Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants

A. Aharoni, A.P. Giri, S. Deuerlein, F.C. Griepink, W.J. de Kogel, F.W.A. Verstappen, H.A. Verhoeven, M.A. Jongsma, W. Schwab, H.J. Bouwmeester

    Research output: Contribution to journalArticleAcademicpeer-review

    349 Citations (Scopus)

    Abstract

    Volatile components, such as terpenoids, are emitted from aerial parts of plants and play a major role in the interaction between plants and their environment. Analysis of the composition and emission pattern of volatiles in the model plant Arabidopsis showed that a range of volatile components are released, primarily from flowers. Most of the volatiles detected were monoterpenes and sesquiterpenes, which in contrast to other volatiles showed a diurnal emission pattern. The active terpenoid metabolism in wild-type Arabidopsis provoked us to conduct an additional set of experiments in which transgenic Arabidopsis overexpressing two different terpene synthases were generated. Leaves of transgenic plants constitutively expressing a dual linalool/nerolidol synthase in the plastids (FaNES1) produced linalool and its glycosylated and hydroxylated derivatives. The sum of glycosylated components was in some of the transgenic lines up to 40- to 60-fold higher than the sum of the corresponding free alcohols. Surprisingly, we also detected the production and emission of nerolidol, albeit at a low level, suggesting that a small pool of its precursor farnesyl diphosphate is present in the plastids. Transgenic lines with strong transgene expression showed growth retardation, possibly as a result of the depletion of isoprenoid precursors in the plastids. In dual-choice assays with Myzus persicae, the FaNES1-expressing lines significantly repelled the aphids. Overexpression of a typical cytosolic sesquiterpene synthase resulted in the production of only trace amounts of the expected sesquiterpene, suggesting tight control of the cytosolic pool of farnesyl diphosphate, the precursor for sesquiterpenoid biosynthesis. This study further demonstrates the value of Arabidopsis for studies of the biosynthesis and ecological role of terpenoids and provides new insights into their metabolism in wild-type and transgenic plants
    Original languageEnglish
    Pages (from-to)2866-2884
    JournalThe Plant Cell
    Volume15
    Issue number12
    DOIs
    Publication statusPublished - 2003

    Fingerprint

    Genetically Modified Plants
    Terpenes
    Arabidopsis
    terpenoids
    sesquiterpenoids
    Plastids
    Sesquiterpenes
    genetically modified organisms
    plastids
    Aphids
    metabolism
    linalool
    transgenic plants
    Aerial Plant Components
    biosynthesis
    Monoterpenes
    isoprenoids
    Myzus persicae
    Transgenes
    monoterpenoids

    Keywords

    • sesquiterpene cyclase gene
    • linalool synthase gene
    • functional expression
    • monoterpene biosynthesis
    • isoprenoid biosynthesis
    • diphosphate synthase
    • cdna isolation
    • s-linalool
    • glandular trichomes
    • thaliana

    Cite this

    Aharoni, A., Giri, A. P., Deuerlein, S., Griepink, F. C., de Kogel, W. J., Verstappen, F. W. A., ... Bouwmeester, H. J. (2003). Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants. The Plant Cell, 15(12), 2866-2884. https://doi.org/10.1105/tpc.016253
    Aharoni, A. ; Giri, A.P. ; Deuerlein, S. ; Griepink, F.C. ; de Kogel, W.J. ; Verstappen, F.W.A. ; Verhoeven, H.A. ; Jongsma, M.A. ; Schwab, W. ; Bouwmeester, H.J. / Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants. In: The Plant Cell. 2003 ; Vol. 15, No. 12. pp. 2866-2884.
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    author = "A. Aharoni and A.P. Giri and S. Deuerlein and F.C. Griepink and {de Kogel}, W.J. and F.W.A. Verstappen and H.A. Verhoeven and M.A. Jongsma and W. Schwab and H.J. Bouwmeester",
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    Aharoni, A, Giri, AP, Deuerlein, S, Griepink, FC, de Kogel, WJ, Verstappen, FWA, Verhoeven, HA, Jongsma, MA, Schwab, W & Bouwmeester, HJ 2003, 'Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants', The Plant Cell, vol. 15, no. 12, pp. 2866-2884. https://doi.org/10.1105/tpc.016253

    Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants. / Aharoni, A.; Giri, A.P.; Deuerlein, S.; Griepink, F.C.; de Kogel, W.J.; Verstappen, F.W.A.; Verhoeven, H.A.; Jongsma, M.A.; Schwab, W.; Bouwmeester, H.J.

    In: The Plant Cell, Vol. 15, No. 12, 2003, p. 2866-2884.

    Research output: Contribution to journalArticleAcademicpeer-review

    TY - JOUR

    T1 - Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants

    AU - Aharoni, A.

    AU - Giri, A.P.

    AU - Deuerlein, S.

    AU - Griepink, F.C.

    AU - de Kogel, W.J.

    AU - Verstappen, F.W.A.

    AU - Verhoeven, H.A.

    AU - Jongsma, M.A.

    AU - Schwab, W.

    AU - Bouwmeester, H.J.

    PY - 2003

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    AB - Volatile components, such as terpenoids, are emitted from aerial parts of plants and play a major role in the interaction between plants and their environment. Analysis of the composition and emission pattern of volatiles in the model plant Arabidopsis showed that a range of volatile components are released, primarily from flowers. Most of the volatiles detected were monoterpenes and sesquiterpenes, which in contrast to other volatiles showed a diurnal emission pattern. The active terpenoid metabolism in wild-type Arabidopsis provoked us to conduct an additional set of experiments in which transgenic Arabidopsis overexpressing two different terpene synthases were generated. Leaves of transgenic plants constitutively expressing a dual linalool/nerolidol synthase in the plastids (FaNES1) produced linalool and its glycosylated and hydroxylated derivatives. The sum of glycosylated components was in some of the transgenic lines up to 40- to 60-fold higher than the sum of the corresponding free alcohols. Surprisingly, we also detected the production and emission of nerolidol, albeit at a low level, suggesting that a small pool of its precursor farnesyl diphosphate is present in the plastids. Transgenic lines with strong transgene expression showed growth retardation, possibly as a result of the depletion of isoprenoid precursors in the plastids. In dual-choice assays with Myzus persicae, the FaNES1-expressing lines significantly repelled the aphids. Overexpression of a typical cytosolic sesquiterpene synthase resulted in the production of only trace amounts of the expected sesquiterpene, suggesting tight control of the cytosolic pool of farnesyl diphosphate, the precursor for sesquiterpenoid biosynthesis. This study further demonstrates the value of Arabidopsis for studies of the biosynthesis and ecological role of terpenoids and provides new insights into their metabolism in wild-type and transgenic plants

    KW - sesquiterpene cyclase gene

    KW - linalool synthase gene

    KW - functional expression

    KW - monoterpene biosynthesis

    KW - isoprenoid biosynthesis

    KW - diphosphate synthase

    KW - cdna isolation

    KW - s-linalool

    KW - glandular trichomes

    KW - thaliana

    U2 - 10.1105/tpc.016253

    DO - 10.1105/tpc.016253

    M3 - Article

    VL - 15

    SP - 2866

    EP - 2884

    JO - The Plant Cell

    JF - The Plant Cell

    SN - 1040-4651

    IS - 12

    ER -