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

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