This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (41) Citing Articles via Google Scholar Google Scholar Articles by Aharoni, A. Articles by Bouwmeester, H. J. Search for Related Content PubMed PubMed Citation Articles by Aharoni, A. Articles by Bouwmeester, H. J. Agricola Articles by Aharoni, A. Articles by Bouwmeester, H. J.

Gain and Loss of Fruit Flavor Compounds Produced by Wild and Cultivated Strawberry Species

^a Plant Research International, 6700 AA, Wageningen, The Netherlands
^b Plant Molecular Biology Unit, Division of Biochemical Sciences, National Chemical Laboratory, Pune 411 008, India
^c Lehrstuhl für Lebensmittelchemie, Universität Würzburg, Am Hubland, 97074 Würzburg, Germany

¹ To whom correspondence should be addressed. E-mail asaph.aharoni{at}weizmann.ac.il; fax 972-8-9344181.

The blends of flavor compounds produced by fruits serve as biological perfumes used to attract living creatures, including humans. They include hundreds of metabolites and vary in their characteristic fruit flavor composition. The molecular mechanisms by which fruit flavor and aroma compounds are gained and lost during evolution and domestication are largely unknown. Here, we report on processes that may have been responsible for the evolution of diversity in strawberry (Fragaria spp) fruit flavor components. Whereas the terpenoid profile of cultivated strawberry species is dominated by the monoterpene linalool and the sesquiterpene nerolidol, fruit of wild strawberry species emit mainly olefinic monoterpenes and myrtenyl acetate, which are not found in the cultivated species. We used cDNA microarray analysis to identify the F. ananassa Nerolidol Synthase1 (FaNES1) gene in cultivated strawberry and showed that the recombinant FaNES1 enzyme produced in Escherichia coli cells is capable of generating both linalool and nerolidol when supplied with geranyl diphosphate (GPP) or farnesyl diphosphate (FPP), respectively. Characterization of additional genes that are very similar to FaNES1 from both the wild and cultivated strawberry species (FaNES2 and F. vesca NES1) showed that only FaNES1 is exclusively present and highly expressed in the fruit of cultivated (octaploid) varieties. It encodes a protein truncated at its N terminus. Green fluorescent protein localization experiments suggest that a change in subcellular localization led to the FaNES1 enzyme encountering both GPP and FPP, allowing it to produce linalool and nerolidol. Conversely, an insertional mutation affected the expression of a terpene synthase gene that differs from that in the cultivated species (termed F. ananassa Pinene Synthase). It encodes an enzyme capable of catalyzing the biosynthesis of the typical wild species monoterpenes, such as -pinene and ß-myrcene, and caused the loss of these compounds in the cultivated strawberries. The loss of -pinene also further influenced the fruit flavor profile because it was no longer available as a substrate for the production of the downstream compounds myrtenol and myrtenyl acetate. This phenomenon was demonstrated by cloning and characterizing a cytochrome P450 gene (Pinene Hydroxylase) that encodes the enzyme catalyzing the C10 hydroxylation of -pinene to myrtenol. The findings shed light on the molecular evolutionary mechanisms resulting in different flavor profiles that are eventually selected for in domesticated species.

This article has been cited by other articles:

				A. Fait, K. Hanhineva, R. Beleggia, N. Dai, I. Rogachev, V. J. Nikiforova, A. R. Fernie, and A. Aharoni Reconfiguration of the Achene and Receptacle Metabolic Networks during Strawberry Fruit Development Plant Physiology, October 1, 2008; 148(2): 730 - 750. [Abstract] [Full Text] [PDF]

				V. Shulaev, S. S. Korban, B. Sosinski, A. G. Abbott, H. S. Aldwinckle, K. M. Folta, A. Iezzoni, D. Main, P. Arus, A. M. Dandekar, et al. Multiple Models for Rosaceae Genomics Plant Physiology, July 1, 2008; 147(3): 985 - 1003. [Abstract] [Full Text] [PDF]

				M. Herde, K. Gartner, T. G. Kollner, B. Fode, W. Boland, J. Gershenzon, C. Gatz, and D. Tholl Identification and Regulation of TPS04/GES, an Arabidopsis Geranyllinalool Synthase Catalyzing the First Step in the Formation of the Insect-Induced Volatile C16-Homoterpene TMTT PLANT CELL, April 1, 2008; 20(4): 1152 - 1168. [Abstract] [Full Text] [PDF]

				C. Lin, B. Shen, Z. Xu, T. G. Kollner, J. Degenhardt, and H. K. Dooner Characterization of the Monoterpene Synthase Gene tps26, the Ortholog of a Gene Induced by Insect Herbivory in Maize Plant Physiology, March 1, 2008; 146(3): 940 - 951. [Abstract] [Full Text] [PDF]

				S. Bocobza, A. Adato, T. Mandel, M. Shapira, E. Nudler, and A. Aharoni Riboswitch-dependent gene regulation and its evolution in the plant kingdom Genes & Dev., November 15, 2007; 21(22): 2874 - 2879. [Abstract] [Full Text] [PDF]

				S. C. Kampranis, D. Ioannidis, A. Purvis, W. Mahrez, E. Ninga, N. A. Katerelos, S. Anssour, J. M. Dunwell, J. Degenhardt, A. M. Makris, et al. Rational Conversion of Substrate and Product Specificity in a Salvia Monoterpene Synthase: Structural Insights into the Evolution of Terpene Synthase Function PLANT CELL, June 1, 2007; 19(6): 1994 - 2005. [Abstract] [Full Text] [PDF]

				C. Stewart Jr, M. Mazourek, G. M. Stellari, M. O'Connell, and M. Jahn Genetic control of pungency in C. chinense via the Pun1 locus J. Exp. Bot., March 5, 2007; (2007) erl243v1. [Abstract] [Full Text] [PDF]

				I. Hernandez, D. Molenaar, J. Beekwilder, H. Bouwmeester, and J. E. T. van Hylckama Vlieg Expression of Plant Flavor Genes in Lactococcus lactis Appl. Envir. Microbiol., March 1, 2007; 73(5): 1544 - 1552. [Abstract] [Full Text] [PDF]

				S. Lunkenbein, E. M. J. Salentijn, H. A. Coiner, M. J. Boone, F. A. Krens, and W. Schwab Up- and down-regulation of Fragariaxananassa O-methyltransferase: impacts on furanone and phenylpropanoid metabolism J. Exp. Bot., July 1, 2006; 57(10): 2445 - 2453. [Abstract] [Full Text] [PDF]

				T. Raab, J. A. Lopez-Raez, D. Klein, J. L. Caballero, E. Moyano, W. Schwab, and J. Munoz-Blanco FaQR, Required for the Biosynthesis of the Strawberry Flavor Compound 4-Hydroxy-2,5-Dimethyl-3(2H)-Furanone, Encodes an Enone Oxidoreductase PLANT CELL, April 1, 2006; 18(4): 1023 - 1037. [Abstract] [Full Text] [PDF]

				D. M. Tieman, M. Zeigler, E. A. Schmelz, M. G. Taylor, P. Bliss, M. Kirst, and H. J. Klee Identification of loci affecting flavour volatile emissions in tomato fruits J. Exp. Bot., March 1, 2006; 57(4): 887 - 896. [Abstract] [Full Text] [PDF]

				S. A. Goff and H. J. Klee Plant Volatile Compounds: Sensory Cues for Health and Nutritional Value? Science, February 10, 2006; 311(5762): 815 - 819. [Abstract] [Full Text] [PDF]

				I. F. Kappers, A. Aharoni, T. W. J. M. van Herpen, L. L. P. Luckerhoff, M. Dicke, and H. J. Bouwmeester Genetic Engineering of Terpenoid Metabolism Attracts Bodyguards to Arabidopsis Science, September 23, 2005; 309(5743): 2070 - 2072. [Abstract] [Full Text] [PDF]