Identification of rose phenylacetaldehyde synthase by functional complementation in yeast

Plant Molecular Biology

Volumn 72, Issue 3, 2010, Pages 235-245

  Farhi, Moran ^a   Lavie, Orly ^a   Masci, Tania ^a   Hendel Rahmanim, Keren ^a   Weiss, David ^a   Abeliovich, Hagai ^a   Vainstein, Alexander ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

2 Phenylacetaldehyde; 2 Phenylethylalchohol; ARO10 floral scent; Rose; Volatiles

Indexed keywords

ACETALDEHYDE; DRUG DERIVATIVE; ESSENTIAL OIL; MESSENGER RNA; PHENETHYL ALCOHOL; PHENYLACETALDEHYDE; VEGETABLE PROTEIN;

ARTICLE; CIRCADIAN RHYTHM; ENZYMOLOGY; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; ODOR; PHYSIOLOGY; ROSE; SACCHAROMYCES CEREVISIAE;

ACETALDEHYDE; CIRCADIAN RHYTHM; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; ODORS; OILS, VOLATILE; PHENYLETHYL ALCOHOL; PLANT PROTEINS; RNA, MESSENGER; ROSA; SACCHAROMYCES CEREVISIAE;

PETUNIA; ROSA HYBRID CULTIVAR; SACCHAROMYCES CEREVISIAE;

EID: 75949102627     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-009-9564-0     Document Type: Article

References (53)

1. 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 Physiol 135: 1865-1878. doi: 10. 1104/pp. 104. 042580.
2. 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 Physiol 135: 1993-2011. doi: 10. 1104/pp. 104. 045468.
3. Brunke EJ, Hammerschmidt FJ, Schmaus G (1992) Scent of roses recent results. Flavour Frag J 7: 195-198.
4. Channlière 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 Lett 515: 35-38.
5. Chen H, Fink GR (2006) Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20: 1150-1161. doi: 10. 1101/gad. 1411806.
6. Clark GS (1990) Phenethyl alcohol. Perfumer Flavor 15: 37-44.
7. Cseke LJ, Kaufman PB, Kirakosyan A (2007) The biology of essential oils in the pollination of flowers. Nat Prod Commun 2: 1317-1336.
8. Dobres MS (2008) Barriers to genetically engineered ornamentals: an industry perspective. In: da-Silva JAT (ed) Floriculture, ornamental and plant biotechnology. Global Science Books, UK, pp 1-115.
9. Dudareva N, Pichersky E (2006) Biology of floral scent. CRC Press-Taylor & Francis Group, Boca Raton.
10. 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. doi: 10. 1105/tpc. 12. 6. 949.
11. Etschmann MMW, Schrader J (2006) An aqueous-organic two-phase bioprocess for efficient production of the natural aroma chemicals 2-phenylethanol and 2-phenylethylacetate with yeast. Appl Microbiol Biotechnol 71: 440-443. doi: 10. 1007/s00253-005-0281-6.
12. Farhi M, Dudareva N, Masci T, Weiss D, Vainstein A, Abeliovich H (2006) Synthesis of the food flavoring methyl benzoate by genetically engineered Saccharomyces cerevisiae. J Biotechnol 122: 307-315. doi: 10. 1016/j. jbiotec. 2005. 12. 007.
13. Flament I, Debonneville C, Furrer A (1993) Volatile constituents of roses-characterization of cultivars based on the headspace analysis of living flower emissions. Bioactive Volatile Compd Plants 525: 269-281.
14. Fridman E, Pichersky E (2005) Metabolomics, genomics, proteomics, and the identification of enzymes and their substrates and products. Curr Opin Plant Biol 8: 242-248. doi: 10. 1016/j. pbi. 2005. 03. 004.
15. Gao F, Daugulis AJ (2009) Bioproduction of the aroma compound 2-phenylethanol in a solid-liquid two-phase partitioning bioreactor system by Kluyveromyces marxianus. Biotechnol Bioeng 104: 332-339. doi: 10. 1002/bit. 22387.
16. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Guide to yeast genetics and molecular and cell biology. Methods Enzymol 350: 87-96.
17. 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. doi: 10. 1105/tpc. 005207.
18. Hayashi S, Yagi K, Ishikawa T, Kawasaki M, Asai T, Picone J, Turnbull C, Hiratake J, Sakata K, Takada M, Ogawa K, Watanabe N (2004) Emission of 2-phenylethanol from its β-D-glucopyranoside and the biogenesis of these compounds from [H-2(8)] l-phenylalanine in rose flowers. Tetrahedron 60: 7005-7013. doi: 10. 1016/j. tet. 2003. 10. 130.
19. Hazelwood LA, Daran J-M, van Maris AJA, Pronk JT, Dickinson JR (2008) The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74: 2259-2266. doi: 10. 1128/aem. 02625-07.
20. Helsper J, 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: 88-95.
21. Hendel-Rahmanim K, Masci T, Vainstein A, Weiss D (2007) Diurnal regulation of scent emission in rose flowers. Planta 226: 1491-1499. doi: 10. 1007/s00425-007-0582-3.
22. 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. J Biol Chem 281: 23357-23366. doi: 10. 1074/jbc. M602708200.
23. Knudsen JT, Tollsten L, Bergstrom LG (1993) Floral scents-a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33: 253-280.
24. 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. doi: 10. 1105/tpc. 13. 10. 2333.
25. Lavid N, Wang J, Shalit M, Guterman I, Bar E, Beuerle T, Menda N, Shafir S, Zamir D, Adam Z, Vainstein A, Weiss D, Pichersky E, Lewinsohn E (2002) O-Methyltransferases involved in the biosynthesis of volatile phenolic derivatives in rose petals. Plant Physiol 129: 1899-1907. doi: 10. 1104/pp. 005330.
26. Lavie O (2006) Identification and characterization of genes involved in the biosynthesis of scent volatile phenylacetaldehyde. M. Sc., Thesis, The Hebrew University of Jerusalem.
27. Leclercq-Perlat MN, Corrieu G, Spinnler HE (2004) Comparison of volatile compounds produced in model cheese medium deacidified by Debaryomyces hansenii or Kluyveromyces marxianus. J Dairy Sci 87: 1545-1550.
28. Moyal Ben Zvi M, 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 Biotechnol J 6: 403-415. doi: 10. 1111/j. 1467-7652. 2008. 00329. x.
29. Pichersky E, Dudareva N (2007) Scent engineering: toward the goal of controlling how flowers smell. Trends Biotechnol 25: 105-110.
30. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature's diversity and ingenuity. Science 311: 808-811. doi: 10. 1126/science. 1118510.
31. Picone JM, Clery RA, Watanabe N, MacTavish HS, Turnbull CGN (2004) Rhythmic emission of floral volatiles from Rosa damascena semperflorens cv. 'Quatre Saisons'. Planta 219: 468-478.
32. Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press, NY, pp 159-184.
33. Rose USR, Tumlinson JH (2005) Systemic induction of volatile release in cotton: how specific is the signal to herbivory? Planta 222: 327-335. doi: 10. 1007/s00425-005-1528-2.
34. Rose M, Kotter P, Hauf J, Entian KD (2003) The yeast strain collection EUROSCARF: a source for useful tools in yeast genetics and molecular biology. Yeast 20: S343.
35. Sakai M, Hirata H, Sayama H, Sekiguchi K, Itano H, Asai T, Dohra H, Hara M, Watanabe N (2007) Production of 2-phenylethanol in roses as the dominant floral scent compound from l-phenylalanine by two key enzymes, a PLP-dependent decarboxylase and a phenylacetaldehyde reductase. Biosci Biotechnol Biochem 71: 2408-2419.
36. Sakai M, Tomita S, Hirata H, Asai T, Dohra H, Hara M, Watanabe N (2008) Purification and characterization of β-glucosidase involved in the emission of 2-phenylethanol from rose flowers. Biosci Biotechnol Biochem 72: 219-221.
37. Scalliet G, Journot N, Jullien F, Baudino S, Magnard JL, Channeliere S, Vergne P, Dumas C, Bendahmane M, Cock JM, Hugueney P (2002) Biosynthesis of the major scent components 3, 5-dimethoxytoluene and 1, 3, 5-trimethoxybenzene by novel rose O-methyltransferases. FEBS Lett 523: 113-118.
38. Scalliet G, Piola F, Douady CJ, Rety S, Raymond O, Baudino S, Bordji K, Bendahmane M, Dumas C, Cock JM, Hugueney P (2008) Scent evolution in Chinese roses. Proc Natl Acad Sci USA 105: 5927-5932. doi: 10. 1073/pnas. 0711551105.
39. Schiestl FP, Ayasse M, Paulus HF, Lofstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399: 421-422.
40. Schuurink RC, Haring MA, Clark DG (2006) Regulation of volatile benzenoid biosynthesis in petunia flowers. Trends Plant Sci 11: 20-25.
41. Shalit M, Shafir S, Larkov O, Bar E, Kaslassi D, Adam Z, Zamir D, Vainstein A, Weiss D, Ravid U, Lewinsohn E (2004) Volatile compounds emitted by rose cultivars: fragrance perception by man and honeybees. Israel J Plant Sci 52: 245-255.
42. Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot 101: 5-18. doi: 10. 1093/aob/mcm240.
43. 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. doi: 10. 1104/pp. 107. 105916.
44. Takahashi S, Yeo Y, Greenhagen BT, McMullin T, Song L, Maurina-Brunker J, Rosson R, Noel JP, Chappell J (2007) Metabolic engineering of sesquiterpene metabolism in yeast. Biotechnol Bioeng 97: 170-181. doi: 10. 1002/bit. 21216.
45. Tieman D, Taylor M, 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. Proc Natl Acad Sci USA 103: 8287-8292. doi: 10. 1073/pnas. 0602469103.
46. 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. doi: 10. 1016/j. phytochem. 2007. 06. 005.
47. Vainstein A, Lewinsohn E, Weiss D (2006) An integrated genomics approach to identifying floral scent genes in rose. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press-Taylor & Francis Group, Boca Raton, pp 91-102.
48. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17: 1612-1624. doi: 10. 1105/tpc. 104. 028837.
49. Vuralhan Z, Morais MA, Tai S-L, Piper MDW, Pronk JT (2003) Identification and characterization of phenylpyruvate decarboxylase genes in Saccharomyces cerevisiae. Appl Environ Microbiol 69: 4534-4541. doi: 10. 1128/aem. 69. 8. 4534-4541. 2003.
50. Watanabe S, Hayashi K, Yagi K, Asai T, Mactavish H, Picone J, Turnbull C, Watanabe N (2002) Biogenesis of 2-phenylethanol in rose flowers: incorporation of [2H8]l-phenylalanine into 2-phenylethanol and its β-D-glucopyranoside during the flower opening of Rosa 'Hoh-Jun' and Rosa damascena Mill. Biosci Biotechnol Biochem 66: 943-947.
51. Westermann B, Neupert W (2000) Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16: 1421-1427.
52. Yang Z, Sakai M, Sayama H, Shimeno T, Yamaguchi K, Watanabe N (2009) Elucidation of the biochemical pathway of 2-phenylethanol from shikimic acid using isolated protoplasts of rose flowers. J Plant Physiol 166: 887-891.
53. Yitzhak E (2004) Genomic approach to studying rose floral scent. M. Sc., thesis, The Hebrew University of Jerusalem.