Whitefly hijacks a plant detoxification gene that neutralizes plant toxins

Jixing Xia, Zhaojiang Guo, Zezhong Yang, Haolin Han, Shaoli Wang, Haifeng Xu, Xin Yang, Fengshan Yang, Qingjun Wu, Wen Xie, Xuguo Zhou, Wannes Dermauw, Ted C.J. Turlings, Youjun Zhang

Research output: Contribution to journalArticlepeer-review

90 Scopus citations

Abstract

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.

Original languageEnglish
Pages (from-to)1693-1705.e17
JournalCell
Volume184
Issue number7
DOIs
StatePublished - Apr 1 2021

Bibliographical note

Funding Information:
We thank Prof. Xia Cui and Haijing Wang from the Sino-Dutch Joint Laboratory of Horticultural Genomics in our institute for the assistance with the UPLC-QTOF/MS experiment. We also thank all students in our laboratory who helped with dissecting whitefly gut tissues. This research was supported by the National Key R & D Program of China (2019YFD1002100), the National Natural Science Foundation of China (31420103919, 31801747, 32022074), the China Agricultural Research System (CARS-24-C-02), the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables, and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-IVFCAAS). The contribution by T.C.J.T. was supported by European Research Council advanced grant 788949. J.X. Z.G. T.C.J.T. and Y.Z. designed the research. J.X. Z.G. Z.Y. H.H. S.W. H.X. X.Y. F.Y. Q.W. and W.X. performed the experiments. J.X. Z.G. and Z.Y. analyzed the data. J.X. Z.G. X.Z. W.D. T.C.J.T. and Y.Z. wrote and revised the manuscript. The authors declare that a patent has been filed to the China National Intellectual Property Administration (application no. 202010287105.5).

Publisher Copyright:
© 2021 Elsevier Inc.

Keywords

  • Bemisia tabaci
  • co-evolution
  • detoxification
  • horizontal gene transfer
  • insect-plant interaction
  • pest control
  • phenolic glucoside malonyltransferase
  • plant secondary metabolite
  • tomato

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology (all)

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