Strawberry sweetness and consumer preference are enhanced by specific volatile compounds

Fan et al. Horticulture Research (2021)8:66 https://doi.org/10.1038/s41438-021-00502-5 ARTICLE Horticulture Research www.nature.com/hortres Open Access Strawberry sweetness and consumer preference are enhanced by specific volatile compounds 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Zhen Fan1, Tomas Hasing2, Timothy S. Johnson 3, Drake M. Garner3, Michael L. Schwieterman4, Christopher R. Barbey 1, Thomas A. Colquhoun3, Charles A. Sims5, Marcio F. R. Resende 6 and Vance M. Whitaker1 Abstract Breeding crops for improved flavor is challenging due to the high cost of sensory evaluation and the difficulty of connecting sensory experience to chemical composition. The main goal of this study was to identify the chemical drivers of sweetness and consumer liking for fresh strawberries (Fragaria × ananassa). Fruit of 148 strawberry samples from cultivars and breeding selections were grown and harvested over seven years and were subjected to both sensory and chemical analyses. Each panel consisted of at least 100 consumers, resulting in more than 15,000 sensory data points per descriptor. Three sugars, two acids and 113 volatile compounds were quantified. Consumer liking was highly associated with sweetness intensity, texture liking, and flavor intensity, but not sourness intensity. Partial least square analyses revealed 20 volatile compounds that increased sweetness perception independently of sugars; 18 volatiles that increased liking independently of sugars; and 15 volatile compounds that had positive effects on both. Machine learning-based predictive models including sugars, acids, and volatiles explained at least 25% more variation in sweetness and liking than models accounting for sugars and acids only. Volatile compounds such as γdodecalactone; 5-hepten-2-one, 6-methyl; and multiple medium-chain fatty acid esters may serve as targets for breeding or quality control attributes for strawberry products. A genetic association study identified two loci controlling ester production, both on linkage group 6 A. Co-segregating makers in these regions can be used for increasing multiple esters simultaneously. This study demonstrates a paradigm for improvement of fruit sweetness and flavor in which consumers drive the identification of the most important chemical targets, which in turn drives the discovery of genetic targets for marker-assisted breeding. Introduction The cultivated strawberry (Fragaria ×ananassa) is one of the most widely grown fruit crops in the world due to its sweet and aromatic flavor and health-associated compounds including anthocyanins, antioxidants, fiber and ellagic acid1. Breeding for flavor in strawberry has been challenging due to the chemical complexity of the trait and the variability of the production environment. Targeted selection of flavor-associated chemicals in strawberry has thus far been restricted to increasing sugar Correspondence: Vance M. Whitaker (vwhitaker@ufl.edu) 1 Horticultural Sciences Department, University of Florida, IFAS Gulf Coast Research and Education Center, Wimauma, FL, USA 2 Elo Life Systems, Durham, NC, USA Full list of author information is available at the end of the article content. In spite of improvements in eating quality over time, most strawberries on the market still do not meet consumer expectations of sweetness and flavor2. Efforts at flavor improvement must be reinforced by investigating the relationships between fruit chemical diversity and consumer preference. During strawberry fruit ripening, changing auxin levels drive the accumulation of sugars and their derivatives, as well as secondary metabolites3,4. Sucrose, glucose, and fructose comprise the major soluble sugars in strawberry and are rapidly translocated from photosynthesizing organs to fruit, in synchrony with reductions in other sugars including xylose, galactose, sugar phosphates and sugar alcohols3. Besides sugars, amino acids, phenolic compounds and volatiles are the main indicators of fruit © The Author(s) 2021, corrected publication 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Fan et al. Horticulture Research (2021)8:66 ripening. Strawberry aroma is determined by lowmolecular-weight volatile compounds generated during ripening. Over 360 volatiles have been identified in the aroma of cultivated and wild strawberries, with about 280 of them reported in cultivated strawberry5. Esters, primarily methyl and ethyl esters, constitute 25–90% of the total abundance of volatiles in strawberry and provide fruity notes6. Lactones, cyclic esters providing aromas similar to those in peach, are prominent volatiles in some varieties7. Aldehydes such as 2-hexenal, (E)- and 3-hexenal, (Z)- contribute to green or fresh aromas8. Furanones such as furaneol and mesifurane are often associated with sweet aromas9. Sensory analyses are necessary to comprehensively characterize fruit flavors, which are highly influenced by retronasal olfaction10. Odor Activity Values (OAVs), which are ratios of concentration to odor thresholds, were adopted in early studies to identify potent volatile compounds in strawberry11. These studies identified several compounds as important to strawberry flavor including (Z)-3-hexenal (green), 4-hydroxy-2,5-dimethyl-3(2H)furanone (sweet), methyl butanoate (fruity), and ethyl butanoate (fruity). However, OAVs do not account for interactions between the matrix and the volatile, since the denominator only reflects odor intensity in a water solution12. Furthermore, OAVs are only based on orthonasal olfaction which is a different sensory experience than retronasal olfaction. Gas chromatography-olfactometry (GC-O) is another powerful tool to identify potent volatiles in food. Comparable results were obtained by GC-O and OAV for strawberry, agreeing on the most intense odorants8,13. However, while these studies identified potent volatiles, synergy among volatile compounds to produce human sensory responses and interactions between taste and retronasal olfaction were unexplored. Studies on tomato flavor have highlighted the flaws of using OAVs exclusively for determining volatiles important to sensory perceptions14. Large-scale sensory and chemic (...truncated)