1932

Abstract

Although flavor is an essential element for consumer acceptance of food, breeding programs have focused primarily on yield, leading to significant declines in flavor for many vegetables. The deterioration of flavor quality has concerned breeders; however, the complexity of this trait has hindered efforts to improve or even maintain it. Recently, the integration of flavor-associated metabolic profiling with other omics methodologies derived from big data has become a prominent trend in this research field. Here, we provide an overview of known metabolites contributing to flavor in the major vegetables as well as genetic analyses of the relevant metabolic pathways based on different approaches, especially multi-omics. We present examples demonstrating how omics analyses can help us to understand the accomplishments of historical flavor breeding practices and implement further improvements. The integration of genetics, cultivation, and postharvest practices with genome-scale data analyses will create enormous potential for further flavor quality improvements.

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2019-04-29
2024-06-15
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Literature Cited

  1. 1.  Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS 2000. A novel family of mammalian taste receptors. Cell 100:693–702
    [Google Scholar]
  2. 2.  Alseekh S, Tohge T, Wendenberg R, Scossa F, Omranian N et al. 2015. Identification and mode of inheritance of quantitative trait loci for secondary metabolite abundance in tomato. Plant Cell 27:485–512A classical study that revealed the inheritance mode of secondary metabolite abundance.
    [Google Scholar]
  3. 3.  Bauchet G, Grenier S, Samson N, Segura V, Kende A et al. 2017. Identification of major loci and genomic regions controlling acid and volatile content in tomato fruit: implications for flavor improvement. New Phytol 215:624–41A comprehensive metabolite genome-wide association study (mGWAS) that identified flavor quantitative trait loci of tomato fruits.
    [Google Scholar]
  4. 4.  Bell L, Oloyede OO, Lignou S, Wagstaff C, Methven L 2018. Taste and flavor perceptions of glucosinolates, isothiocyanates, and related compounds. Mol. Nutr. Food Res. 62:e1700990
    [Google Scholar]
  5. 5.  Boelens M, de Valois PJ, Wobben HJ, van der Gen A 1971. Volatile flavor compounds from onion. J. Agric. Food Chem. 19:984–98
    [Google Scholar]
  6. 6.  Bouwmeester HJ, Gershenzon J, Konings MC, Croteau R 1998. Biosynthesis of the monoterpenes limonene and carvone in the fruit of caraway. I. Demonstration of enzyme activities and their changes with development. Plant Physiol 117:901–12
    [Google Scholar]
  7. 7.  Brodnitz MH, Pascale JV 1971. Flavor components of garlic extract. J. Agric. Food Chem. 19:269–72
    [Google Scholar]
  8. 8.  Buescher RH, Buescher RW 2001. Production and stability of (E, Z)-2, 6-nonadienal, the major flavor volatile of cucumbers. J. Food Sci. 66:357–61
    [Google Scholar]
  9. 9.  Bushdid C, Magnasco MO, Vosshall LB, Keller A 2014. Humans can discriminate more than 1 trillion olfactory stimuli. Science 343:1370–72
    [Google Scholar]
  10. 10.  Buttery RG 1993. Quantitative and sensory aspects of flavour of tomato and other vegetables and fruits. Flavor Science: Sensible Principles and Techniques TE Acree, R Teranishsi 259–86 Washington, DC: Am. Chem. Soc.
    [Google Scholar]
  11. 11.  Buttery RG, Ling LC 1993. Volatiles of tomato fruit and plant parts: relationship and biogenesis. Bioactive Volatile Compounds from Plants R Teranishi, RG Buttery, H Sugisawa 23–34 Washington, DC: Am. Chem. Soc.
    [Google Scholar]
  12. 12.  Cárdenas PD, Sonawane PD, Heinig U, Bocobza SE, Burdman S, Aharoni A 2015. The bitter side of the nightshades: genomics drives discovery in Solanaceae steroidal alkaloid metabolism. Phytochemistry 113:24–32
    [Google Scholar]
  13. 13.  Cárdenas PD, Sonawane PD, Pollier J, Vanden Bossche R, Dewangan V et al. 2016. GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nat. Commun. 7:10654
    [Google Scholar]
  14. 14.  Causse M, Duffe P, Gomez MC, Buret M, Damidaux R et al. 2004. A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J. Exp. Biol. 55:1671–85
    [Google Scholar]
  15. 15.  Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS 2006. The receptors and cells for mammalian taste. Nature 444:288–94
    [Google Scholar]
  16. 16.  Chen G 2004. Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136:2641–51
    [Google Scholar]
  17. 17.  Chen JC, Chiu MH, Nie RL, Cordell GA, Qiu SX 2005. Cucurbitacins and cucurbitane glycosides: structures and biological activities. Nat. Prod. Rep. 22:386–99
    [Google Scholar]
  18. 18.  Chen W, Gao Y, Xie W, Gong L, Lu K et al. 2014. Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat. Genet. 46:714–21
    [Google Scholar]
  19. 19.  Cheng F, Liu S, Wu J, Fang L, Sun S et al. 2011. BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136
    [Google Scholar]
  20. 20.  Coleman EC, Ho C-T, Chang SS 1981. Isolation and identification of volatile compounds from baked potatoes. J. Agric. Food Chem. 29:42–48
    [Google Scholar]
  21. 21.  Conesa A, Verlinden BE, Artés-Hernández F, Nicolaï B, Artés F 2007. Respiration rates of fresh-cut bell peppers under superatmospheric and low oxygen with or without high carbon dioxide. Postharvest Biol. Technol. 45:81–88
    [Google Scholar]
  22. 22.  Davidovich-Rikanati R, Sitrit Y, Tadmor Y, Iijima Y, Bilenko N et al. 2007. Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway. Nat. Biotechnol. 25:899–901
    [Google Scholar]
  23. 23.  Di R, Kim J, Martin MN, Leustek T, Jhoo JW et al. 2003. Enhancement of the primary flavor compound methional in potato by increasing the level of soluble methionine. J. Agric. Food Chem. 51:5695–702
    [Google Scholar]
  24. 24.  Do GS, Suzuki G, Mukai Y 2004. Genomic organization of a novel root alliinase gene, ALL1, in onion. Gene 325:17–24
    [Google Scholar]
  25. 25.  Duckham SC, Dodson AT, Bakker J, Ames JM 2002. Effect of cultivar and storage time on the volatile flavor components of baked potato. J. Agric. Food Chem. 50:5640–48
    [Google Scholar]
  26. 26.  Dunkel A, Steinhaus M, Kotthoff M, Nowak B, Krautwurst D et al. 2014. Nature's chemical signatures in human olfaction: a foodborne perspective for future biotechnology. Angew. Chem. Int. Edit. 53:7124–43
    [Google Scholar]
  27. 27.  Dwivedi NK, Dhariwal OP, Krishnan SG, Bhandari DC 2010. Distribution and extent of diversity in Cucumis species in the Aravalli ranges of India. Genet. Resour. Crop Evol. 57:443–52
    [Google Scholar]
  28. 28.  Edris AE, Fadel HM 2002. Investigation of the volatile aroma components of garlic leaves essential oil. Possibility of utilization to enrich garlic bulb oil. Eur. Food Res. Technol. 214:105–07
    [Google Scholar]
  29. 29.  Engel E, Baty C, Le Corre D, Souchon I, Martin N 2002. Flavor-active compounds potentially implicated in cooked cauliflower acceptance. J. Agric. Food Chem. 50:6459–67
    [Google Scholar]
  30. 30.  Eshed Y, Zamir D 1994. A genomic library of Lycopersicon pennellii in L. esculentum: a tool for fine mapping of genes. Euphytica 79:175–79
    [Google Scholar]
  31. 31.  Falara V, Akhtar TA, Nguyen TT, Spyropoulou EA, Bleeker PM et al. 2011. The tomato terpene synthase gene family. Plant Physiol 157:770–89
    [Google Scholar]
  32. 32.  Ferrie BJ, Beaudoin N, Burkhart W, Bowsher CG, Rothstein SJ 1994. The cloning of two tomato lipoxygenase genes and their differential expression during fruit ripening. Plant Physiol 106:109–11
    [Google Scholar]
  33. 33.  Fraser PD, Bramley PM 2004. The biosynthesis and nutritional uses of carotenoids. Prog. Lipid. Res. 43:228–65
    [Google Scholar]
  34. 34.  Fukuda T, Okazaki K, Shinano T 2013. Aroma characteristic and volatile profiling of carrot varieties and quantitative role of terpenoid compounds for carrot sensory attributes. J. Food Sci. 78:S1800–6
    [Google Scholar]
  35. 35.  Ginzberg I, Tokuhisa JG, Veilleux RE 2008. Potato steroidal glycoalkaloids: biosynthesis and genetic manipulation. Potato Res 52:1–15
    [Google Scholar]
  36. 36.  Gottfried JA 2010. Central mechanisms of odour object perception. Nat. Rev. Neurosci. 11:628–41
    [Google Scholar]
  37. 37.  Goulet C, Kamiyoshihara Y, Lam NB, Richard T, Taylor MG et al. 2015. Divergence in the enzymatic activities of a tomato and Solanum pennellii alcohol acyltransferase impacts fruit volatile ester composition. Mol. Plant 8:153–62
    [Google Scholar]
  38. 38.  Goulet C, Mageroy MH, Lam NB, Floystad A, Tieman DM, Klee HJ 2012. Role of an esterase in flavor volatile variation within the tomato clade. PNAS 109:19009–14
    [Google Scholar]
  39. 39.  Hanschen FS, Schreiner M 2017. Isothiocyanates, nitriles, and epithionitriles from glucosinolates are affected by genotype and developmental stage in Brassica oleracea varieties. Front. Plant Sci. 8:1095
    [Google Scholar]
  40. 40.  Hara M, Fujii Y, Sasada Y, Kuboi T 2000. cDNA cloning of radish (Raphanus sativus) myrosinase and tissue-specific expression in root. Plant Cell Physiol 41:1102–9
    [Google Scholar]
  41. 41.  Hardigan MA, Laimbeer FPE, Newton L, Crisovan E, Hamilton JP et al. 2017. Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. PNAS 114:E9999–10008
    [Google Scholar]
  42. 42.  Harper AL, Trick M, Higgins J, Fraser F, Clissold L et al. 2012. Associative transcriptomics of traits in the polyploid crop species Brassica napus. Nat. Biotechnol 30:798–802
    [Google Scholar]
  43. 43.  Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W et al. 2006. The cells and logic for mammalian sour taste detection. Nature 442:934–38
    [Google Scholar]
  44. 44.  Husain Q 2010. Chemistry and biochemistry of some vegetable flavors. Handbook of Fruit and Vegetable Flavors YH Hui, F Chen, LML Nollet, RPF Guiné, JL Le Quéré et al.575–625 Hoboken, NJ: Wiley
    [Google Scholar]
  45. 45.  Imai S, Tsuge N, Tomotake M, Nagatome Y, Sawada H et al. 2002. Plant biochemistry: an onion enzyme that makes the eyes water. Nature 419:685A simple and elegant study discovered a new enzyme that synthases the lachrymatory factor in onion.
    [Google Scholar]
  46. 46.  Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B et al. 2013. Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341:175–79Comparative genomics and transcriptomics analyses revealed a syntenic gene cluster that mediates the biosynthesis of glycoalkaloids in tomato and potato.
    [Google Scholar]
  47. 47.  Itkin M, Rogachev I, Alkan N, Rosenberg T, Malitsky S et al. 2011. GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23:4507–25
    [Google Scholar]
  48. 48.  Jakobsen HB, Hansen M, Christensen MR, Brockhoff PB, Olsen CE 1998. Aroma volatiles of blanched green peas (Pisum sativum L.). J. Agric. Food Chem. 46:3727–34
    [Google Scholar]
  49. 49.  Jansen RC, Nap JP 2001. Genetical genomics: the added value from segregation. Trends Genet 17:388–91
    [Google Scholar]
  50. 50.  Jansky SH 2010. Potato flavor. Am. J. Potato Res. 87:209–17
    [Google Scholar]
  51. 51.  Johns T, Alonso JG 1990. Glycoalkaloid change during the domestication of the potato, Solanum Section Petota. Euphytica 50:203–10
    [Google Scholar]
  52. 52.  Johnson BA, Farahbod H, Saber S, Leon M 2005. Effects of functional group position on spatial representations of aliphatic odorants in the rat olfactory bulb. J. Comp. Neurol. 483:192–204
    [Google Scholar]
  53. 53.  Jones MG, Hughes J, Tregova A, Milne J, Tomsett AB, Collin HA 2004. Biosynthesis of the flavour precursors of onion and garlic. J. Exp. Bot. 55:1903–18
    [Google Scholar]
  54. 54.  Keilwagen J, Lehnert H, Berner T, Budahn H, Nothnagel T et al. 2017. The terpene synthase gene family of carrot (Daucus carota L.): identification of QTLs and candidate genes associated with terpenoid volatile compounds. Front. Plant Sci. 8:1930
    [Google Scholar]
  55. 55.  Keller A, Zhuang HY, Chi QY, Vosshall LB, Matsunami H 2007. Genetic variation in a human odorant receptor alters odour perception. Nature 449:468–72
    [Google Scholar]
  56. 56.  Kjeldsen F, Christensen LP, Edelenbos M 2001. Quantitative analysis of aroma compounds in carrot (Daucus carota L.) cultivars by capillary gas chromatography using large-volume injection technique. J. Agric. Food Chem. 49:4342–48
    [Google Scholar]
  57. 57.  Kjeldsen F, Christensen LP, Edelenbos M 2003. Changes in volatile compounds of carrots (Daucus carota L.) during refrigerated and frozen storage. J. Agric. Food Chem. 51:5400–7
    [Google Scholar]
  58. 58.  Kopsell DE, Kopsell DA, Randle WA, Coolong TW, Sams CE, Curran-Celentano J 2003. Kale carotenoids remain stable while flavor compounds respond to changes in sulfur fertility. J. Agric. Food Chem. 51:5319–25
    [Google Scholar]
  59. 59.  Kozukue N, Han JS, Kozukue E, Lee SJ, Kim JA et al. 2005. Analysis of eight capsaicinoids in peppers and pepper-containing foods by high-performance liquid chromatography and liquid chromatography-mass spectrometry. J. Agric. Food Chem. 53:9172–81
    [Google Scholar]
  60. 60.  Lancaster JE, Shaw ML, Joyce MDP, McCallum JA, McManus MT 2000. A novel alliinase from onion roots. Biochemical characterization and cDNA cloning. Plant Physiol 122:1269–79
    [Google Scholar]
  61. 61.  Lang Y, Kisaka H, Sugiyama R, Nomura K, Morita A et al. 2009. Functional loss of pAMT results in biosynthesis of capsinoids, capsaicinoid analogs, in Capsicum annuum cv. CH-19 Sweet. Plant J 59:953–61
    [Google Scholar]
  62. 62.  Leffingwell JC, Alford ED, Leffingwell D 2015. Identification of the volatile constituents of raw pumpkin (Cucurbita pepo L.) by dynamic headspace analyses. Leffingwell Rep 7:1–14
    [Google Scholar]
  63. 63.  León J, Royo J, Vancanneyt G, Sanz C, Silkowski H et al. 2002. Lipoxygenase H1 gene silencing reveals a specific role in supplying fatty acid hydroperoxides for aliphatic aldehyde production. J. Biol. Chem. 277:416–23
    [Google Scholar]
  64. 64.  Li CY, Schilmiller AL, Liu GH, Lee GI, Jayanty S et al. 2005. Role of β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17:971–86
    [Google Scholar]
  65. 65.  Li Y, Colleoni C, Zhang J, Liang Q, Hu Y et al. 2018. Genomic analyses yield markers for identifying agronomically important genes in potato. Mol. Plant 11:473–84
    [Google Scholar]
  66. 66.  Liman ER, Zhang YV, Montell C 2014. Peripheral coding of taste. Neuron 81:984–1000
    [Google Scholar]
  67. 67.  Lin T, Zhu G, Zhang J, Xu X, Yu Q et al. 2014. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46:1220–26
    [Google Scholar]
  68. 68.  Lindemann B 2001. Receptors and transduction in taste. Nature 413:219–25
    [Google Scholar]
  69. 69.  Lou P, Zhao J, He H, Hanhart C, Del Carpio DP et al. 2008. Quantitative trait loci for glucosinolate accumulation in Brassicarapa leaves. New Phytol 179:1017–32
    [Google Scholar]
  70. 70.  Maarse H 1991. Volatile Compounds in Foods and Beverages New York: Dekker
    [Google Scholar]
  71. 71.  Manning K 1985. Food value and chemical composition. The Biology and Technology of the Cultivated Mushroom PB Flegg, DM Spencer, DA Wood 221–30 Chichester, UK: Wiley
    [Google Scholar]
  72. 72.  Mariutto M, Duby F, Adam A, Bureau C, Fauconnier ML et al. 2011. The elicitation of a systemic resistance by Pseudomonas putida BTP1 in tomato involves the stimulation of two lipoxygenase isoforms. BMC Plant Biol 11:29
    [Google Scholar]
  73. 73.  Matsui K, Ujita C, Fujimoto S, Wilkinson J, Hiatt B et al. 2000. Fatty acid 9- and 13-hydroperoxide lyases from cucumber. FEBS Lett 481:183–88
    [Google Scholar]
  74. 74.  Maul F, Sargent SA, Sims CA, Baldwin EA, Balaban MO, Huber DJ 2000. Tomato flavor and aroma quality as affected by storage temperature. J. Food Sci. 65:1228–37
    [Google Scholar]
  75. 75.  Mazourek M, Pujar A, Borovsky Y, Paran I, Mueller L, Jahn MM 2009. A dynamic interface for capsaicinoid systems biology. Plant Physiol 150:1806–21
    [Google Scholar]
  76. 76.  McCallum J, Pither-Joyce M, Shaw M, Kenel F, Davis S et al. 2007. Genetic mapping of sulfur assimilation genes reveals a QTL for onion bulb pungency. Theor. Appl. Genet. 114:815–22
    [Google Scholar]
  77. 77.  McCue KF, Allen PV, Shepherd LV, Blake A, Maccree MM et al. 2007. Potato glycosterol rhamnosyltransferase, the terminal step in triose side-chain biosynthesis. Phytochemistry 68:327–34
    [Google Scholar]
  78. 78.  McCue KF, Allen PV, Shepherd LV, Blake A, Whitworth J et al. 2006. The primary in vivo steroidal alkaloid glucosyltransferase from potato. Phytochemistry 67:1590–97
    [Google Scholar]
  79. 79.  Mie A, Laursen KH, Åberg KM, Forshed J, Lindahl A et al. 2014. Discrimination of conventional and organic white cabbage from a long-term field trial study using untargeted LC-MS-based metabolomics. Anal. Bioanal. Chem. 406:2885–97
    [Google Scholar]
  80. 80.  Moehs CP, Allen PV, Friedman M, Belknap WR 1997. Cloning and expression of solanidine UDP-glucose glucosyltransferase from potato. Plant J 11:227–36
    [Google Scholar]
  81. 81.  Morris WL, Ross HA, Ducreux LJ, Bradshaw JE, Bryan GJ, Taylor MA 2007. Umami compounds are a determinant of the flavor of potato (Solanum tuberosum L.). J. Agric. Food Chem. 55:9627–33
    [Google Scholar]
  82. 82.  Nielsen GS, Poll L 2004. Determination of odor active aroma compounds in freshly cut leek (Allium ampeloprasum var. bulga) and in long-term stored frozen unblanched and blanched leek slices by gas chromatography olfactometry analysis. J. Agric. Food Chem. 52:1642–46
    [Google Scholar]
  83. 83.  Ogawa K, Murota K, Shimura H, Furuya M, Togawa Y et al. 2015. Evidence of capsaicin synthase activity of the Pun1-encoded protein and its role as a determinant of capsaicinoid accumulation in pepper. BMC Plant Biol 15:93
    [Google Scholar]
  84. 84.  Osorio S, Alba R, Damasceno CMB, Lopez-Casado G, Lohse M et al. 2011. Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157:405–25An elegant study demonstrated that the integration of metabolome, transcriptome, and proteome can provide new insights into the metabolic biology of fruit ripening.
    [Google Scholar]
  85. 85.  Ovesná J, Mitrová K, Kučera L 2015. Garlic (A. sativum L.) alliinase gene family polymorphism reflects bolting types and cysteine sulphoxides content. BMC Genet 16:53
    [Google Scholar]
  86. 86.  Padilla G, Cartea ME, Velasco P, de Haro A, Ordas A 2007. Variation of glucosinolates in vegetable crops of Brassicarapa. Phytochemistry 68:536–45
    [Google Scholar]
  87. 87.  Petersen MA, Poll L, Larsen LM 1998. Comparison of volatiles in raw and boiled potatoes using a mild extraction technique combined with GC odour profiling and GC-MS. Food Chem 61:461–66
    [Google Scholar]
  88. 88.  Radovich TJK, Kleinhenz MD, Streeter JG 2005. Irrigation timing relative to head development influences yield components, sugar levels, and glucosinolate concentrations in cabbage. J. Am. Soc. Hortic. Sci. 130:943–49
    [Google Scholar]
  89. 89.  Randle WM, Kopsell DE, Kopsell DA, Snyder RL 1999. Total sulfur and sulfate accumulation in onion is affected by sulfur fertility. J. Plant Nutr. 22:45–51
    [Google Scholar]
  90. 90.  Ritchie MD, Holzinger ER, Li RW, Pendergrass SA, Kim D 2015. Methods of integrating data to uncover genotype–phenotype interactions. Nat. Rev. Genet. 16:85–97
    [Google Scholar]
  91. 91.  Roper SD 2007. Signal transduction and information processing in mammalian taste buds. Pflüg. Arch. 454:759–76
    [Google Scholar]
  92. 92.  Rosa EAS 1997. Glucosinolates from flower buds of portuguese Brassica crops. Phytochemistry 44:1415–19
    [Google Scholar]
  93. 93.  Rosenfeld HJ, Aaby K, Lea P 2002. Influence of temperature and plant density on sensory quality and volatile terpenoids of carrot (Daucus carota L.) root. J. Sci. Food Agric. 82:1384–90
    [Google Scholar]
  94. 94.  Salas JJ, Sánchez CS, García-González DL, Aparicio R 2005. Impact of the suppression of lipoxygenase and hydroperoxide lyase on the quality of the green odor in green leaves. J. Agric. Food Chem. 53:1648–55
    [Google Scholar]
  95. 95.  Sawai S, Ohyama K, Yasumoto S, Seki H, Sakuma T et al. 2014. Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato. Plant Cell 26:3763–74
    [Google Scholar]
  96. 96.  Schonhof I, Krumbein A, Brückner B 2004. Genotypic effects on glucosinolates and sensory properties of broccoli and cauliflower. Nahrung 48:25–33
    [Google Scholar]
  97. 97.  Shang Y, Ma Y, Zhou Y, Zhang H, Duan L et al. 2014. Biosynthesis, regulation, and domestication of bitterness in cucumber. Science 346:1084–88The combination of omics data and biochemistry led to the discovery of the operon-like gene module for cucurbitacin biosynthesis and two master regulators of tissue-specific expression of bitterness in cucumber.
    [Google Scholar]
  98. 98.  Shen J, Tieman D, Jones JB, Taylor MG, Schmelz E et al. 2014. A 13-lipoxygenase, TomloxC, is essential for synthesis of C5 flavour volatiles in tomato. J. Exp. Bot. 65:419–28
    [Google Scholar]
  99. 99.  Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ 2004. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J 40:882–92
    [Google Scholar]
  100. 100.  Sønderby IE, Geu-Flores F, Halkier BA 2010. Biosynthesis of glucosinolates—gene discovery and beyond. Trends Plant Sci 15:283–90
    [Google Scholar]
  101. 101.  Spehr M, Munger SD 2009. Olfactory receptors: G protein–coupled receptors and beyond. J. Neurochem. 109:1570–83
    [Google Scholar]
  102. 102.  Speirs J, Lee E, Holt K, Yong-Duk K, Scott NS et al. 1998. Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol 117:1047–58
    [Google Scholar]
  103. 103.  Spyropoulou EA, Dekker HL, Steemers L, van Maarseveen JH, de Koster CG et al. 2017. Identification and characterization of (3Z):(2E)-hexenal isomerases from cucumber. Front. Plant Sci. 8:1342
    [Google Scholar]
  104. 104.  Tadmor Y, Fridman E, Gur A, Larkov O, Lastochkin E et al. 2002. Identification of malodorous, a wild species allele affecting tomato aroma that was selected against during domestication. J. Agric. Food Chem. 50:2005–9
    [Google Scholar]
  105. 105.  Tandon KS, Baldwin EA, Shewfelt RL 2000. Aroma perception of individual volatile compounds in fresh tomatoes (Lycopersicon esculentum, Mill.) as affected by the medium of evaluation. Postharvest Biol. Technol. 20:261–68
    [Google Scholar]
  106. 106.  Tanner S, Shen ZX, Ng J, Florea L, Guigo R et al. 2007. Improving gene annotation using peptide mass spectrometry. Genome Res 17:231–39
    [Google Scholar]
  107. 107.  Tholl D 2006. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr. Opin. Plant Biol. 9:297–304
    [Google Scholar]
  108. 108.  Tholl D 2015. Biosynthesis and biological functions of terpenoids in plants. Adv. Biochem. Eng. Biotechnol. 148:63–106
    [Google Scholar]
  109. 109.  Tieman D, Bliss P, McIntyre LM, Blandon-Ubeda A, Bies D et al. 2012. The chemical interactions underlying tomato flavor preferences. Curr. Biol. 22:1035–39Flavor preferences are dependent on not only the abundance of odors but also the variation in the rate at which odor intensities occur above a threshold.
    [Google Scholar]
  110. 110.  Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ 2006. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. PNAS 103:8287–92
    [Google Scholar]
  111. 111.  Tieman D, Zeigler M, Schmelz E, Taylor MG, Rushing S et al. 2010. Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62:113–23
    [Google Scholar]
  112. 112.  Tieman D, Zhu G, Resende MFR Jr, Lin T, Nguyen C et al. 2017. A chemical genetic roadmap to improved tomato flavor. Science 355:391–94Consumer taste test, metabolomics, and genomics were integrated to reveal the chemical and genetic basis of tomato flavor.
    [Google Scholar]
  113. 113.  Tikunov Y, Lommen A, de Vos CHR, Verhoeven HA, Bino RJ et al. 2005. A novel approach for nontargeted data analysis for metabolomics. Large-scale profiling of tomato fruit volatiles. Plant Physiol 139:1125–37
    [Google Scholar]
  114. 114.  Tsai SY, Wu TP, Huang SJ, Mau JL 2007. Nonvolatile taste components of Agaricus bisporus harvested at different stages of maturity. Food Chem 103:1457–64
    [Google Scholar]
  115. 115.  Urano Y, Manabe T, Noji M, Saito K 2000. Molecular cloning and functional characterization of cDNAs encoding cysteine synthase and serine acetyltransferase that may be responsible for high cellular cysteine content in Allium tuberosum. Gene 257:269–77
    [Google Scholar]
  116. 116.  Urbanczyk-Wochniak E, Luedemann A, Kopka J, Selbig J, Roessner-Tunali U et al. 2003. Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Rep 4:989–93
    [Google Scholar]
  117. 117.  Vallejo F, Tomás-Barberán F, Garcia-Viguera C 2003. Health-promoting compounds in broccoli as influenced by refrigerated transport and retail sale period. J. Agric. Food Chem. 51:3029–34
    [Google Scholar]
  118. 118.  Van Damme EJ, Smeets K, Torrekens S, Van Leuven F, Peumans WJ 1992. Isolation and characterization of alliinase cDNA clones from garlic (Allium sativum L.) and related species. Eur. J. Biochem. 209:751–57
    [Google Scholar]
  119. 119.  van Doorn HE, van der Kruk GC, van Holst G-J, Raaijmakers-Ruijs NCME, Postma E et al. 1998. The glucosinolates sinigrin and progoitrin are important determinants for taste preference and bitterness of brussels sprouts. J. Sci. Food Agric. 78:30–38
    [Google Scholar]
  120. 120.  Venkateshwarlu C, Chandravadana MV, Tewari RP 1999. Volatile flavour components of some edible mushrooms (Basidiomycetes). Flavour Frag. J. 14:191–94
    [Google Scholar]
  121. 121.  Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC 2005. ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612–24
    [Google Scholar]
  122. 122.  Vogel JT, Tieman DM, Sims CA, Odabasi AZ, Clark DG, Klee HJ 2010. Carotenoid content impacts flavor acceptability in tomato (Solanum lycopersicum). J. Sci. Food Agric. 90:2233–40
    [Google Scholar]
  123. 123.  Wei G, Tian P, Zhang FX, Qin H, Miao H et al. 2016. Integrative analyses of nontargeted volatile profiling and transcriptome data provide molecular insight into VOC diversity in cucumber plants (Cucumis sativus). Plant Physiol 172:603–18
    [Google Scholar]
  124. 124.  Widder S, Sabater Lüntzel C, Dittner T, Pickenhagen W 2000. 3-Mercapto-2-methylpentan-1-ol, a new powerful aroma compound. J. Agric. Food Chem. 48:418–23
    [Google Scholar]
  125. 125.  Yahyaa M, Bar E, Dubey NK, Meir A, Davidovich-Rikanati R et al. 2013. Formation of norisoprenoid flavor compounds in carrot (Daucus carota L.) roots: characterization of a cyclic-specific carotenoid cleavage dioxygenase 1 gene. J. Agric. Food Chem. 61:12244–52
    [Google Scholar]
  126. 126.  Yahyaa M, Tholl D, Cormier G, Jensen R, Simon PW, Ibdah M 2015. Identification and characterization of terpene synthases potentially involved in the formation of volatile terpenes in carrot (Daucus carota L.) roots. J. Agric. Food Chem. 63:4870–78
    [Google Scholar]
  127. 127.  Yin L, Chen H, Cao B, Lei J, Chen G 2017. Molecular characterization of MYB28 involved in aliphatic glucosinolate biosynthesis in Chinese kale (Brassica oleracea var. alboglabra Bailey). Front. Plant Sci 8:1083
    [Google Scholar]
  128. 128.  Yoshimoto N, Onuma M, Sugino Y, Nakabayashi R, Imai S et al. 2015. Identification of a flavin-containing S-oxygenating monooxygenase involved in alliin biosynthesis in garlic. Plant J 83:941–51
    [Google Scholar]
  129. 129.  Yoshimoto N, Yabe A, Sugino Y, Murakami S, Sai-Ngam N et al. 2015. Garlic γ-glutamyl transpeptidases that catalyze deglutamylation of biosynthetic intermediate of alliin. Front. Plant Sci. 5:758
    [Google Scholar]
  130. 130.  Zang YX, Kim HU, Kim JA, Lim MH, Jin M et al. 2009. Genome-wide identification of glucosinolate synthesis genes in Brassicarapa. FEBS J 276:3559–74
    [Google Scholar]
  131. 131.  Zanor MI, Rambla JL, Chaib J, Steppa A, Medina A et al. 2009. 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. 60:2139–54
    [Google Scholar]
  132. 132.  Zhang B, Tieman DM, Jiao C, Xu Y, Chen K et al. 2016. Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation. PNAS 113:12580–85An exciting study revealed that methylation of ripening-related genes in low-temperature storage leads to reduced flavor quality.
    [Google Scholar]
  133. 133.  Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I et al. 2003. The receptors for mammalian sweet and umami taste. Cell 115:255–66
    [Google Scholar]
  134. 134.  Zhou Y, Ma Y, Zeng J, Duan L, Xue X et al. 2016. Convergence and divergence of bitterness biosynthesis and regulation in Cucurbitaceae. Nat. Plants 2:16183
    [Google Scholar]
  135. 135.  Zhu G, Wang S, Huang Z, Zhang S, Liao Q et al. 2018. Rewiring of the fruit metabolome in tomato breeding. Cell 172:249–61.e12Multi-omics analyses revealed how the appearance- and taste-oriented breeding process modulates the metabolic makeup of the tomato.
    [Google Scholar]
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