Whitefly hijacks a plant detoxification gene that neutralizes plant toxins

• Published in: Cell 2021-04, Vol.184 (7), p.1693-1705.e17
• Main Authors: Xia, Jixing, Guo, Zhaojiang, Yang, Zezhong, Han, Haolin, Wang, Shaoli, Xu, Haifeng, Yang, Xin, Yang, Fengshan, Wu, Qingjun, Xie, Wen, Zhou, Xuguo, Dermauw, Wannes, Turlings, Ted C.J., Zhang, Youjun
• Format: Article
• Language: English
• Subjects: Animals; Bemisia tabaci; co-evolution; detoxification; Gene Transfer, Horizontal; Genes, Plant; Glucosides - chemistry; Glucosides - metabolism; Hemiptera - genetics; Hemiptera - physiology; Herbivory; horizontal gene transfer; Insect Proteins - antagonists & inhibitors; Insect Proteins - classification; Insect Proteins - genetics; Insect Proteins - metabolism; insect-plant interaction; Intestinal Mucosa - metabolism; Lycopersicon esculentum - genetics; Lycopersicon esculentum - metabolism; Malonyl Coenzyme A - metabolism; pest control; phenolic glucoside malonyltransferase; Phylogeny; plant secondary metabolite; Plants, Genetically Modified - genetics; Plants, Genetically Modified - metabolism; RNA Interference; RNA, Double-Stranded - metabolism; tomato; Toxins, Biological - chemistry; Toxins, Biological - metabolism
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2021.02.014

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. [Display omitted] •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 The cosmopolitan agricultural pest Bemisia tabaci has acquired a plant-derived gene through a plant-to-insect horizontal gene transfer event. This acquired gene allows whiteflies to detoxify plant defense compounds and continue to feed on their plant hosts.