Functional Genomics Reveals That a Compact Terpene Synthase Gene Family Can Account for Terpene Volatile Production in Apple1[W]

• Published in: Plant physiology (Bethesda) Vol. 161; no. 2; pp. 787 - 804
• Main Authors: Nieuwenhuizen, Niels J., Green, Sol A., Chen, Xiuyin, Bailleul, Estelle J.D., Matich, Adam J., Wang, Mindy Y., Atkinson, Ross G.
• Format: Journal Article
• Language: English
• Published: American Society of Plant Biologists 19.12.2012
• Subjects: Genes, Development, and Evolution
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.112.208249

Apple is shown to contain only a small number of functional terpene synthase genes whose evolution appears to have been shaped by genome-wide duplication events and commercial breeding strategies. Terpenes are specialized plant metabolites that act as attractants to pollinators and as defensive compounds against pathogens and herbivores, but they also play an important role in determining the quality of horticultural food products. We show that the genome of cultivated apple ( Malus domestica ) contains 55 putative terpene synthase ( TPS ) genes, of which only 10 are predicted to be functional. This low number of predicted functional TPS genes compared with other plant species was supported by the identification of only eight potentially functional TPS enzymes in apple ‘Royal Gala’ expressed sequence tag databases, including the previously characterized apple ( E,E )-α-farnesene synthase. In planta functional characterization of these TPS enzymes showed that they could account for the majority of terpene volatiles produced in cv Royal Gala, including the sesquiterpenes germacrene-D and ( E )-β-caryophyllene, the monoterpenes linalool and α-pinene, and the homoterpene ( E )-4,8-dimethyl-1,3,7-nonatriene. Relative expression analysis of the TPS genes indicated that floral and vegetative tissues were the primary sites of terpene production in cv Royal Gala. However, production of cv Royal Gala floral-specific terpenes and TPS genes was observed in the fruit of some heritage apple cultivars. Our results suggest that the apple TPS gene family has been shaped by a combination of ancestral and more recent genome-wide duplication events. The relatively small number of functional enzymes suggests that the remaining terpenes produced in floral and vegetative and fruit tissues are maintained under a positive selective pressure, while the small number of terpenes found in the fruit of modern cultivars may be related to commercial breeding strategies.