Scent evolution in Chinese roses

  1. Gabriel Scalliet†,‡,
  2. Florence Piola§,
  3. Christophe J. Douady§,
  4. Stéphane Réty,
  5. Olivier Raymond†,
  6. Sylvie Baudino‖,
  7. Karim Bordji†,††,
  8. Mohammed Bendahmane†,
  9. Christian Dumas†,
  10. J. Mark Cock†,‡‡, and
  11. Philippe Hugueney†,§§,¶¶
  1. †Laboratoire Reproduction et Développement des Plantes, Institut Fédératif de Recherche 128, Unité Mixte de Recherche 5667, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Université Lyon 1, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon Cedex 07, France;
  2. §Laboratoire d'Ecologie des Hydrosystèmes Fluviaux, Unité Mixte de Recherche 5023, Centre National de la Recherche Scientifique, Université Lyon 1, 43 Boulevard du 11 Novembre 1918, 69622 Villeurbanne Cedex, France;
  3. Laboratoire de Cristallographie et RMN Biologique, Unité Mixte de Recherche 8015, Centre National de la Recherche Scientifique-Faculté de Pharmacie, 4 Avenue de l'Observatoire, case 48, 75270 Paris Cedex 06, France; and
  4. ‖Laboratoire de Biotechnologies Végétales Appliquées aux Plantes Aromatiques et Médicinales, EA3061, Université Jean Monnet, 23 Rue du Dr. Michelon, 42023 Saint-Etienne Cedex 2, France

  1. Edited by Eran Pichersky, University of Michigan, Ann Arbor, MI, and accepted by the Editorial Board March 2, 2008 (received for review December 7, 2007)

Abstract

The phenolic methyl ether 3,5-dimethoxytoluene (DMT) is a major scent compound of many modern rose varieties, and its fragrance participates in the characteristic “tea scent” that gave their name to Tea and Hybrid Tea roses. Among wild roses, phenolic methyl ether (PME) biosynthesis is restricted to Chinese rose species, but the progenitors of modern roses included both European and Chinese species (e.g., Rosa chinensis cv Old Blush), so this trait was transmitted to their hybrid progeny. The last steps of the biosynthetic pathways leading to DMT involve two methylation reactions catalyzed by the highly similar orcinol O-methyltransferases (OOMT) 1 and 2. OOMT1 and OOMT2 enzymes exhibit different substrate specificities that are consistent with their operating sequentially in DMT biosynthesis. Here, we show that these different substrate specificities are mostly due to a single amino acid polymorphism in the phenolic substrate binding site of OOMTs. An analysis of the OOMT gene family in 18 species representing the diversity of the genus Rosa indicated that only Chinese roses possess both the OOMT2 and the OOMT1 genes. In addition, we provide evidence that the Chinese-rose-specific OOMT1 genes most probably evolved from an OOMT2-like gene that has homologues in the genomes of all extant roses. We propose that the emergence of the OOMT1 gene may have been a critical step in the evolution of scent production in Chinese roses.

Footnotes

  • ¶¶To whom correspondence should be addressed. E-mail: philippe.hugueney{at}ens-lyon.fr

  • Author contributions: G.S. and F.P. contributed equally to this work; G.S., F.P., C.J.D., S.R., O.R., S.B., C.D., J.M.C., and P.H. designed research; G.S., F.P., C.J.D., S.R., O.R., S.B., K.B., M.B., and P.H. performed research; G.S., F.P., C.J.D., S.R., O.R., S.B., K.B., M.B., and P.H. analyzed data; and G.S., F.P., C.J.D., J.M.C., and P.H. wrote the paper.

  • ↵ ‡Present address: Syngenta Crop Protection Münschwillen AG, WST-540.2.51 Schaffhauserstrasse CH-4332 Stein, Switzerland.

  • ↵ ††Present address: GIP Cyceron, Unité Mixte de Recherche, Centre National de la Recherche Scientifique 6185, Boulevard Becquerel, BP 5229 14074 Caen Cedex, France.

  • ↵ ‡‡Present address: Unité Mixte de Recherche 7139, Station Biologique, Centre National de la Recherche Scientifique, Université Pierre & Marie Curie Paris VI, Place Georges Teissier, BP74 29682 Roscoff Cedex, France.

  • ↵ §§Present address: Laboratoire de Génétique et d'Amélioration de la Vigne, Unité Mixte de Recherche 1131, Institut National de la Recherche Agronomique, Université Louis Pasteur Strasbourg, 28 Rue de Herrlisheim BP 20507, 68021 Colmar Cedex, France.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. E.P. is a guest editor invited by the Editorial Board.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank/EMBL databases (accession nos. AM182763–AM182856).

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0711551105/DCSupplemental.

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  1. Published online before print April 14, 2008, doi: 10.1073/pnas.0711551105 PNAS April 15, 2008 vol. 105 no. 15 5927-5932
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