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Regulation of simultaneous synthesis of floral scent terpenoids by the 1,8-cineole synthase of Nicotiana suaveolens

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Abstract

The white flowers of N. suaveolens emit a complex bouquet of fragrance volatiles. The dominant compounds are benzenoids (e.g. methyl benzoate, methyl salicylate, benzyl benzoate and benzyl salicylate), monoterpenes (1,8-cineole, limonene, sabinene, E-β-ocimene, β-β-myrcene, α- and β-pinene and α-terpineole) and sesquiterpenes (e.g. caryophyllene), which are all emitted at higher levels during the night. Here, we show that the simultaneous nocturnal emission of most monoterpenes is realized by a single floral-specific multi-product enzyme (1,8-cineole synthase, CIN), which synthesizes the monoterpenes of the “cineole cassette”. Interestingly, N. suaveolens is the only known taxon of the Suaveolentes section to have a flower emitting “cineole cassette of monoterpenes” which is otherwise typical for the Alatae section. Gene sequence analysis of CIN has revealed the highest similarities to other angiosperm monoterpene synthases from Vitis vinifera, Quercus ilex, Citrus unshiu and C. limon, which cluster in the same branch of the terpene synthase B subfamily. However, based on its synthesized products, N. suaveolens CIN shares similarity with enzymes of the Arabidopsis thaliana root and Salvia officinalis leaf. The N. suaveolens CIN gene is only expressed in the stigma/style tissue and petals. Thin sections of petals present the enzyme primarily in the adaxial and abaxial epidermis; this facilitates the comprehensive emission of volatiles in all spacial directions. The oscillation of monoterpene emission is a consequence of the regulation of the CIN gene by the circadian clock, with oscillations occurring at the level of transcript and protein accumulations and of enzyme activity. Light/dark or dark/light transition signals synchronize the slow-running endogenous clock. Two strategies for synchronized scent emission have been established in N. suaveolens flowers: (i) the synthesis of volatile organic compounds by a multi-product enzyme and (ii) the coordination of biosynthetic pathways by a circadian clock.

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Abbreviations

LIS:

Linalool synthase

CIN:

Cineole synthase

GPP:

Geranyl pyrophosphate

VOCs:

Volatile organic compounds

LL:

Continuous illumination

DD:

Continuous darkness

LD :

Light/dark regime

SPME:

Solid phase micro extraction

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Acknowledgements

The authors thank Rita Heese (University of Rostock) for her technical assistance, Diana Rohrbeck for her help with in situ hybridizations and Sandra Saschenbrecker for many RNA samples. We also thank Natalia Dudareva (University Purdue, Indiana, USA) and Eran Pichersky (University Ann Arbor, Michigan, USA) for their initial help in clone isolation and enzyme characterization. This project was financially supported by the DFG to BP.

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  1. Susanna Roeder

    Present address: Department of Molecular, Cellular and Developmental Biology, University of Michigan, 830 N. University Street, Ann Arbor, MI, 48109-1048, USA

Authors and Affiliations

  1. Institute of Biological Sciences, University of Rostock, Albert-Einstein-Str. 3, Rostock, 18059, Germany

    Susanna Roeder, Anna-Maria Hartmann, Uta Effmert & Birgit Piechulla

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  1. Susanna Roeder
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  2. Anna-Maria Hartmann
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Correspondence to Birgit Piechulla.

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Roeder, S., Hartmann, AM., Effmert, U. et al. Regulation of simultaneous synthesis of floral scent terpenoids by the 1,8-cineole synthase of Nicotiana suaveolens . Plant Mol Biol 65, 107–124 (2007). https://doi.org/10.1007/s11103-007-9202-7

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