DOI QR코드

DOI QR Code

Improvement of floral scent of ornamentals via metabolic engineering

화훼작물의 향기 성분 증대를 위한 대사 공학

  • Kang, Seung-Won (Department of Applied Plant Science, Chung-Ang University) ;
  • Seo, Sang-Gyu (Natural Science Research Institute, University of Seoul) ;
  • Ryu, So-Young (Department of Applied Plant Science, Chung-Ang University) ;
  • Pak, Chun-Ho (Division of Biotechnology, College of Life Sciences and Biotechnology, Korea University) ;
  • Lee, Gung-Pyo (Department of Applied Plant Science, Chung-Ang University)
  • 강승원 (중앙대학교 식물응용과학과) ;
  • 서상규 (서울시립대학교 자연과학연구소) ;
  • 류소영 (중앙대학교 식물응용과학과) ;
  • 박천호 (고려대학교 생명과학대학 생명공학부) ;
  • 이긍표 (중앙대학교 식물응용과학과)
  • Received : 2010.03.05
  • Accepted : 2010.03.17
  • Published : 2010.03.31

Abstract

Floral scent emitted from many plants is the key factor for pollinator attraction and defense for survival in nature and is important industrial materials for perfumery as well. It is a complex mixture of various organic molecules with a high volatility or a high vapor pressure. In general, floral scents are divided into three categories, aliphatics, terpenoids, and phenylpropanoids/benzenoids, based on its origin. About 1,700 scent compounds have been identified and their biochemistry and molecular biology also have elucidated their biosynthesis from various flowering plants during the last ten years. In addition to improvement of vase life, flower color and shape, and/or disease resistance, floral scent is coming up to the major breeding target for improvement of marketability. Therefore, metabolic engineering can be an important tool in near future and may be able to facilitate the breeding program for novel cultivar selection and improvement of marketability of floricultural crops.

Keywords

References

  1. Abd El-Mawla A, Beerhues L (2002) Benzoic acid biosynthesis in cell cultures of Hypericum androsaemum. Planta 214:727-733 https://doi.org/10.1007/s004250100657
  2. Adam K-P, Thiel R, Zapp J (1999) Incorporation of $1-[1-^{13}C]$ deoxy-D-xylulose in chamomile sesquiterpenes. Archives of Biochemistry and Biophysics 369:127-132 https://doi.org/10.1006/abbi.1999.1346
  3. Akiyama K, Matsuzaki K-i, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824-827 https://doi.org/10.1038/nature03608
  4. Aranovich D, Lewinsohn E, Zaccai M (2007) Post-harvest enhancement of aroma in transgenic lisianthus (Eustoma grandiflorum) using the Clarkia breweri benzyl alcohol acetyltransferase (BEAT) gene. Postharvest Biology and Technology 43:255-260 https://doi.org/10.1016/j.postharvbio.2006.09.001
  5. Arimura G-i, Kopke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol 146:965-973 https://doi.org/10.1104/pp.107.111088
  6. Becker A, Lange M (2010) VIGS - genomics goes functional. Trends in Plant Science 15:1-4 https://doi.org/10.1016/j.tplants.2009.09.002
  7. Beuerle T, Pichersky E (2002) Purification and characterization of benzoate:coenzyme A ligase from Clarkia breweri. Archives of Biochemistry and Biophysics 400:258-264 https://doi.org/10.1016/S0003-9861(02)00026-7
  8. Boatright J, Negre F, Chen X, 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 Physiol 135:1993-2011 https://doi.org/10.1104/pp.104.045468
  9. Bohlmann J, Gershenzon J, Aubourg S (2000) Biochemical, molecular, genetic and evolutionary aspects of defense-related terpenoid metabolism in conifers Recent Advances in Phytochemistry 34:109-150 https://doi.org/10.1016/S0079-9920(00)80006-4
  10. Bottcher C, von Roepenack-Lahaye E, Schmidt J, Schmotz C, Neumann S, Scheel D, Clemens S (2008) Metabolome analysis of biosynthetic mutants reveals a diversity of metabolic changes and allows identification of a large number of new compounds in arabidopsis. Plant Physiol 147:2107-2120 https://doi.org/10.1104/pp.108.117754
  11. Bruhn CM, Feldman N, Garlitz C, Haewood J, Ivans E, Marshall M, Riley A, Thurber D, Williamson E (1991) Consumer perceptions of quality: Apricots, cantaloupes, peaches, pears, strawberries, and tomatoes. Journal of Food Quality 14:187-195 https://doi.org/10.1111/j.1745-4557.1991.tb00060.x
  12. Burch-Smith TM, Schiff M, Liu Y, Dinesh-Kumar SP (2006) Efficient virus-induced gene silencing in arabidopsis. Plant Physiol 142:21-27 https://doi.org/10.1104/pp.106.084624
  13. Channeliere S, Rivière S, Scalliet G, Szecsi J, Jullien F, Dolle C, Vergne P, Dumas C, Bendahmane M, Hugueney P, Cock JM (2002) Analysis of gene expression in rose petals using expressed sequence tags. FEBS Letters 515:35-38 https://doi.org/10.1016/S0014-5793(02)02413-4
  14. Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from arabidopsis Flowers. Plant Cell 15:481-494 https://doi.org/10.1105/tpc.007989
  15. Collu G, Unver N, Peltenburg-Looman AMG, van der Heijden R, Verpoorte R, Memelink J (2001) Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Letters 508:215-220 https://doi.org/10.1016/S0014-5793(01)03045-9
  16. 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. The Plant Journal 56:228-238 https://doi.org/10.1111/j.1365-313X.2008.03599.x
  17. Dexter RJ, Verdonk JC, Underwood BA, Shibuya K, Schmelz EA, Clark DG (2008) Tissue-specific PhBPBT expression is differentially regulated in response to endogenous ethylene. Journal of Experimental Botany 59:609-618 https://doi.org/10.1093/jxb/erm337
  18. Dicke M, Loreto F (2010) Induced plant volatiles: from genes to climate change. Trends in Plant Science In Press, DOI: 10.1016/j.tplants.2010.01.007
  19. 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 8:1137-1148 https://doi.org/10.1105/tpc.8.7.1137
  20. 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 https://doi.org/10.1105/tpc.12.6.949
  21. Dudareva N, Pichersky E (2006) Floral scent metabolic pathways: Their regulation and evolution. In Biology of floral scent, N. Dudareva and E. Pichersky, eds., Boca Raton, FL., CLC Press, USA
  22. Eisenreich W, Sagner S, Zenk MH, Bacher A (1997) Monoterpenoid essential oils are not of mevalonoid origin. Tetrahedron Letters 38:3889-3892 https://doi.org/10.1016/S0040-4039(97)00761-2
  23. Goff SA, Klee HJ (2006) Plant volatile vompounds: Sensory cues for health and nutritional value? Science 311:815-819 https://doi.org/10.1126/science.1112614
  24. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189-194 https://doi.org/10.1038/nature07271
  25. Gouinguene SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296-1307 https://doi.org/10.1104/pp.001941
  26. Guterman I, Shalit M, Menda N, Piestun D, Dafny-Yelin M, Shalev G, Bar E, Davydov O, Ovadis M, Emanuel M, Wang J, Adam Z, Pichersky E, Lewinsohn E, Zamir D, Vainstein A, Weiss D (2002) Rose scent: Genomics approach to discovering novel floral fragrance-related genes. Plant Cell 14:2325-2338 https://doi.org/10.1105/tpc.005207
  27. Herde M, Gartner K, Kollner TG, Fode B, Boland W, Gershenzon J, Gatz C, Tholl D (2008) Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile $C_{16}-Homoterpene$ TMTT. Plant Cell 20:1152-1168 https://doi.org/10.1105/tpc.106.049478
  28. Hsiao Y-Y, Tsai W-C, Kuoh C-S, Huang T-H, Wang H-C, Wu T-S, Leu Y-L, Chen W-H, Chen H-H (2006) Comparison of transcripts in Phalaenopsis bellina and Phalaenopsis equestris (Orchidaceae) flowers to deduce monoterpene biosynthesis pathway. BMC Plant Biology 6:14 https://doi.org/10.1186/1471-2229-6-14
  29. Kaminaga Y, Schnepp J, Peel G, Kish CM, Ben-Nissan G, Weiss D, Orlova I, Lavie O, Rhodes D, Wood K, Porterfield DM, Cooper AJL, Schloss JV, Pichersky E, Vainstein A, Dudareva N (2006) Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. Journal of Biological Chemistry 281:23357-23366 https://doi.org/10.1074/jbc.M602708200
  30. Kegge W, Pierik R (2009) Biogenic volatile organic compounds and plant competition. Trends in Plant Science In Press, DOI: 10.1016/j.tplants.2009.11.007
  31. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. The Botanical Review 72:1-120 https://doi.org/10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2
  32. Knudsen JT, Tollsten L, Bergstr LG (1993) Floral scents--a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253-280 https://doi.org/10.1016/0031-9422(93)85502-I
  33. Kollner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The Variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16:1115-1131 https://doi.org/10.1105/tpc.019877
  34. 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 of the United States of America 97:13172-13177 https://doi.org/10.1073/pnas.240454797
  35. Laule O, Furholz A, Chang H-S, 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 of the United States of America 100:6866-6871 https://doi.org/10.1073/pnas.1031755100
  36. 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 https://doi.org/10.1023/A:1026755414773
  37. Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam K-H, Amar O, Lastochkin E, Larkov O, Ravid U, Hiatt W, Gepstein S, Pichersky E (2001) Enhanced levels of the aroma and flavor compound S-Linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol 127:1256-1265 https://doi.org/10.1104/pp.010293
  38. Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. The Plant Journal 30:415-429 https://doi.org/10.1046/j.1365-313X.2002.01297.x
  39. Lu S, Xu R, Jia J-W, Pang J, Matsuda SPT, Chen X-Y (2002) Cloning and functional characterization of a ${\beta}-pinene$ synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiol 130:477-486 https://doi.org/10.1104/pp.006544
  40. Lucker J, Bouwmeester HJ, Schwab W, Blaas J, Plas LHWvd, Verhoeven HA (2001) Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of $S-linalyl-{\beta}-D-glucopyranoside$ The Plant Journal 27:315-324 https://doi.org/10.1046/j.1365-313x.2001.01097.x
  41. Lucker J, Schwab W, van Hautum B, Blaas J, van der Plas LHW, Bouwmeester HJ, Verhoeven HA (2004) Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiol 134:510-519 https://doi.org/10.1104/pp.103.030189
  42. Ma C, Wang H, Lu X, Wang H, Xu G, Liu B (2009) Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry. Metabolomics 5:497-506 https://doi.org/10.1007/s11306-009-0170-6
  43. MacFarlane SA (1999) Molecular biology of the tobraviruses. J Gen Virol 80:2799-2807 https://doi.org/10.1099/0022-1317-80-11-2799
  44. McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7:1015-1026 https://doi.org/10.1105/tpc.7.7.1015
  45. Ministry of Food, Agriculture, Forestry and Fisheries (MIFAFF) (2009). Status of floriculture production in 2008. Rpt. 11-1541000-000017-10, Seoul
  46. Moerkercke AV, Schauvinhold I, Pichersky E, Haring MA, Schuurink RC (2009) A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production. The Plant Journal 60:292-302 https://doi.org/10.1111/j.1365-313X.2009.03953.x
  47. 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 tpc.016766 https://doi.org/10.1105/tpc.016766
  48. Orlova I, Marshall-Colon A, Schnepp J, Wood B, Varbanova M, Fridman E, Blakeslee JJ, Peer WA, Murphy AS, Rhodes D, Pichersky E, Dudareva N (2006) Reduction of benzenoid synthesis in petunia flowers reveals multiple pathways to benzoic acid and enhancement in auxin transport. Plant Cell 18:3458-3475 https://doi.org/10.1105/tpc.106.046227
  49. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 5:237-243 https://doi.org/10.1016/S1369-5266(02)00251-0
  50. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: Nature’s diversity and ingenuity. Science 311:808-811 https://doi.org/10.1126/science.1118510
  51. Ratcliff F, Martin-Hernandez AM, Baulcombe DC (2001) Tobacco rattle virus as a vector for analysis of gene function by silencing. The Plant Journal 25:237-245 https://doi.org/10.1046/j.0960-7412.2000.00942.x
  52. Ribnicky DM, Shulaev V, Raskin I (1998) Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol 118:565-572 https://doi.org/10.1104/pp.118.2.565
  53. Rodriguez-Concepcion M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130:1079-1089 https://doi.org/10.1104/pp.007138
  54. Roeder S, Hartmann A-M, Effmert U, Piechulla B (2007) Regulation of simultaneous synthesis of floral scent terpenoids by the 1,8-cineole synthase of Nicotiana suaveolens. Plant Molecular Biology 65:107-124 https://doi.org/10.1007/s11103-007-9202-7
  55. Rohmer M, Seemann M, Horbach S, Bringer-Meyer S, Sahm H (1996) Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. Journal of the American Chemical Society 118:2564-2566 https://doi.org/10.1021/ja9538344
  56. Sasaki K, Saito T, Lamsa M, Oksman-Caldentey K-M, Suzuki M, Ohyama K, Muranaka T, Ohara K, Yazaki K (2007) Plants utilize isoprene emission as a thermotolerance mechanism. Plant Cell Physiol 48:1254-1262 https://doi.org/10.1093/pcp/pcm104
  57. Spitzer B, Zvi MMB, Ovadis M, Marhevka E, Barkai O, Edelbaum O, Marton I, Masci T, Alon M, Morin S, Rogachev I, Aharoni A, Vainstein A (2007) Reverse genetics of floral scent: Application of tobacco rattle virus-based gene silencing in petunia. Plant Physiol 145:1241-1250 https://doi.org/10.1104/pp.107.105916
  58. Suntornwat O, Koocharoensap S (2005) ${\beta}-glucosidase$ activity and scent production in some flowers. Acta Hort 679:195-199
  59. Tanaka Y, Katsumoto Y, Brugliera F, Mason J (2005) Genetic engineering in floriculture. Plant Cell Tissue and Organ Culture 80:1-24 https://doi.org/10.1007/s11240-004-0739-8
  60. Tholl D, Rose USR (2006) Detection and identification of floral scent compounds. In Biology of floral scents. N. Dudareva and E. Pichersky eds. Boca Raton Fl., CLC Pres, USA
  61. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195-200 https://doi.org/10.1038/nature07272
  62. Vainstein A, Lewinsohn E, Pichersky E, Weiss D (2001) Floral fragrance. New inroads into an old commodity. Plant Physiol 127:1383-1389 https://doi.org/10.1104/pp.010706
  63. van Uffelen RLM, de Groot NSP (2005) Floriculture world wide; production, trade and consumption patterns show market opportunities and challenges. LEI paper 29148:
  64. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612-1624 https://doi.org/10.1105/tpc.104.028837
  65. Watanabe N, Watanabe S, Nakajima R, Moon J-H, Shimokihara K, Inagaki J, Etoh H, Asai T, Sakata K, Ina K (1993) Formation of flower fragrance compounds from their precursors by enzymic action during flower opening. Bioscience, Biotechnology, and Biochemistry 57:1101-1106 https://doi.org/10.1271/bbb.57.1101
  66. 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 Biotech 24:1441-1447 https://doi.org/10.1038/nbt1251
  67. Zuker A, Tzfira T, Ben-Meir H, Ovadis M, Shklarman E, Itzhaki H, Forkmann G, Martens S, Neta-Sharir I, Weiss D, Vainstein A (2002) Modification of flower color and fragrance by antisense suppression of the flavanone 3-hydroxylase gene. Molecular Breeding 9:33-41 https://doi.org/10.1023/A:1019204531262
  68. Zuker A, Tzfira T, Vainstein A (1998) Genetic engineering for cut-flower improvement. Biotechnology Advances 16:33-79 https://doi.org/10.1016/S0734-9750(97)00063-3

Cited by

  1. Production of transgenic cucumber expressing phytoene synthase-2A carotene desaturase gene vol.43, pp.3, 2016, https://doi.org/10.5010/JPB.2016.43.3.341
  2. Study on Growth and Flowering Characteristics in the Spring Sowing for Selection of Rapeseed (Brassica napus L.) Varieties vol.28, pp.1, 2015, https://doi.org/10.7732/kjpr.2015.28.1.111
  3. The use of cotyledonary-node explants in Agrobacterium tumefaciensmediated transformation of cucumber (Cucumis sativus L.) vol.38, pp.3, 2011, https://doi.org/10.5010/JPB.2011.38.3.198