Targeted approaches to improve tomato fruit taste

Abstract

Tomato (Solanum lycopersicum) is the most valuable fruit and horticultural crop species worldwide. Compared with the fruits of their progenitors, those of modern tomato cultivars are, however, often described as having unsatisfactory taste or lacking flavor. The flavor of a tomato fruit arises from a complex mix of tastes and volatile metabolites, including sugars, acids, amino acids, and various volatiles. However, considerable differences in fruit flavor occur among tomato varieties, resulting in mixed consumer experiences. While tomato breeding has traditionally been driven by the desire for continual increases in yield and the introduction of traits that provide a long shelf-life, consumers are prepared to pay a reasonable premium for taste. Therefore, it is necessary to characterize preferences of tomato flavor and to define its underlying genetic basis. Here, we review recent conceptual and technological advances that have rendered this more feasible, including multi-omics-based QTL and association analyses, along with the use of trained testing panels, and machine learning approaches. This review proposes how the comprehensive datasets compiled to date could allow a precise rational design of tomato germplasm resources with improved organoleptic quality for the future.

Acknowledgements

We apologize to those authors whose work could not be discussed due to space limitations. This work was supported by the Hainan Province Science and Technology Special Fund (ZDYF2022XDNY144), the National Natural Science Foundation of China (No. 32100212), the National Key R&D Program of China (2021YFA0909600), the Young Elite Scientists Sponsorship Program by CAST (No. 2019QNRC001), the Hainan Provincial Academician Innovation Platform Project (No. HD-YSZX-202004), the Hainan University Startup Fund [Nos. KYQD (ZR) 1916 and KYQD (ZR) 21025] and the Innovation Project of Postgraduates of Hainan Province (No. Qhys2021-171).

Author contributions

S-C.W. and J.Y. conceptualized and prepared the review and wrote the original draft. J.Y., Q.Q., L.-J.X., S.-C.W., and A.R.F. conducted the literature review and edited the manuscript. Q.Q. constructed the figures. S.-C.W. was responsible for the conceptualization and funding acquisition.

Conflict of interest

The authors declare that they have no conflict of interest.

References

[1] Goff SA, Klee HJ . Plant volatile compounds: sensory cues for health and nutritional value? Science. 2006; 311: 815-9.

[2] Li J, Scarano A, Gonzalez NM et al. Biofortified tomatoes provide a new route to vitamin D sufficiency. Nat Plants. 2022; 8: 611-6.

[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. 2012; 77: 193-8.

[4] Zhang B, Tieman DM, Jiao C et al. Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation. Proc Natl Acad Sci USA. 2016; 113: 12580-5.

[5] Powell ALT, Nguyen CV, Hill T et al. Uniform ripening encodes a golden 2-like transcription factor regulating tomato fruit chloroplast development. Science. 2012; 336: 1711-5.

[6] Klee HJ, Tieman DM . Genetic challenges of flavor improvement in tomato. Trends Genet. 2013; 29: 257-62.

[7] Tieman D, Zhu G, Resende MFR Jr et al. A chemical genetic roadmap to improved tomato flavor. Science. 2017; 355: 391-4.

[8] Zhao J, Sauvage C, Bitton F et al. Multiple haplotype-based analyses provide genetic and evolutionary insights into tomato fruit weight and composition. Hortic Res. 2022; 9: uhab009.

[9] Prudent M, Causse M, Génard M et al. Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection. J Exp Bot. 2009; 60: 923-37.

[10] Colantonio V, Ferrão LFV, Tieman DM et al. Metabolomic selection for enhanced fruit flavor. Proc Natl Acad Sci USA. 2022; 119: e2115865119.

[11] Klee HJ, Tieman DM . The genetics of fruit flavour preferences. Nat Rev Genet. 2018; 19: 347-56.

[12] Fernie AR, Alseekh S . Metabolomic selection-based machine learning improves fruit taste prediction. Proc Natl Acad Sci USA. 2022; 119: e2201078119.

[13] Bartoshuk LM, Klee HJ . Better fruits and vegetables through sensory analysis. Curr Biol. 2013; 23: R374-8.

[14] Zhao J, Sauvage C, Zhao J et al. Meta-analysis of genome-wide association studies provides insights into genetic control of tomato flavor. Nat Commun. 2019; 10: 1534.

[15] Baldwin EA, Scott JW, Shewmaker CK et al. Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components. HortScience. 2000; 35: 1013-22.

[16] Goulet C, Kamiyoshihara Y, Lam NB et al. Divergence in the enzymatic activities of a tomato and Solanum pennellii alcohol acyltransferase impacts fruit volatile ester composition . Mol Plant. 2015; 8: 153-62.

[17] Zhu GT, Gou JB, Klee H et al. Next-gen approaches to flavor-related metabolism. Annu Rev Plant Biol. 2019; 70: 187-212.

[18] Tieman D, Bliss P, McIntyre LM et al. The chemical interactions underlying tomato flavor preferences. Curr Biol. 2012; 22: 1035-9.

[19] Alseekh S, Aharoni A, Brotman Y et al. Mass spectrometry-based metabolomics: a guide for annotation, quantification and best reporting practices. Nat Methods. 2021; 18: 747-56.

[20] de Souza LP, Alseekh S, Scossa F et al. Ultra-high-performance liquid chromatography high-resolution mass spectrometry variants for metabolomics research. Nat Methods. 2021; 18: 733-46.

[21] Reineccius G. Flavor deterioration during food storage. In: Leif H S, Jens R and Mogens L A (eds), Chemical Deterioration and Physical Instability of Food and Beverages. Elsevier, 2010, 95-112.

[22] Andujar-Ortiz I, Peppard TL, Reineccius G . Flavoromics for determining markers of cooked and fermented flavor in strawberry juices. Abstr Pap Am Chem Soc. 2014; 1191: 293-312.

[23] Blank I, Wüst M, Yeretzian C . Expression of multidisciplinary flavor science: research highlights from the 12th Weurman symposium. J Agric Food Chem. 2009; 57: 9857-9.

[24] Gao C, Tello E, Peterson DG . Identification of coffee compounds that suppress bitterness of brew. Food Chem. 2021; 350: 129225.

[25] Gracka A, Jelen HH, Majcher M et al. Flavoromics approach in monitoring changes in volatile compounds of virgin rapeseed oil caused by seed roasting. J Chromatogr A. 2016; 1428: 292-304.

[26] Ronningen IG, Peterson DG . Identification of aging-associated food quality changes in citrus products using untargeted chemical profiling. J Agric Food Chem. 2018; 66: 682-8.

[27] Sittipod S, Schwartz E, Paravisini L et al. Identification of flavor modulating compounds that positively impact coffee quality. Food Chem. 2019; 301: 125250.

[28] Savoi S, Wong DCJ, Arapitsas P et al. Transcriptome and metabolite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes (Vitis vinifera L.). BMC Plant Biol. 2016; 16: 67.

[29] Agius C, von Tucher S, Poppenberger B et al. Quantification of sugars and organic acids in tomato fruits. MethodsX. 2018; 5: 537-50.

[30] Lin D, Zhu X, Qi B et al. SlMIR164A regulates fruit ripening and quality by controlling SlNAM2 and SlNAM3 in tomato . Plant Biotechnol J. 2022; 20: 1456-69.

[31] Schauer N, Zamir D, Fernie AR . Metabolic profiling of leaves and fruit of wild species tomato: a survey of the Solanum lycopersicum complex . J Exp Bot. 2005; 56: 297-307.

[32] Shammai A, Petreikov M, Yeselson Y et al. Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit . Plant J. 2018; 96: 343-57.

[33] Chen LQ, Qu XQ, Hou BH et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2012; 335: 207-11.

[34] Paolo D, Bianchi G, Morelli CF et al. Impact of drying techniques, seasonal variation and organic growing on flavor compounds profiles in two Italian tomato varieties. Food Chem. 2019; 298: 125062.

[35] Scarano A, Gerardi C, Sommella E et al. Engineering the polyphenolic biosynthetic pathway stimulates metabolic and molecular changes during fruit ripening in “bronze” tomato. Hortic Res. 2022; 9: uhac097.

[36] Centeno DC, Osorio S, Nunes-Nesi A et al. Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell. 2011; 23: 162-84.

[37] Cebolla-Cornejo J, Roselló S, Valcárcel M et al. Evaluation of genotype and environment effects on taste and aroma flavor components of Spanish fresh tomato varieties. J Agric Food Chem. 2011; 59: 2440-50.

[38] Lobit P, Genard M, Soing P et al. Modelling malic acid accumulation in fruits: relationships with organic acids, potassium, and temperature. J Exp Bot. 2006; 57: 1471-83.

[39] Ye J, Wang X, Hu T et al. An indel in the promoter of Al-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. Plant Cell. 2017; 29: 2249-68.

[40] Ma B, Chen J, Zheng H et al. Comparative assessment of sugar and malic acid composition in cultivated and wild apples. Food Chem. 2015; 172: 86-91.

[41] Anthon GE, LeStrange M, Barrett DM . Changes in pH, acids, sugars and other quality parameters during extended vine holding of ripe processing tomatoes. J Sci Food Agr. 2011; 91: 1175-81.

[42] Buttery RG, Ling LC . Volatile compounds of tomato fruit and plant parts: relationship and biogenesis. ACS Symp Ser Am Chem Soc. 1993; 525: 23-34.

[43] Tikunov YM, Roohanitaziani R, Meijer-Dekens F et al. The genetic and functional analysis of flavor in commercial tomato: the FLORAL4 gene underlies a QTL for floral aroma volatiles in tomato fruit . Plant J. 2020; 103: 1189-204.

[44] Rachel DR, Sitrit Y, Tadmor Y et al. Tomato aroma: biochemistry and biotechnology. In: Daphna HF, Nativ D (eds), Biotechnology in Flavor Production. John Wiley & Sons, 2016, 243-63.

[45] Garbowicz K, Liu Z, Alseekh S et al. Quantitative trait loci analysis identifies a prominent gene involved in the production of fatty acid-derived flavor volatiles in tomato. Mol Plant. 2018; 11: 1147-65.

[46] Gonda I, Bar E, Portnoy V et al. Branched-chain and aromatic amino acid catabolism into aroma volatiles in Cucumis melo L. fruit . J Exp Bot. 2010; 61: 1111-23.

[47] Kochevenko A, Araújo WL, Maloney GS et al. Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits. Mol Plant. 2012; 5: 366-75.

[48] Kaminaga Y, Schnepp J, Peel G et al. Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J Biol Chem. 2006; 281: 23357-66.

[49] Tieman DM, Loucas HM, Kim JY et al. Tomato phenylacetaldehyde reductases catalyze the last step in the synthesis of the aroma volatile 2-phenylethanol. Phytochemistry. 2007; 68: 2660-9.

[50] Tieman D, Taylor M, Schauer N et al. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci USA. 2006; 103: 8287-92.

[51] Koeduka T, Fridman E, Gang DR et al. Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. Proc Natl Acad Sci USA. 2006; 103: 10128-33.

[52] Zubieta C, Ross JR, Koscheski P et al. Structural basis for substrate recognition in the salicylic acid carboxyl methyltransferase family. Plant Cell. 2003; 15: 1704-16.

[53] Tieman D, Zeigler M, Schmelz E et al. Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J. 2010; 62: 113-23.

[54] Liscombe DK, Kamiyoshihara Y, Ghironzi J et al. A flavin-dependent monooxygenase produces nitrogenous tomato aroma volatiles using cysteine as a nitrogen source. Proc Natl Acad Sci USA. 2022; 119: e2118676119.

[55] Lewinsohn E, Sitrit Y, Bar E et al. Carotenoid pigmentation affects the volatile composition of tomato and watermelon fruits, as revealed by comparative genetic analyses. J Agric Food Chem. 2005; 53: 3142-8.

[56] Simkin AJ, Schwartz SH, Auldridge M et al. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J. 2004; 40: 882-92.

[57] Vogel JT, Tieman DM, Sims CA et al. Carotenoid content impacts flavor acceptability in tomato (Solanum lycopersicum). J Sci Food Agric. 2010; 90: 2233-40.

[58] Falara V, Akhtar TA, Nguyen TTH et al. The tomato terpene synthase gene family. Plant Physiol. 2011; 157: 770-89.

[59] Cárdenas PD, Sonawane PD, Heinig U et al. The bitter side of the nightshades: genomics drives discovery in Solanaceae steroidal alkaloid metabolism. Phytochemistry. 2015; 113: 24-32.

[60] Itkin M, Heinig U, Tzfadia O et al. Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science. 2013; 341: 175-9.

[61] Itkin M, Rogachev I, Alkan N et al. GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell. 2011; 23: 4507-25.

[62] Cárdenas PD, Sonawane PD, Heinig U et al. Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases . Nat Commun. 2019; 10: 5169.

[63] Kazachkova Y, Zemach I, Panda S et al. The GORKY glycoalkaloid transporter is indispensable for preventing tomato bitterness. Nat Plants. 2021; 7: 468-80.

[64] de Lourdes Mata Bilbao M, Andrés-Lacueva C, Jáuregui O et al. Determination of flavonoids in a citrus fruit extract by LC-DAD and LC-MS. Food Chem. 2007; 101: 1742-7.

[65] Adato A, Mandel T, Mintz-Oron S et al. Fruit-surface flavonoid accumulation in tomato is controlled by a SIMYB12-regulated transcriptional network . PLoS Genet. 2009; 5: e1000777.

[66] Bovy A, Schijlen E, Hall RD . Metabolic engineering of flavonoids in tomato (Solanum lycopersicum): the potential for metabolomics . Metabolomics. 2007; 3: 399-412.

[67] Jung UJ, Kim SR . Effects of naringin, a flavanone glycoside in grapefruits and citrus fruits, on the nigrostriatal dopaminergic projection in the adult brain. Neural Regen Res. 2014; 9: 1514-7.

[68] Muir SR, Collins GJ, Robinson S et al. Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol. 2001; 19: 470-4.

[69] Dong J, Chen Y, Yang F et al. Naringin exerts therapeutic effects on mice colitis: a study based on transcriptomics combined with functional experiments. Front Pharmacol. 2021; 12: 729414.

[70] Pagés G, Deborde C, Lemaire-Chamley M et al. MRSI vs CEST MRI to understand tomato metabolism in ripening fruit: is there a better contrast? Anal Bioanal Chem. 2021; 413: 1251-7.

[71] Li Y, Chen Y, Zhou L et al. MicroTom metabolic network: rewiring tomato metabolic regulatory network throughout the growth cycle. Mol Plant. 2020; 13: 1203-18.

[72] Tikunov YM, De Vos RCH, González Paramá SAM et al. A role for differential glycoconjugation in the emission of phenylpropanoid volatiles from tomato fruit discovered using a metabolic data fusion approach. Plant Physiol. 2009; 152: 55-70.

[73] Tikunov Y, Lommen A, de Vos CHR et al. A novel approach for nontargeted data analysis for metabolomics. Large-scale profiling of tomato fruit volatiles. Plant Physiol. 2005; 139: 1125-37.

[74] Van Schadewijk R, Krug JR, Shen D et al. Magnetic resonance microscopy at cellular resolution and localised spectroscopy of Medicago truncatula at 22.3 tesla . Sci Rep. 2020; 10: 971.

[75] Sreenivasulu N, Fernie AR . Diversity: current and prospective secondary metabolites for nutrition and medicine. Curr Opin Biotechnol. 2021; 74: 164-70.

[76] Zhang Y, Butelli E, Alseekh S et al. Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nat Commun. 2015; 6: 8635.

[77] Butelli E, Titta L, Giorgio M et al. Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol. 2008; 26: 1301-8.

[78] Herrera-Rocha F, Cala MP, Aguirre Mejía JL et al. Dissecting fine-flavor cocoa bean fermentation through metabolomics analysis to break down the current metabolic paradigm. Sci Rep. 2021; 11: 21904.

[79] Krishnan P, Kruger NJ, Ratcliffe RG. Metabolite fingerprinting and profiling in plants using NMR. J Exp Bot. 2005; 56: 255-65.

[80] Peris M, Escuder-Gilabert L . Electronic noses and tongues to assess food authenticity and adulteration. Trends Food Sci Tech. 2016; 58: 40-54.

[81] Vitalis F, Zaukuu JLZ, Bodor Z et al. Detection and quantification of tomato paste adulteration using conventional and rapid analytical methods. Sensors (Basel). 2020; 20: 6059.

[82] Xu S, Sun X, Lu H et al. Detecting and monitoring the flavor of tomato (Solanum lycopersicum) under the impact of postharvest handlings by physicochemical parameters and electronic nose . Sensors-Basel. 2018; 18: 1847.

[83] Fernie AR, Aharoni A . Pan-genomic illumination of tomato identifies novel gene-trait interactions. Trends Plant Sci. 2019; 24: 882-4.

[84] Liu D, Yang L, Zhang JZ et al. Domestication and breeding changed tomato fruit transcriptome. J Integr Agr. 2020; 19: 120-32.

[85] Sauvage C, Segura V, Bauchet G et al. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 2014; 165: 1120-32.

[86] Zhu G, Wang S, Huang Z et al. Rewiring of the fruit metabolome in tomato breeding. Cell. 2018; 172: 249-261.e12.

[87] Alonge M, Wang X, Benoit M et al. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell. 2020; 182: 145-161.e23.

[88] Cárdenas PD, Sonawane PD, Pollier J et al. GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nat Commun. 2016; 7: 10654.

[89] Schwahn K, de Souza LP, Fernie AR et al. Metabolomics-assisted refinement of the pathways of steroidal glycoalkaloid biosynthesis in the tomato clade. J Integr Plant Biol. 2014; 56: 864-75.

[90] Yu G, Li C, Zhang L et al. An allelic variant of GAME9 determines its binding capacity with the GAME17 promoter in the regulation of steroidal glycoalkaloid biosynthesis in tomato . J Exp Bot. 2020; 71: 2527-36.

[91] Grisel JE, Crabbe JC . Quantitative trait loci mapping. Alcohol Health Res World. 1995; 19: 220-7.

[92] Luo J . Metabolite-based genome-wide association studies in plants. Curr Opin Plant Biol. 2015; 24: 31-8.

[93] Ye J, Li W, Ai G et al. Genome-wide association analysis identifies a natural variation in basic helix-loop-helix transcription factor regulating ascorbate biosynthesis via D-mannose/L-galactose pathway in tomato. PLoS Genet. 2019; 15: e1008149.

[94] Bauchet G, Grenier S, Samson N et al. Identification of major loci and genomic regions controlling acid and volatile content in tomato fruit: implications for flavor improvement. New Phytol. 2017; 215: 624-41.

[95] Li X, Tieman D, Liu Z et al. Identification of a lipase gene with a role in tomato fruit short-chain fatty acid-derived flavor volatiles by genome-wide association. Plant J. 2020; 104: 631-44.

[96] Mathieu S, Cin VD, Fei Z et al. Flavour compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition. J Exp Bot. 2009; 60: 325-37.

[97] Pereira L, Sapkota M, Alonge M et al. Natural genetic diversity in tomato flavor genes. Front Plant Sci. 2021; 12: 642828.

[98] Wang R, Shu P, Zhang C et al. Integrative analyses of metabolome and genome-wide transcriptome reveal the regulatory network governing flavor formation in kiwifruit (Actinidia chinensis). New Phytol. 2021; 233: 373-89.

[99] Beleggia R, Rau D, Laidò G et al. Evolutionary metabolomics reveals domestication-associated changes in tetraploid wheat kernels. Mol Biol Evol. 2016; 33: 1740-53.

[100] Shepherd GM . Smell images and the flavour system in the human brain. Nature. 2006; 444: 316-21.

[101] Stommel J, Abbott JA, Saftner RA et al. Sensory and objective quality attributes of beta-carotene and lycopene-rich tomato fruit. J Am Soc Hortic Sci. 2005; 130: 244-51.

[102] Farneti B, Khomenko I, Grisenti M et al. Exploring blueberry aroma complexity by chromatographic and direct-injection spectrometric techniques. Front Plant Sci. 2017; 8: 617.

[103] Dong X, Gao Y, Chen W et al. Spatiotemporal distribution of phenolamides and the genetics of natural variation of hydroxycinnamoyl spermidine in rice. Mol Plant. 2015; 8: 111-21.

[104] Yuan H, Cao G, Hou X et al. Development of a widely-targeted volatilomics method for profiling the volatilomes in plants. Mol Plant. 2021; 15: 189-202.

[105] Wen W, Li D, Li X et al. Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat Commun. 2014; 5: 3438.

[106] Fernie AR, Schauer N . Metabolomics-assisted breeding: a viable option for crop improvement? Trends Genet. 2009; 25: 39-48.

[107] Huang X, Huang S, Han B et al. The integrated genomics of crop domestication and breeding. Cell. 2022; 185: 2828-39.

[108] Szymański J, Bocobza S, Panda S et al. Analysis of wild tomato introgression lines elucidates the genetic basis of transcriptome and metabolome variation underlying fruit traits and pathogen response. Nat Genet. 2020; 52: 1111-21.

[109] Maloney GS, Kochevenko A, Tieman DM et al. Characterization of the branched-chain amino acid aminotransferase enzyme family in tomato. Plant Physiol. 2010; 153: 925-36.

[110] Dominguez M, Dugas E, Benchouaia M et al. The impact of transposable elements on tomato diversity. Nat Commun. 2020; 11: 4058.

[111] Davidovich-Rikanati R, Sitrit Y, Tadmor Y et al. Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway. Nat Biotechnol. 2007; 25: 899-901.

[112] Gao L, Gonda I, Sun H et al. The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nat Genet. 2019; 51: 1044- 51.

[113] Shen JY, Tieman D, Jones JB et al. A 13-lipoxygenase, Tomlox C, is essential for synthesis of C5 flavour volatiles in tomato. J Exp Bot. 2014; 65: 419-28.

[114] Leon J, Royo J, Vancanneyt G et al. Lipoxygenase H1 gene silencing reveals a specific role in supplying fatty acid hydroperoxides for aliphatic aldehyde production. J Biol Chem. 2002; 277: 416-23.

[115] Goulet C, Mageroy MH, Lam NB et al. Role of an esterase in flavor volatile variation within the tomato clade. Proc Natl Acad Sci USA. 2012; 109: 19009-14.

[116] Speirs J, Lee E, Holt K et al. Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol. 1998; 117: 1047-58.