[Cell] Whitefly hijacks a plant detoxification gene that neutralizes plant toxins

Plants protect themselves with a vast array of toxic secondary metabolites, yet most plants serve as food for insects. The evolutionary processes that allow herbivorous insects to resist plant defenses remain largely unknown. The whitefly Bemisia tabaci is a cosmopolitan, highly polyphagous agricultural pest that vectors several serious plant pathogenic viruses and is an excellent model to probe the molecular mechanisms involved in overcoming plant defenses. Here, we show that, through an exceptional horizontal gene transfer event, the whitefly has acquired the plant-derived phenolic glucoside malonyltransferase gene BtPMaT1. This gene enables whiteflies to neutralize phenolic glucosides. This was confirmed by genetically transforming tomato plants to produce small interfering RNAs that silence BtPMaT1, thus impairing the whiteflies’ detoxification ability. These findings reveal an evolutionary scenario whereby herbivores harness the genetic toolkit of their host plants to develop resistance to plant defenses and how this can be exploited for crop protection.

 • Many plants contain phenolic glycosides that are toxic for insect herbivores
 • Whitefly carries a plant-derived phenolic glucoside malonyltransferase gene BtPMaT1
 • BtPMaT1 enables whiteflies to neutralize phenolic glycosides in host plants
 • Plant-mediated silencing of BtPMaT1 confers tomato full resistance to whiteflies

Schematic overview of how the acquisition of the plant gene BtPMaT1 empowers the whitefly B. tabaci to neutralize plant phenolic glycosides

BtPMaT1 is a phenolic glucoside malonyltransferase gene horizontally transferred from plants to B. tabaci. In B. tabaci, malonylation of phenolic glycosides is catalyzed by BtPMaT1 and neutralizes plant-produced phenolic glycosides. These findings introduce a paradigm by which herbivorous insects can acquire a weapon from their host plants to conversely thwart the plants’ chemical defenses, reminiscent of the wisdom of the ancient Chinese philosopher Han Fei, “Attack your shield with your spear.” Silencing experiments show that the same wisdom can be applied to combat the global pest.