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

doi:10.1016/j.cell.2021.02.014

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

Entomology

Research output: Contribution to journal › Article › peer-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 language	English
Pages (from-to)	1693-1705.e17
Journal	Cell
Volume	184
Issue number	7
DOIs	https://doi.org/10.1016/j.cell.2021.02.014
State	Published - 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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10.1016/j.cell.2021.02.014

Cite this

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title = "Whitefly hijacks a plant detoxification gene that neutralizes plant toxins",

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{\textquoteright} 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.",

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

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

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: {\textcopyright} 2021 Elsevier Inc.",

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AU - Xia, Jixing

AU - Guo, Zhaojiang

AU - Yang, Zezhong

AU - Han, Haolin

AU - Wang, Shaoli

AU - Xu, Haifeng

AU - Yang, Xin

AU - Yang, Fengshan

AU - Wu, Qingjun

AU - Xie, Wen

AU - Zhou, Xuguo

AU - Dermauw, Wannes

AU - Turlings, Ted C.J.

AU - Zhang, Youjun

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N2 - 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.

AB - 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.

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KW - plant secondary metabolite

KW - tomato

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ER -

Whitefly hijacks a plant detoxification gene that neutralizes plant toxins

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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