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Research ArticleBIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES
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Enhanced Levels of the Aroma and Flavor Compound S-Linalool by Metabolic Engineering of the Terpenoid Pathway in Tomato Fruits

Efraim Lewinsohn, Fernond Schalechet, Jack Wilkinson, Kenji Matsui, Yaakov Tadmor, Kyoung-Hee Nam, Orit Amar, Elena Lastochkin, Olga Larkov, Uzi Ravid, William Hiatt, Shimon Gepstein, Eran Pichersky
Efraim Lewinsohn
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Fernond Schalechet
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Jack Wilkinson
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Kenji Matsui
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Yaakov Tadmor
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Kyoung-Hee Nam
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Orit Amar
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Elena Lastochkin
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Olga Larkov
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Uzi Ravid
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William Hiatt
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Shimon Gepstein
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Eran Pichersky
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Published November 2001. DOI: https://doi.org/10.1104/pp.010293

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    Fig. 1.

    Diversion of the existing plastid terpenoid pathway leading to carotenoids into the production ofS-linalool in ripening tomatoes by the expression of theC. breweri LIS transgene. DOXP, Deoxy-d-xylulose 5-phosphate; GPPS, geranyl diphosphate synthase; GGPPS, geranylgeranyl diphosphate synthase.

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    Fig. 2.

    Presence of S-linalool and 8-hydroxylinalool in LIS-transgenic tomato fruits. Fresh tomato fruits were extracted with tert-butyl methyl ether (MTBE) and analyzed by gas chromatography-MS using an HP5 column as described in “Materials and Methods.” The trace obtained for them/z = 93 typical for linalool and other monoterpene derivatives is shown. Top, An extract from a typical transgenic CB3 fruit; bottom, non-transformed control.

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    Fig. 3.

    Enantiomeric composition of the linalool accumulated in LIS-transgenic tomatoes. The same extract utilized in Figure 2 was analyzed on a chiral Restek Rt-βDEXsm column (top). The separation of a racemic (synthetic) mixture of linalool under the same conditions is shown (bottom).

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    Fig. 4.

    Accumulation of S-linalool (squares) and 8-hydroxylinalool (circles) in transgenic and control tomatoes during fruit maturation. A, CB3 variety; B, UC82B variety. White symbols represent transgenic plants and black symbols represent non-transformed controls. Each data point represents an average and these of data obtained from two to seven different fruits analyzed separately, but originating from the same plants.

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    Table I.

    Volatiles in LIS-transgenic and control tomato fruits

    Volatile DetectedDetection MethodUC82BCB3
    TransformedControlTransformedControl
    ng g−1/fresh wt
    Aliphatic acids, aldehydes, and alcohols
     Pentanoic acidRetention time (RT), mass spectrometry (MS)20  (0–61)12  (0–20)
     Hexanoic acidRT, MS48  (0–103)Traces66  (0–103)Traces
     DecanolRT, MS25  (0–76)2.8  (0–5)––
     Nonanoic acidRT, MSTraces2  (0–5)5  (0–15)8  (0–13)
     2,4-HeptadienalRT, MS––Traces8  (0–25)
     Dodecanoic acidRT, MS27  (10–57)10  (8–14)Traces16  (0–25)
     Tetradecanoic acidRT, MS24  (0–58)Traces17  (0–30)28  (15–40)
    Oxygenated and nonoxygenated monoterpenes
     MyrceneRT, MS20  (0–60)10  (0–29)17  (0–51)Traces
     LimoneneRT, MS97  (64–130)1  (0–2)––
     β-OcimeneRT, MS20  (0–61)Traces––
     γ-TerpineneRT, MS7  (0–22)Traces––
     TerpinoleneRT, MS11  (0–34)Traces––
     Linalool 1-a RT, MS 187  (123–258) 0 456  (165–833) 0
     GeranialRT, MS4  (0–11)1  (0–2.5)0.5  (0–2)4  (2–6)
     AcetoxylinaloolMS5  (0–14)0––
     8-Hydroxylinalool RT, MS 113  (94–147) 0 345  (199–504) 0
    Phenolic derivatives
     BenzaldehydeRT, MS13  (0–39)Traces8  (0–25)Traces
     Benzyl alcoholRT, MS96  (48–187)50  (36–71)167  (120–217)77  (56–105)
     GuaiacolRT, MS128  (54–178)43  (0–65)537  (54–1026)252  (16–391)
     2-Phenylethyl alcoholRT, MS165  (40–307)120  (100–134)206  (133–249)123  (80–200)
     Benzoic acidRT, MS38  (0–101)38  (6–100)5  (0–15)7  (0–22)
     Methyl salicylateRT, MS167  (50–249)58  (0–94)205  (129–317)173  (53–251)
     4-VinylphenolRT, MS147  (55–310)75  (35–145)179  (139–254)87  (44–115)
     4-Vinyl 2-methoxyphenolMS130  (0–282)92  (29–195)297  (112–659)77  (47–96)
     Salicylic acidMS––2  (0–7)Traces
     EugenolRT, MS45  (0–91)33  (22–50)28  (24–34)16  (11–19)
     VanillinRT, MS3  (0–8)2  (0–4)4  (0–11)7  (4–8)
     2-MethoxyhydroquinoneMS––7  (0–20)17  (0–36)
     4-Methoxy-2-methylphenolMS7  (0–12)10  (9–13)––
     AcetovanilloneRT, MS––30  (19–39)28  (18–42)
     Vanillic acidMS––10  (7–23)Traces
     BenzophenoneMS15  (0–32)5  (0–7)14  (0–31)7  (6–7)
     Homovanillic acidMS26  (0–54)15  (8–28)48  (22–94)18  (0–34)
     MethylbenzophenoneMS67  (51–94)16  (10–21)67  (42–87)48  (32–65)
     Coumaric acidMS––Traces13  (0–38)
    Nor-isoprenes
     GeranylacetoneRT, MSTraces5  (3–9)Traces3  (0–7)
     β-IononeMS––Traces3  (0–10)
     6-Methyl-2-hepten-1-oneRT, MSTraces6  (0–17)––
    Other
     3-(Methylthio)-1-propanolRT, MS––44  (25–81)59  (17–129)
     2-IsobutylthiazoleMSTraces13  (0–22)Traces22  (18–28)
     FuraneolRT, MS5  (0–16)33  (22–44)––
     Butyl butyrateMS109  (91–128)52  (49–56)46  (0–98)47  (29–64)
     DihydroactindiolideMS7  (0–11)10  (9–13)Traces6  (4–7)
     Unknown 1MS60  (0–112)0425  (0–922)0
     Unknown 2MS135  (37–290)0––

    Means and ranges of three independent determinations are shown. One fruit from three plants, each originating from an independent transformation event, was analyzed for each variety.

      • ↵F1-a  Bold indicates identified linalool and linalool derivatives.

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      Table II.

      Levels of S-linalool and other terpenoids in LIS-transgenic and control ripe tomato fruits

      Plant Lineγ-Tocopherolα-TocopherolLuteinLycopeneβ-CaroteneS-Linalool
      μg g−1 fresh wt (± se)
      CB3 LIS-transgenic10.45  (0.31)8.49  (0.82)2.28  (0.24)66.51  (5.50)5.53  (0.56)0.31  (0.01)
      CB3 Controls11.07  (0.09)7.02  (0.09)1.99  (0.21)63.75  (14.91)3.00  (0.48)0.00  (0.00)
      UC82B LIS-transgenic11.83  (0.34)7.45  (0.75)1.62  (0.50)76.60  (1.11)3.35  (0.60)0.25  (0.05)
      UC82B Controls10.40  (0.98)6.40  (1.82)2.15  (0.13)91.02  (24.63)4.80  (0.14)0.00  (0.00)

      Transformation was verified by PCR. Means and se of two to five independent determinations from one fruit from plants containing high S-linalool levels that originated in one transformation event for each variety and compared with controls.

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      Enhanced Levels of the Aroma and Flavor Compound S-Linalool by Metabolic Engineering of the Terpenoid Pathway in Tomato Fruits
      Efraim Lewinsohn, Fernond Schalechet, Jack Wilkinson, Kenji Matsui, Yaakov Tadmor, Kyoung-Hee Nam, Orit Amar, Elena Lastochkin, Olga Larkov, Uzi Ravid, William Hiatt, Shimon Gepstein, Eran Pichersky
      Plant Physiology Nov 2001, 127 (3) 1256-1265; DOI: 10.1104/pp.010293

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      Enhanced Levels of the Aroma and Flavor Compound S-Linalool by Metabolic Engineering of the Terpenoid Pathway in Tomato Fruits
      Efraim Lewinsohn, Fernond Schalechet, Jack Wilkinson, Kenji Matsui, Yaakov Tadmor, Kyoung-Hee Nam, Orit Amar, Elena Lastochkin, Olga Larkov, Uzi Ravid, William Hiatt, Shimon Gepstein, Eran Pichersky
      Plant Physiology Nov 2001, 127 (3) 1256-1265; DOI: 10.1104/pp.010293
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