Review Article | Published:

The genetics of fruit flavour preferences

Nature Reviews Geneticsvolume 19pages347356 (2018) | Download Citation

Abstract

Intensively bred fruit crops, including tomatoes and strawberries, are widely viewed as lacking flavour. The lack of breeder focus on the consumer is largely due to the genetic complexity of the flavour phenotype as well as a lack of a simple assay that can define consumer preferences. Rapid advances in genomics have opened up new opportunities to understand the chemistry and genetics of flavour. Here, we describe the underlying causes for the loss of flavour in fruits over time and delineate a blueprint for defining the chemistry of consumer liking, reducing that knowledge into a molecular roadmap for flavour improvement.

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References

  1. 1.

    Whiteside, T. Tomatoes. The New Yorker 36–61 (24 Jan 1977).

  2. 2.

    Bruhn, C. M. et al. Consumer perceptions of quality: apricots, cantaloupes, peaches, pears, strawberries, and tomatoes. J. Food. Qual. 14, 187–195 (1991).

  3. 3.

    Fernqvist, F. & Hunter, E. Who’s to blame for tasteless tomatoes? The effect of tomato chilling on consumers’ taste perceptions. Eur. J. Hortic. Sci. 77, 193–198 (2012).

  4. 4.

    Teixeira, A., Eiras-Dias, J., Castellarin, S. D. & Geros, H. Berry phenolics of grapevine under challenging environments. Int. J. Mol. Sci. 14, 18711–18739 (2013).

  5. 5.

    Karppinen, K., Zoratti, L., Nguyenquynh, N., Häggman, H. & Jaakola, L. On the developmental and environmental regulation of secondary metabolism in Vaccinium spp. berries. Front. Plant Sci. 7, 655 (2016).

  6. 6.

    Schiffman, S. S. Taste and smell losses in normal aging and disease. J. Am. Med. Assoc. 278, 1357–1362 (1997).

  7. 7.

    Bushdid, C., Magnasco, M. O., Vosshall, L. B. & Keller, A. Humans can discriminate more than 1 trillion olfactory stimuli. Science 343, 1370–1372 (2014).

  8. 8.

    Schaefer, H. M., Schmidt, V. & Winkler, H. Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos 102, 318–328 (2003).

  9. 9.

    Carrari, F. et al. Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant. Physiol. 142, 1380–1396 (2006).

  10. 10.

    Baldwin, E. A., Scott, J. W., Shewmaker, C. K. & Schuch, W. Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components. Hort Sci. 35, 1013–1022 (2000).

  11. 11.

    Dimick, P. S. & Hoskin, J. C. Review of apple flavour — state of the art. Crit. Rev. Food. Sci. Nutr. 18, 387–409 (1983).

  12. 12.

    Garcia, C., Quek, S.-Y., Stevenson, R. & Winz, R. Kiwifruit flavour: a review. Trends Food Sci. Technol. 24, 82–91 (2012).

  13. 13.

    Tikunov, Y. et al. Non-smoky glycosyltransferase1 prevents the release of smoky aroma from tomato fruit. Plant Cell 25, 3067–3078 (2013). Identifies an important function for glycosylation as a means to modify the contents of important flavour volatile chemicals.

  14. 14.

    Buttery, R. G., Teranishi, R., Flath, R. A. & Ling, L. C. in Flavor Chemistry: Trends and Developments (Teranishi, R., Buttery, R. G. & Shahidi, F. eds) 213–222 (American Chemical Society, Washington DC, 1987). One of the first papers to systematically identify the most important volatile chemicals contributing to tomato flavour.

  15. 15.

    Hasin-Brumshtein, Y., Lancet, D. & Olender, T. Human olfaction: from genomic variation to phenotypic diversity. Trends. Genet. 25, 178–184 (2009).

  16. 16.

    Tandon, K. S., Baldwin, E. A. & Shewfelt, R. L. Aroma perception of individual volatile compounds in fresh tomatoes (Lycopersicon esculentum, Mill.) as affected by the medium of evaluation. Postharvest. Biol. Technol. 20, 261–268 (2000).

  17. 17.

    Cometto-Muñiz, J. E. & Abraham, M. H. Human olfactory detection of homologous n-alcohols measured via concentration-response functions. Pharmacol. Biochem. Behav. 89, 279–291 (2008).

  18. 18.

    Firestein, S. How the olfactory system makes sense of scents. Nature 413, 211–218 (2001).

  19. 19.

    Tadmor, Y. et al. Identification of malodorous, a wild species allele affecting tomato aroma that was selected against during domestication. J. Agric. Food. Chem. 50, 2005–2009 (2002).

  20. 20.

    Plotto, A., Bai, J. & Baldwin, E. in Springer Handbook of Odor (ed. Buettner, A.) 27–28 (Springer International Publishing, Switzerland, 2017). A thorough review of the flavour chemical compositions of a large range of fruits.

  21. 21.

    Schwieterman, M. L. et al. Strawberry flavor: diverse chemical compositions, a seasonal influence, and effects on sensory perception. PLoS. ONE. 9, e88446 (2014).

  22. 22.

    Visai, C. & Vanoli, M. Volatile compound production during growth and ripening of peaches and nectarines. Sci. Hortic. 70, 15–24 (1997).

  23. 23.

    Tieman, D. et al. A chemical genetic roadmap to improved tomato flavor. Science 355, 391–394 (2017). Broadly defines the most important tomato chemicals contributing to consumer preferences and identifies QTLs impacting the contents of those chemicals in fruit.

  24. 24.

    Tieman, D. M. et al. The chemical interactions underlying tomato flavor preferences. Curr. Biol. 22, 1–5 (2012).

  25. 25.

    Goff, S. A. & Klee, H. J. Plant volatile compounds: sensory cues for health and nutritional value? Science 311, 815–819 (2006).

  26. 26.

    Ulrich, D. & Olbricht, K. A search for the ideal flavor of strawberry–comparison of consumer acceptance and metabolite patterns in Fragaria×ananassa Duch. J. Appl. Bot. Food Qual. 89, 223–234 (2016).

  27. 27.

    Gilbert, J. L. et al. Identifying breeding priorities for blueberry flavor using biochemical, sensory, and genotype by environment analyses. PLoS. ONE 10, e0138494 (2015).

  28. 28.

    Bai, Y. L. & Lindhout, P. Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann. Bot. 100, 1085–1094 (2007).

  29. 29.

    Tanksley, S. D. The genetic, developmental and molecular bases of fruit size and shape variation in tomato. Plant Cell 16, 181–189 (2004).

  30. 30.

    Lin, T. et al. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46, 1220–1226 (2014). A systematic evaluation of multiple tomato genome sequences demonstrating the impact of human selection on genome diversity.

  31. 31.

    Zhu, G. et al. Rewiring of the fruit metabolome in tomato breeding. Cell 172, 249–261 (2018). An integrated examination of the effects of breeding on the genome, transcriptome and metabolome.

  32. 32.

    Powell, A. L. T. et al. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336, 1711–1715 (2012). A great example of unintended negative consequences of breeding selection on tomato fruit quality.

  33. 33.

    Causse, M. et al. Consumer preferences for fresh tomato at the European scale: a common segmentation on taste and firmness. J. Food Sci. 75, S531–S541 (2010).

  34. 34.

    Bartoshuk, L. & Klee, H. Better fruits and vegetables through sensory analysis. Curr. Biol. 23, R374–R378 (2013).

  35. 35.

    Eshed, Y. & Zamir, D. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141, 1147–1162 (1995).

  36. 36.

    Monforte, A. J. & Tanksley, S. D. Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43, 803–813 (2000).

  37. 37.

    Fridman, E., Carrari, F., Liu, Y. S., Fernie, A. R. & Zamir, D. Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305, 1786–1789 (2004).

  38. 38.

    Zanor, M. et al. Metabolic characterization of loci affecting sensory attributes in tomato allows an assessment of the influence of the levels of primary metabolites and volatile organic contents. J. Exp. Bot. 60, 2139–2154 (2009).

  39. 39.

    Zhang, J. et al. Genome-wide association mapping for tomato volatiles positively contributing to tomato flavor. Front. Plant Sci. 6, 1042 (2015).

  40. 40.

    Ronen, G., Carmel-Goren, L., Zamir, D. & Hirschberg, J. An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc.Natl Acad. Sci. USA 97, 11102–11107 (2000).

  41. 41.

    Isaacson, T., Ronen, G., Zamir, D. & Hirschberg, J. Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 14, 333–342 (2002).

  42. 42.

    Tieman, D. et al. Aromatic amino acid decarboxylases participate in the synthesis of the flavor and aroma volatiles 2-phenylethanol and 2-phenylacetaldehyde in tomato fruits. Proc. Natl Acad. Sci. USA 103, 8287–8292 (2006).

  43. 43.

    Mageroy, M. H., Floystad, A., Taylor, M. G., Tieman, D. M. & Klee, H. J. A. Solanum lycopersicum catechol-O-methyltransferase involved in synthesis of the flavor molecule guaiacol. Plant. J. 69, 1043–1051 (2012).

  44. 44.

    Goulet, C. et al. Role of an esterase in flavor volatile variation within the tomato clade. Proc. Natl Acad. Sci. USA 109, 19009–19014 (2012).

  45. 45.

    Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641 (2012).

  46. 46.

    Bolger, A. et al. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat. Genet. 46, 1034–1038 (2014).

  47. 47.

    Ranjan, A. et al. eQTL regulating transcript levels associated with diverse biological processes in tomato. Plant. Physiol. 172, 328–340 (2016).

  48. 48.

    Bauchet, G. et al. Identification of major loci and genomic regions controlling acid and volatile content in tomato fruit: implications for flavor improvement. New. Phytol. 215, 624–641 (2017).

  49. 49.

    Pillet, J. et al. Identification of a methyltransferase catalyzing the final step of methyl anthranilate synthesis in cultivated strawberry. BMC Plant Biol. 17, 147–158 (2017).

  50. 50.

    Schieberle, P. & Hofmann, T. Evaluation of the character impact odorants in fresh strawberry juice by quantitative measurements and sensory studies on model mixtures. J. Agr. Food Chem. 45, 227–232 (1997).

  51. 51.

    Schreier, P. Quantitative composition of volatile constituents in cultivated strawberries. Fragaria Ananassa cv. Senga Sengana, Senga Litessa and Senga Gourmella. J. Sci. Food Agric. 31, 487–494 (1980).

  52. 52.

    Aharoni, A. et al. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12, 647–661 (2000).

  53. 53.

    Chambers, A. H. et al. Identification of a strawberry flavor gene candidate using an integrated genetic-genomic-analytical chemistry approach. BMC Genomics. 15, 217 (2014).

  54. 54.

    Duan, N. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat. Commun. 8, 249 (2017).

  55. 55.

    Bai, Y., Dougherty, D., Cheng, L. L. & Xu, K. N. A natural mutation-led truncation in one of the two aluminum activated malate transporter-like genes at the Ma locus is associated with low fruit acidity in apple. Mol. Genet. Genomics 287, 663–678 (2012).

  56. 56.

    Kumar, S. et al. Genome-wide scans reveal genetic architecture of apple flavour volatiles. Mol. Breed. 35, 118–133 (2015).

  57. 57.

    Farneti, B. et al. Genome-wide association study unravels the genetic control of the apple volatilome and its interplay with fruit texture. J. Exp. Bot. 68, 1467–1478 (2017).

  58. 58.

    Zhou, Y. et al. Convergence and divergence of bitterness biosynthesis and regulation in Cucurbitaceae. Nat. Plants 2, 16183 (2016).

  59. 59.

    Moskowitz, H., Gofman, A. & Beckley, J. Using high-level consumer research methods to create a tool-driven guidebook and database for product development and marketing. J. Sens. Stud. 21, 54–100 (2006).

  60. 60.

    Goulet, C. et al. Divergence in the enzymatic activities of a tomato and solanum pennellii alcohol acyltransferase impacts fruit volatile ester composition. Mol. Plant 8, 153–162 (2015).

  61. 61.

    Tieman, D. M. et al. Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant. J. 62, 113–123 (2010).

  62. 62.

    Dal Cin, V. et al. Ectopic expression of a MYB transcription factor defines a set of co-regulated tomato phenylalanine and phenylpropanoid synthesis genes. Plant Cell 23, 2738–2753 (2011).

  63. 63.

    Tieman, D., Loucas, H., Kim, J.-Y., Clark, D. & Klee, H. Tomato phenylacetaldehyde reductases catalyze the last step in the synthesis of the aroma volatile 2-phenylethanol. Phytochemistry. 68, 2660–2669 (2007).

  64. 64.

    Chen, G. P. et al. Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant. Physiol. 136, 2641–2651 (2004).

  65. 65.

    Howe, G. A., Lee, G. I., Itoh, A., Li, L. & DeRocher, A. E. Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant. Physiol. 123, 711–724 (2000).

  66. 66.

    Speirs, J. et al. Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant. Physiol. 117, 1047–1058 (1998).

  67. 67.

    Simkin, A., Schwartz, S., Auldridge, M., Taylor, M. & Klee, H. The tomato carotenoid cleavage dioxgenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone and geranylacetone. Plant. J. 40, 882–892 (2004).

  68. 68.

    Folta, K. M. & Klee, H. J. Sensory sacrifices when we mass-produce mass produce. Hortic. Res. 3, 16032 (2016).

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Acknowledgements

The tomato work performed by the authors and described here was supported by grants from the US National Science Foundation as well as an endowment provided to the University of Florida by the Lyle Dickman family.

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Affiliations

  1. University of Florida, Horticultural Sciences, Gainesville, FL, USA

    • Harry J. Klee
    •  & Denise M. Tieman

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  2. Search for Denise M. Tieman in:

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The authors contributed equally to all aspects of the manuscript.

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The authors declare no competing interests.

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Corresponding author

Correspondence to Harry J. Klee.

Glossary

Cultivar

A plant variety that has been produced in cultivation by selective breeding for desirable characteristics.

Molecular breeding

A process broadly encompassing all aspects of molecular biology, including genetic engineering and genome editing, but more narrowly defined as the use of large-scale genomic data to define genetic differences between individuals in a breeding population. These polymorphisms are used to develop genetic markers that facilitate the rapid selection of cultivars with desired traits.

Genome-wide association studies

(GWAS). Association mapping of a phenotype in a population with whole-genome DNA polymorphisms.

Volatile organic compounds

Organic compounds that have a high vapour pressure at room temperature. High vapour pressure allows the chemical to partition into the gas phase. Volatile organic compounds are important contributors to flavour when they vapourize in the mouth and travel to the olfactory epithelium where they are recognized by specific sets of receptors.

Principal component analysis

A statistical method that is used to simplify a complex data set by transforming a series of correlated variables into a smaller number of uncorrelated variables called principal components.

Retronasal olfaction

The sensory modality responsible for flavour. Perception of volatiles generated within the mouth and transmitted to the olfactory epithelium.

Linkage drag

A negative effect on some aspect of quality or plant performance upon backcrossing a gene into a different cultivar. Typically refers to negative effects associated with genes physically linked to the gene of interest. A particular problem when introgressing a trait (such as disease resistance) from a different sexually compatible species.

Introgression lines

(ILs). A genetic line that contains a gene or region of a chromosome from one species in the genome of another. It is created by repeated backcrossing of an interspecific hybrid with one of its parents.

Heirloom varieties

Older varieties that have been maintained for some desirable attribute (for example, flavour, colour and shape). Although there is no legal definition of ‘heirloom’, it is generally considered to be inbred. Heirlooms usually lack the performance and disease resistance found in modern cultivars.

Quantitative trait locus

(QTL). A region of a chromosome that quantitatively influences a measured phenotype. That region, defined by polymorphic molecular markers, contains one or more physically linked genes causative of the phenotype.

Selection bottleneck

A substantial enrichment for a specific subset of genes with reduced allelic variation relative to the variation found in a species. Loss of diversity through intensive breeding with a small population.

Backcrossing

Recurrent crossing to a parental variety in order to introduce specific genetic loci into an otherwise isogenic line.

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DOI

https://doi.org/10.1038/s41576-018-0002-5

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