non-isoprenoid-emitting oak (Quercus suber): monoterpene acquisition, translocation, and effect on the photosynthetic properties at high temperatures. New Phytol 146:27–36Google Scholar
  23. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–634Google Scholar
  24. Dudareva N, Cseke L, Blanc VM, Pichersky E (1996) Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell 8:1137–1148Google Scholar
  25. Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt J et al (2003) (E)-β-Ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15:1227–1241Google Scholar
  26. Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D et al (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102:933–938Google Scholar
  27. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32Google Scholar
  28. Fahnrich A, Krause K, Piechulla B (2011) Product variability of the ‘cineole cassette’monoterpene synthases of related Nicotiana species. Mol Plant 4:965–984Google Scholar
  29. Falara V, Akhtar TA, Nguyen TT, Spyropoulou EA, Bleeker PM, Schauvinhold I et al (2011) The tomato terpene synthase gene family. Plant Physiol 157:770–789Google Scholar
  30. Faldt J, Martin D, Miller B, Rawat S, Bohlmann J (2003) Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol Biol 51:119–133Google Scholar
  31. Fan YP, Wang XR, Yu RC, Yang P (2007) Analysis on the aroma components in several species of Hedychium. Acta Hortic Sin 34(1):231 (in Chinese) Google Scholar
  32. Galata M, Sarker LS, Mahmoud SS (2014) Transcriptome profiling, and cloning and characterization of the main monoterpene synthases of Coriandrum sativum L. Phytochemistry 102:64–73Google Scholar
  33. Ginglinger JF, Boachon B, Höfer R, Paetz C, Köllner TG, Miesch L et al (2013) Gene coexpression analysis reveals complex metabolism of the monoterpene alcohol linalool in Arabidopsis flowers. Plant Cell 25:4640–4657Google Scholar
  34. Green SA, Chen X, Nieuwenhuizen NJ, Matich AJ, Wang MY, Bunn BJ et al (2011) Identification, functional characterization, and regulation of the enzyme responsible for floral (E)-nerolidol biosynthesis in kiwifruit (Actinidia chinensis). J Exp Bot 63:1951–1967Google Scholar
  35. Gutensohn M, Orlova I, Nguyen TT, Davidovich-Rikanati R, Ferruzzi MG, Sitrit Y et al (2013) Cytosolic monoterpene biosynthesis is supported by plastid-generated geranyl diphosphate substrate in transgenic tomato fruits. Plant J 75:351–363Google Scholar
  36. Helsper JP, Davies JA, Bouwmeester HJ, Krol AF, van Kampen MH (1998) Circadian rhythmicity in emission of volatile compounds by flowers of Rosa hybrida L. cv. Honesty. Planta 207:88–95Google Scholar
  37. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648Google Scholar
  38. Hsiao YY, Jeng MF, Tsai WC, Chuang YC, Li CY, Wu TS et al (2008) A novel homodimeric geranyl diphosphate synthase from the orchid Phalaenopsis bellina lacking a DD(X)2–4D motif. Plant J 55:719–733Google Scholar
  39. 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 Mol Biol 66:663–673Google Scholar
  40. Hu Z, Zhang H, Leng P, Zhao J, Wang W, Wang S (2013) The emission of floral scent from Lilium ‘siberia’ in response to light intensity and temperature. Acta Physiol Plant 35:1691–1700Google Scholar
  41. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J et al (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008Google Scholar
  42. Hyatt DC, Youn B, Zhao Y, Santhamma B, Coates RM, Croteau RB et al (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Proc Natl Acad Sci USA 104:5360–5365Google Scholar
  43. Jayaramaiah RH, Anand A, Beedkar SD, Dholakia BB, Punekar SA, Kalunke RM et al (2016) Functional characterization and transient expression manipulation of a new sesquiterpene synthase involved in β-caryophyllene accumulation in Ocimum. Biochem Biophys Res Commun 473:265–271Google Scholar
  44. Jia JW, Crock J, Lu S, Croteau R, Chen XY (1999) (3R)-Linalool synthase from Artemisia annua L.: cDNA isolation, characterization, and wound induction. Arch Biochem Biophys 372:143–149Google Scholar
  45. Jin J, Kim MJ, Dhandapani S, Tjhang JG, Yin JL, Wong L et al (2015) The floral transcriptome of ylang ylang (Cananga odorata var. fruticosa) uncovers biosynthetic pathways for volatile organic compounds and a multifunctional and novel sesquiterpene synthase. J Exp Bot 66:3959–3975Google Scholar
  46. Jones CG, Moniodis J, Zulak KG, Scaffidi A, Plummer JA, Ghisalberti EL et al (2012) Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase (TPS)-a and TPS-b subfamilies, including santalene synthases. J Biol Chem 287:37713. Google Scholar
  47. Kappers IF, Aharoni A, Van Herpen TW, Luckerhoff LL, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072Google Scholar
  48. Kite GC, Leon C (1995) Volatile compounds emitted from flowers and leaves of Brugmansia × candida (Solanaceae). Phytochemistry 40:1093–1095Google Scholar
  49. Knudsen JT, Tollsten L, Bergström LG (1993) Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280Google Scholar
  50. Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120Google Scholar
  51. Kolosova N, Gorenstein N, Kish CM, Dudareva N (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:2333–2347Google Scholar
  52. Kong Y, Sun M, Pan HT, Zhang QX (2012) Composition and emission rhythm of floral scent volatiles from eight lily cut flowers. J Am Soc Hortic Sci 137:376–382Google Scholar
  53. Landmann C, Fink B, Festner M, Dregus M, Engel KH, Schwab W (2007) Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Arch Biochem Biophys 465:417–429Google Scholar
  54. Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities. Plant Biotechnol J 11:169–196Google Scholar
  55. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948Google Scholar
  56. Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB et al (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871Google Scholar
  57. Lee S, Chappell J (2008) Biochemical and genomic characterization of terpene synthases in Magnolia grandiflora. Plant Physiol 147:1017–1033Google Scholar
  58. Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam KH 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 127:1256–1265Google Scholar
  59. Li RH, Fan YP (2007) Changes in floral aroma constituents in Hedychium coronarium Koenig during different blooming stages. Plant Physiol Commun 43:176Google Scholar
  60. Li RH, Fan YP (2011) Molecular cloning and expression analysis of a terpene synthase gene, HcTPS2, in Hedychium coronarium. Plant Mol Biol Rep 29:35–42Google Scholar
  61. Lin YL, Lee YR, Huang WK, Chang ST, Chu FH (2014) Characterization of S-(+)-linalool synthase from several provenances of Cinnamomum osmophloeum. Tree Genet Genomes 10:75–86. Google Scholar
  62. Lu S, Xu R, Jia JW, Pang J, Matsuda SP, Chen XY (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. Google Scholar
  63. 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 Slinalyl-β-d-glucopyranoside. Plant J 27:315–324Google Scholar
  64. Lucker J, El Tamer MK, Schwab W, Verstappen FW, van der Plas LH, Bouwmeester HJ et al (2002) Monoterpene biosynthesis in lemon (Citrus limon). FEBS J 269:3160–3171. Google Scholar
  65. Luo D, Xu H, Liu Z, Guo J, Li H, Chen L et al (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573. Google Scholar
  66. Majetic CJ, Raguso RA, Ashman TL (2009) The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. Funct Ecol 23:480–487Google Scholar
  67. Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O et al (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10b:226. Google Scholar
  68. Martín D, Piulachs MD, Cunillera N, Ferrer A, Bellés X (2007) Mitochondrial targeting of farnesyl diphosphate synthase is a widespread phenomenon in eukaryotes. Biochim Biophys Acta 1773:419–426. Google Scholar
  69. McWatters HG, Roden LC, Staiger D (2001) Picking out parallels: plant circadian clocks in context. Philos Trans R Soc Lond B Biol Sci Ser B 356:1735–1743. Google Scholar
  70. Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:1936–1949. Google Scholar
  71. 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 J 55:224–239Google Scholar
  72. Nieuwenhuizen NJ, Wang MY, Matich AJ, Green SA, Chen X, Yauk YK et al (2009) Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa). J Exp Bot 60:3203–3219Google Scholar
  73. Okada K, Saito T, Nakagawa T, Kawamukai M, Kamiya Y (2000) Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol 122:1045–1056Google Scholar
  74. Pichersky E, Dudareva N (2007) Scent engineering: toward the goal of controlling how flowers smell. Trends Biotechnol 25:105–110Google Scholar
  75. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243Google Scholar
  76. Pichersky E, Raguso RA, Lewinsohn E, Croteau R (1994) Floral scent production in Clarkia (Onagraceae) (I. Localization and developmental modulation of monoterpene emission and linalool synthase activity). Plant Physiol 106:1533–1540Google Scholar
  77. Pulido P, Perello C, Rodriguez-Concepcion M (2012) New insights into plant isoprenoid metabolism. Mol Plant 5:964–967Google Scholar
  78. Rohrbeck D, Buss D, Effmert U, Piechulla B (2006) Localization of methyl benzoate synthesis and emission in Stephanotis floribunda and Nicotiana suaveolens flowers. Plant Biol 8:615–626Google Scholar
  79. Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656Google Scholar
  80. Schnee C, Köllner TG, Gershenzon J, Degenhardt J (2002) The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-β-farnesene,(E)-nerolidol, and (E,E)-farnesol after herbivore damage. Plant Physiol 130:2049–2060Google Scholar
  81. Schuurink RC, Haring MA, Clark DG (2006) Regulation of volatile benzenoid biosynthesis in petunia flowers. Trends Plant Sci 11:20–25Google Scholar
  82. Sharkey TD, Yeh S (2001) Isoprene emission from plants. Ann Rev Plant Biol 52:407–436Google Scholar
  83. Shimada T, Endo T, Fujii H, Hara M, Omura M (2005) Isolation and characterization of (E)-beta-ocimene and 1, 8 cineole synthases in Citrus unshiu Marc. Plant Sci 168:987–995Google Scholar
  84. Simkin AJ, Guirimand G, Papon N, Courdavault V, Thabet I, Ginis O et al (2011) Peroxisomal localization of the final steps of the mevalonic acid pathway in planta. Planta 234:903–914Google Scholar
  85. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739Google Scholar
  86. Thabet I, Guirimand G, Guihur A, Lanoue A, Courdavault V, Papon N et al (2012) Characterization and subcellular localization of geranylgeranyl diphosphate synthase from Catharanthus roseus. Mol Biol Rep 39:3235–3243Google Scholar
  87. Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304Google Scholar
  88. 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 J 42:757–771Google Scholar
  89. van Schie CC, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64:251–263Google Scholar
  90. Wang J, Fuguang LI, Qianru LI et al (2002) Construction of a screening vector by cloning the green fluorescent protein gene into the plasmid pUC18. J Henan Med Univ. Google Scholar
  91. 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. Nat Biotechnol 24:1441–1447Google Scholar
  92. Yahyaa M, Tholl D, Cormier G, Jensen R, Simon PW, Ibdah M (2015) Identification and characterization of terpene synthases potentially involved in the formation of volatile terpenes in carrot (Daucus carota L.) roots. J Agric Food Chem 63:4870–4878Google Scholar
  93. Yang CQ, Wu XM, Ruan JX, Hu WL, Mao YB, Chen XY et al (2013) Isolation and characterization of terpene synthases in cotton (Gossypium hirsutum). Phytochemistry 96:46–56Google Scholar
  94. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565. Google Scholar
  95. Yu F, Utsumi R (2009) Diversity, regulation, and genetic manipulation of plant mono-and sesquiterpenoid biosynthesis. Cell Mol Life Sci 66:3043–3052Google Scholar
  96. Yuan JS, Köllner TG, Wiggins G, Grant J, Degenhardt J, Chen F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J 55:491–503Google Scholar
  97. Yue YY, Yu RC, Fan YP (2014) Characterization of two monoterpene synthases involved in floral scent formation in Hedychium coronarium. Planta 240:745–762Google Scholar
  98. Yue YY, Yu RC, Fan YP (2015) Transcriptome profiling provides new insights into the formation of floral scent in Hedychium coronarium. BMC Genom 16:470Google Scholar
  99. Zeng H, Bio T, Qi W, Jian Z, Ping SL, Ke ZZ (2017) Transcriptome sequencing analysis reveals a difference in monoterpene biosynthesis between scented Lilium ‘Siberia’ and unscented Lilium ‘Novano’. Front Plant Sci 8:1351. Google Scholar
  100. Zhang HX, Leng PS, Zeng H, Hu ZH, Zhao J, Wang WH, Xu F et al (2013) The floral scent emitted from Lilium ‘Siberia’ at different flowering stages and diurnal variation. Acta Hortic Sin 40:693–702Google Scholar
  101. Zhang TX, Sun M, Li LL, Guo YH, Xie XH, Hu BW (2017) Molecular cloning and expression analysis of a monoterpene synthase gene involved in floral scent production in lily (Lilium ‘Siberia’). Russ J Plant Physiol 64:600–607Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.The Research Center for Ornamental Plants, College of Forestry and Landscape ArchitectureSouth China Agricultural UniversityGuangzhouChina
  2. 2.College of Life SciencesSouth China Agricultural UniversityGuangzhouChina
  3. 3.Department of Horticulture, College of AgricultureUniversity of SargodhaPunjabPakistan
  4. 4.Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural UniversityGuangzhouChina

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