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Diurnal regulation of scent emission in rose flowers

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Abstract

Previous studies have shown diurnal oscillation of scent emission in rose flowers with a peak during the day (Helsper in Planta 207:88–95, 1998; Picone in Planta 219:468–478, 2004). Here, we studied the regulation of scent production and emission in Rosa hybrida cv. Fragrant Cloud during the daily cycle and focused on two terpenoid compounds, germacrene D and geranyl acetate, whose biosynthetic genes have been characterized by us previously. The emission of geranyl acetate oscillated during the daily light/dark cycle with a peak early in the light period. A similar daily fluctuation was found in the endogenous level of this compound and in the expression of its biosynthetic gene, alcohol acetyl transferase (RhAAT). The rhythmic expression of RhAAT continued under conditions of constant light or darkness, indicating regulation by the endogenous circadian clock. However, the accumulation and emission of geranyl acetate ceased under continuous light. Our results suggest that geranyl acetate production is limited by the level of its substrate geraniol, which is suppressed under constant light conditions. The emission of germacrene D also oscillated during the daily cycle with a peak early in the light period. However, the endogenous level of this compound and the expression of its biosynthetic gene germacrene D synthase (RhGDS) were constant throughout the day. The diurnal oscillation of germacrene D emission ceased under continuous light, suggesting direct regulation by light. Our results demonstrate the complexity of the diurnal regulation of scent emission: although the daily emission of most scent compounds is synchronized, various independently evolved mechanisms control the production, accumulation and release of different volatiles.

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Abbreviations

2-PE:

2-Phenylethanol

2-PEG:

Glycosylated 2-PE;

BAMT:

Benzoic acid carboxyl methyltransferase

RhAAT:

Rosa hybrida alcohol acetyl transferase

RhGDS:

Rosa hybrida germacrene D synthase

SAMT:

S-Adenosyl-l-Met:salicylic acid carboxyl methyltransferase

References

  • Croteau R, Karp F (1991) Origin of natural odorants. In: Muller P, Lamparsky D (eds) Perfume: art, science and technology. Elsevier Applied Sciences, New York, pp 101–126

    Google Scholar 

  • Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1250–1318

    Google Scholar 

  • Dobson HEM, Bergstrom G, Groth I (1990) Differences in fragrance chemistry between flower parts of Rosa rugosa Thunb. (Rosaceae). Isr J Bot 39:143–156

    CAS  Google Scholar 

  • Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–633

    Article  PubMed  CAS  Google Scholar 

  • Dudareva N, Negre F (2005) Practical applications of research into the regulation of plant volatile emission. Curr Opin Plant Biol 8:113–118

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Faldt J, Miller B, Bohlmann J (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 15:1227–1241

    Article  PubMed  CAS  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  PubMed  CAS  Google Scholar 

  • Guterman I, Shalit M, Menda N, Piestun D, Dafny-Yelin M, Shalev G, Davydov O, Ovadis M, Emanuel M, Wang J, Adam Z, Pichersky E, Lewinsohn E, Zamir D, Vainstein A, Weiss D (2002) Rose scent: genomic approach to discover novel floral fragrance-related genes. Plant Cell 14:2325–2338

    Article  PubMed  CAS  Google Scholar 

  • Helsper JPFG, 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

    Article  CAS  Google Scholar 

  • Hoballah ME, Stuurman J, Turlings TCJ, Guerin PM, Connetable S, Kuhlemeier C (2005) The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta. Planta 222:141–150

    Article  PubMed  CAS  Google Scholar 

  • Jakobsen HB, Olsen CE (1994) Influence of climactic factors on emission of flower volatiles in situ. Planta 192:365–371

    CAS  Google Scholar 

  • Jetter R (2006) Examination of processes involved in the emission of scent volatioles. In: Dudareva N, Pichersky ER (eds) Biology of floral scent. CRC, Boca Raton, pp 125–144

    Google Scholar 

  • Jones MB, Mansfield TA (1975) Circadian rhythms in plants. Sci Prog Oxford 62:103–125

    CAS  Google Scholar 

  • Knudsen JT, Tollesten L, Bergstrom GL (1993) Floral scent—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:252–280

    Article  Google Scholar 

  • Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lavid N, Wang J, Shalit M, Gutterman 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

    Article  PubMed  CAS  Google Scholar 

  • Loughrin JH, Hamilton-Kemp TR, Andersen RA, Hildebrand DF (1991) Circadian rhythm of volatile emission from flower of Nicotiana sylvestris and N. suaveolens. Physiol Plant 83:492–496

    Article  CAS  Google Scholar 

  • Pham-Delegue MH, Etievant P, Guichard E, Marilleau R, Douault P, Chauffaille J, Masson C (1990) Chemicals involved in honeybee-sunflower relationship. J Chem Ecol 16:3053–3065

    Article  CAS  Google Scholar 

  • Picone MJ, 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

    Article  PubMed  CAS  Google Scholar 

  • Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol 25:159–184

    PubMed  CAS  Google Scholar 

  • Pott MB, Effmert U, Piechulla B (2003) Transcriptional and post-translational regulation of S-adenosyl-l-methionine: salicylic acid carboxyl methyltransferase (SAMT) during Stephanotis floribunda flower development. J Plant Physiol 160:635–643

    Article  PubMed  CAS  Google Scholar 

  • Raguso RA, Pichersky E (1995) Floral volatiles from Clarkia breweri and Clarkia concinna (Onagraceae): recent evolution of floral scent and moth pollination. Plant Syst Evol 194:55–67

    Article  CAS  Google Scholar 

  • Raguso RA, Light DM, Pichersky E (1996) Electroantennogram responses of Hyles lineata (Sphingidae: Lepidoptera) to volatile compounds from Clarkia breweri (Onagraceae) and other moth-pollinated flowers. J Chem Ecol 22:1735–1766

    Article  CAS  Google Scholar 

  • Schuurink RC, Haring MA, Clark DG (2006) Regulation of volatile benzenoid biosynthesis in petunia flowers. Trends Plant Sci 11:20–25

    Article  PubMed  CAS  Google Scholar 

  • Shalit M, Guterman I, Volpin H, Bar E, Tamari T, Menda N, Adam Z, Zamir D, Vainstein A, Weiss D, Pichersky E, Lewinsohn E (2003) Volatile ester formation in roses: identification of an acetyl-CoA:geraniol acetyltransferase in developing rose petals. Plant Physiol 131:1868–1876

    Article  PubMed  CAS  Google Scholar 

  • 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 honey bees. Isr J Plant Sci 52:245–255

    Article  CAS  Google Scholar 

  • Simkin AJ, Underwood BA, Auldridge M, Loucas HM, Shibuya K, Schmelz E, Clark DG, Klee HJ (2004) Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of beta-ionone, a fragrance volatile of petunia. Plant Physiol 136:3504–3514

    Article  PubMed  CAS  Google Scholar 

  • 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 Physiol 138:255–266

    Article  PubMed  CAS  Google Scholar 

  • Vainstein A, Lewinsohn E, Pichersky E, Weiss D (2001) Floral fragrance. New inroads into an old commodity. Plant Physiol 127:1383–1389

    Article  PubMed  CAS  Google Scholar 

  • Weiss EA (1997) Essential oil crops. CAB International, Wallingford Oxon, p 411

    Google Scholar 

Download references

Acknowledgments

This work was supported by the US Israel Binational Agriculture Research and Development fund (grant no. US-3437) and by the Pearlstein Fund for research in floriculture at the Hebrew University. We thank the donors for their help.

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Correspondence to David Weiss.

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Hendel-Rahmanim, K., Masci, T., Vainstein, A. et al. Diurnal regulation of scent emission in rose flowers. Planta 226, 1491–1499 (2007). https://doi.org/10.1007/s00425-007-0582-3

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