Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs

Daniela Lai, Martina Pičmanová, Maher Abou Hachem, Mohammed Saddik Motawia, Carl Erik Olsen, Birger Lindberg Møller, Fred Rook, Adam M. Takos

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    Abstract

    Flowers and leaves of Lotus japonicus contain α-, β-, and γ-hydroxynitrile glucoside (HNG) defense compounds, which are bioactivated by β-glucosidase enzymes (BGDs). The α-HNGs are referred to as cyanogenic glucosides because their hydrolysis upon tissue disruption leads to release of toxic hydrogen cyanide gas, which can deter herbivore feeding. BGD2 and BGD4 are HNG metabolizing BGD enzymes expressed in leaves. Only BGD2 is able to hydrolyse the α-HNGs. Loss of function mutants of BGD2 are acyanogenic in leaves but fully retain cyanogenesis in flowers pointing to the existence of an alternative cyanogenic BGD in flowers. This enzyme, named BGD3, is identified and characterized in this study. Whereas all floral tissues contain α-HNGs, only those tissues in which BGD3 is expressed, the keel and the enclosed reproductive organs, are cyanogenic. Biochemical analysis, active site architecture molecular modelling, and the observation that L. japonicus accessions lacking cyanogenic flowers contain a non-functional BGD3 gene, all support the key role of BGD3 in floral cyanogenesis. The nectar of L. japonicus flowers was also found to contain HNGs and additionally their diglycosides. The observed specialisation in HNG based defence in L. japonicus flowers is discussed in the context of balancing the attraction of pollinators with the protection of reproductive structures against herbivores.
    Original languageEnglish
    JournalPLANT MOLECULAR BIOLOGY
    Volume89
    Issue number1-2
    Pages (from-to)21-34
    Number of pages14
    ISSN0167-4412
    DOIs
    Publication statusPublished - 2015

    Keywords

    • Cyanogenesis defense
    • Florivory
    • Hydroxynitrile glucosides
    • Lotus japonicus
    • Toxic nectar
    • β-Glucosidase

    Cite this

    Lai, Daniela ; Pičmanová, Martina ; Abou Hachem, Maher ; Motawia, Mohammed Saddik ; Olsen, Carl Erik ; Møller, Birger Lindberg ; Rook, Fred ; Takos, Adam M. / Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs. In: PLANT MOLECULAR BIOLOGY. 2015 ; Vol. 89, No. 1-2. pp. 21-34.
    @article{66011b332ae94f7bbf552fe766438ccb,
    title = "Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs",
    abstract = "Flowers and leaves of Lotus japonicus contain α-, β-, and γ-hydroxynitrile glucoside (HNG) defense compounds, which are bioactivated by β-glucosidase enzymes (BGDs). The α-HNGs are referred to as cyanogenic glucosides because their hydrolysis upon tissue disruption leads to release of toxic hydrogen cyanide gas, which can deter herbivore feeding. BGD2 and BGD4 are HNG metabolizing BGD enzymes expressed in leaves. Only BGD2 is able to hydrolyse the α-HNGs. Loss of function mutants of BGD2 are acyanogenic in leaves but fully retain cyanogenesis in flowers pointing to the existence of an alternative cyanogenic BGD in flowers. This enzyme, named BGD3, is identified and characterized in this study. Whereas all floral tissues contain α-HNGs, only those tissues in which BGD3 is expressed, the keel and the enclosed reproductive organs, are cyanogenic. Biochemical analysis, active site architecture molecular modelling, and the observation that L. japonicus accessions lacking cyanogenic flowers contain a non-functional BGD3 gene, all support the key role of BGD3 in floral cyanogenesis. The nectar of L. japonicus flowers was also found to contain HNGs and additionally their diglycosides. The observed specialisation in HNG based defence in L. japonicus flowers is discussed in the context of balancing the attraction of pollinators with the protection of reproductive structures against herbivores.",
    keywords = "Cyanogenesis defense, Florivory, Hydroxynitrile glucosides, Lotus japonicus, Toxic nectar, β-Glucosidase",
    author = "Daniela Lai and Martina Pičmanov{\'a} and {Abou Hachem}, Maher and Motawia, {Mohammed Saddik} and Olsen, {Carl Erik} and M{\o}ller, {Birger Lindberg} and Fred Rook and Takos, {Adam M.}",
    year = "2015",
    doi = "10.1007/s11103-015-0348-4",
    language = "English",
    volume = "89",
    pages = "21--34",
    journal = "Plant Molecular Biology",
    issn = "0167-4412",
    publisher = "Springer Netherlands",
    number = "1-2",

    }

    Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs. / Lai, Daniela; Pičmanová, Martina; Abou Hachem, Maher ; Motawia, Mohammed Saddik; Olsen, Carl Erik; Møller, Birger Lindberg; Rook, Fred; Takos, Adam M.

    In: PLANT MOLECULAR BIOLOGY, Vol. 89, No. 1-2, 2015, p. 21-34.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs

    AU - Lai, Daniela

    AU - Pičmanová, Martina

    AU - Abou Hachem, Maher

    AU - Motawia, Mohammed Saddik

    AU - Olsen, Carl Erik

    AU - Møller, Birger Lindberg

    AU - Rook, Fred

    AU - Takos, Adam M.

    PY - 2015

    Y1 - 2015

    N2 - Flowers and leaves of Lotus japonicus contain α-, β-, and γ-hydroxynitrile glucoside (HNG) defense compounds, which are bioactivated by β-glucosidase enzymes (BGDs). The α-HNGs are referred to as cyanogenic glucosides because their hydrolysis upon tissue disruption leads to release of toxic hydrogen cyanide gas, which can deter herbivore feeding. BGD2 and BGD4 are HNG metabolizing BGD enzymes expressed in leaves. Only BGD2 is able to hydrolyse the α-HNGs. Loss of function mutants of BGD2 are acyanogenic in leaves but fully retain cyanogenesis in flowers pointing to the existence of an alternative cyanogenic BGD in flowers. This enzyme, named BGD3, is identified and characterized in this study. Whereas all floral tissues contain α-HNGs, only those tissues in which BGD3 is expressed, the keel and the enclosed reproductive organs, are cyanogenic. Biochemical analysis, active site architecture molecular modelling, and the observation that L. japonicus accessions lacking cyanogenic flowers contain a non-functional BGD3 gene, all support the key role of BGD3 in floral cyanogenesis. The nectar of L. japonicus flowers was also found to contain HNGs and additionally their diglycosides. The observed specialisation in HNG based defence in L. japonicus flowers is discussed in the context of balancing the attraction of pollinators with the protection of reproductive structures against herbivores.

    AB - Flowers and leaves of Lotus japonicus contain α-, β-, and γ-hydroxynitrile glucoside (HNG) defense compounds, which are bioactivated by β-glucosidase enzymes (BGDs). The α-HNGs are referred to as cyanogenic glucosides because their hydrolysis upon tissue disruption leads to release of toxic hydrogen cyanide gas, which can deter herbivore feeding. BGD2 and BGD4 are HNG metabolizing BGD enzymes expressed in leaves. Only BGD2 is able to hydrolyse the α-HNGs. Loss of function mutants of BGD2 are acyanogenic in leaves but fully retain cyanogenesis in flowers pointing to the existence of an alternative cyanogenic BGD in flowers. This enzyme, named BGD3, is identified and characterized in this study. Whereas all floral tissues contain α-HNGs, only those tissues in which BGD3 is expressed, the keel and the enclosed reproductive organs, are cyanogenic. Biochemical analysis, active site architecture molecular modelling, and the observation that L. japonicus accessions lacking cyanogenic flowers contain a non-functional BGD3 gene, all support the key role of BGD3 in floral cyanogenesis. The nectar of L. japonicus flowers was also found to contain HNGs and additionally their diglycosides. The observed specialisation in HNG based defence in L. japonicus flowers is discussed in the context of balancing the attraction of pollinators with the protection of reproductive structures against herbivores.

    KW - Cyanogenesis defense

    KW - Florivory

    KW - Hydroxynitrile glucosides

    KW - Lotus japonicus

    KW - Toxic nectar

    KW - β-Glucosidase

    U2 - 10.1007/s11103-015-0348-4

    DO - 10.1007/s11103-015-0348-4

    M3 - Journal article

    VL - 89

    SP - 21

    EP - 34

    JO - Plant Molecular Biology

    JF - Plant Molecular Biology

    SN - 0167-4412

    IS - 1-2

    ER -