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A single transcription factor facilitates an insect host combating Bacillus thuringiensis infection while maintaining fitness

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  • Zhaojiang Guo

    (Chinese Academy of Agricultural Sciences
    Guangdong Laboratory for Lingnan Modern Agriculture)

  • Le Guo

    (Chinese Academy of Agricultural Sciences)

  • Jianying Qin

    (Chinese Academy of Agricultural Sciences)

  • Fan Ye

    (Chinese Academy of Agricultural Sciences)

  • Dan Sun

    (Chinese Academy of Agricultural Sciences)

  • Qingjun Wu

    (Chinese Academy of Agricultural Sciences)

  • Shaoli Wang

    (Chinese Academy of Agricultural Sciences)

  • Neil Crickmore

    (University of Sussex)

  • Xuguo Zhou

    (University of Kentucky)

  • Alejandra Bravo

    (Universidad Nacional Autónoma de México)

  • Mario Soberón

    (Universidad Nacional Autónoma de México)

  • Youjun Zhang

    (Chinese Academy of Agricultural Sciences)

Abstract

Maintaining fitness during pathogen infection is vital for host survival as an excessive response can be as detrimental as the infection itself. Fitness costs are frequently associated with insect hosts countering the toxic effect of the entomopathogenic bacterium Bacillus thuringiensis (Bt), which delay the evolution of resistance to this pathogen. The insect pest Plutella xylostella has evolved a mechanism to resist Bt toxins without incurring significant fitness costs. Here, we reveal that non-phosphorylated and phosphorylated forms of a MAPK-modulated transcription factor fushi tarazu factor 1 (FTZ-F1) can respectively orchestrate down-regulation of Bt Cry1Ac toxin receptors and up-regulation of non-receptor paralogs via two distinct binding sites, thereby presenting Bt toxin resistance without growth penalty. Our findings reveal how host organisms can co-opt a master molecular switch to overcome pathogen invasion with low cost, and contribute to understanding the underlying mechanism of growth-defense tradeoffs during host-pathogen interactions in P. xylostella.

Suggested Citation

  • Zhaojiang Guo & Le Guo & Jianying Qin & Fan Ye & Dan Sun & Qingjun Wu & Shaoli Wang & Neil Crickmore & Xuguo Zhou & Alejandra Bravo & Mario Soberón & Youjun Zhang, 2022. "A single transcription factor facilitates an insect host combating Bacillus thuringiensis infection while maintaining fitness," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33706-x
    DOI: 10.1038/s41467-022-33706-x
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    References listed on IDEAS

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    1. Antoine Guichet & John W. R. Copeland & Miklós Erdélyi & Daniela Hlousek & Péter Závorszky & Jacqueline Ho & Susan Brown & Anthony Percival-Smith & Henry M. Krause & Anne Ephrussi, 1997. "The nuclear receptor homologue Ftz-F1 and the homeodomain protein Ftz are mutually dependent cofactors," Nature, Nature, vol. 385(6616), pages 548-552, February.
    2. Shengnan Li & Dexing Lin & Yunwei Zhang & Min Deng & Yongxing Chen & Bin Lv & Boshu Li & Yuan Lei & Yanpeng Wang & Long Zhao & Yueting Liang & Jinxing Liu & Kunling Chen & Zhiyong Liu & Jun Xiao & Jin, 2022. "Genome-edited powdery mildew resistance in wheat without growth penalties," Nature, Nature, vol. 602(7897), pages 455-460, February.
    3. Yan Yu & Willis Li & Kai Su & Miyuki Yussa & Wei Han & Norbert Perrimon & Leslie Pick, 1997. "The nuclear hormone receptor Ftz-F1 is a cofactor for the Drosophila homeodomain protein Ftz," Nature, Nature, vol. 385(6616), pages 552-555, February.
    4. Zhaojiang Guo & Shi Kang & Dan Sun & Lijun Gong & Junlei Zhou & Jianying Qin & Le Guo & Liuhong Zhu & Yang Bai & Fan Ye & Qingjun Wu & Shaoli Wang & Neil Crickmore & Xuguo Zhou & Youjun Zhang, 2020. "MAPK-dependent hormonal signaling plasticity contributes to overcoming Bacillus thuringiensis toxin action in an insect host," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
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