Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The genetics of fruit flavour preferences

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Synthesis pathways for tomato flavour volatiles.
Fig. 2: Identification of a locus controlling synthesis of phenylalanine-derived volatiles.
Fig. 3: Average changes in flavour-associated chemicals in modern tomato varieties.
Fig. 4: A roadmap for consumer-assisted genetic selection.

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).

    Article  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  6. 6.

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

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  12. 12.

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

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. 18.

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

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. 22.

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

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  24. 24.

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

    Article  CAS  Google Scholar 

  25. 25.

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

    Article  PubMed  CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  34. 34.

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

    Article  PubMed  CAS  Google Scholar 

  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).

    PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

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

    Article  CAS  Google Scholar 

  46. 46.

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  47. 47.

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  56. 56.

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

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. 58.

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  68. 68.

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the manuscript.

Corresponding author

Correspondence to Harry J. Klee.

Ethics declarations

Competing interests

The authors declare no competing interests.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Klee, H.J., Tieman, D.M. The genetics of fruit flavour preferences. Nat Rev Genet 19, 347–356 (2018). https://doi.org/10.1038/s41576-018-0002-5

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing