Fruit secondary metabolites play pivotal roles in plant evolution by deterring herbivores and attracting seed dispersers. However, the mechanisms by which these compounds evolve and drive diversification in citrus remain poorly understood. In this study, we demonstrate that the emergence of the bitter compound neohesperidoside (Neo) has contributed to citrus dissemination by enhancing defense against biotic stresses. Targeted metabolomic analyses revealed that Neo accumulation emerged in early-diverging citrus, whereas the presence of its non-bitter counterpart rutinoside (Rut) can be traced back to Citrus-related species. Comparative genomics and enzyme functional assays revealed that Neo biosynthesis arose from duplication of two di-glucosyltransferase genes, CmdGlcT-1 and UGT79B203, in early-diverging citrus, followed by neofunctionalization into enzymes of Cm1,2RhaT and UGT79B202, capable of synthesizing Neo. A structurally conserved amino acid residue, corresponding to Phe195 in Cm1,2RhaT and Leu201 in UGT79B203, was identified as essential for this functional shift. Compared to Rut, Neo exhibited stronger antifungal and anti-feeding effects, suggesting its potential role in enhancing biotic defense, which may have contributed to the broader geographical distribution of early-diverging citrus species. These findings provide new insights into the evolutionary origin of citrus bitterness and highlight the adaptive role of specialized metabolites in mediating plant-environment interactions.
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