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Peer-reviewedCC BY 4.0Nucleic Acids Research

Microsatellite expansion redirects chromatin modifiers to confer insect resistance to Bt bioinsecticides

  • Chunzheng Ouyang1
  • Kaiyue Sun1
  • Fu Wang1
  • Fan Ye1
  • Liuhong Zhu1
  • Lina Dong1
  • Yang Bai1
  • Zhouqiang Cheng1
  • Mingmei Wu1
  • Neil Crickmore2
  • Xuguo Zhou3
  • Youjun Zhang1
1 more authors
  • Zhaojiang Guo1
  1. 1State Key Laboratory of Vegetable Biobreeding, Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences , Beijing 100081 ,
  2. 2School of Life Sciences, University of Sussex , Brighton BN1 9QE ,
  3. 3Department of Entomology, School of Integrative Biology, College of Liberal Arts & Sciences, University of Illinois Urbana-Champaign , Illinois 61801-3795 ,
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Abstract

Microsatellites are highly mutable genomic elements, yet their role in adaptive gene regulation in insects remains poorly understood. Here, we show that a tetranucleotide (ATGT) microsatellite expansion in the promoter of ABCC2, a key Bacillus thuringiensis (Bt) toxin receptor gene, epigenetically silences its expression and confers resistance to Bt Cry1Ac toxin in Plutella xylostella (L.). Mechanistically, long repeats (≥27 units) in Cry1Ac-resistant strains preferentially recruit the histone methyltransferase E(z), promoting H3K27me2/3 deposition, chromatin compaction, and transcriptional silencing, whereas short repeats in susceptible strains maintain open chromatin through Tip60-mediated H4K5 acetylation. This repeat expansion alone is sufficient to repress ABCC2, thereby conferring Bt resistance, while repeat length, chromatin state, and associated phenotypes partially revert under relaxed selection. These findings define a previously uncharacterized cis-acting element dynamically orchestrating insecticide resistance-associated gene expression and identify microsatellite-driven chromatin remodeling as a general and plastic regulatory strategy underlying rapid xenobiotic-resistance evolution in insects.

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Cite

BibTeXRIS
BibTeX
@article{ouyang2026microsatellite,
  title = {{Microsatellite expansion redirects chromatin modifiers to confer insect resistance to Bt bioinsecticides}},
  author = {Chunzheng Ouyang and Kaiyue Sun and Fu Wang and Fan Ye and Liuhong Zhu and Lina Dong and Yang Bai and Zhouqiang Cheng and Mingmei Wu and Neil Crickmore and Xuguo Zhou and Youjun Zhang and Zhaojiang Guo},
  journal = {Nucleic Acids Research},
  year = {2026},
  month = oct,
  doi = {10.1093/nar/gkag1058},
  url = {https://academic.oup.com/nar/article/doi/10.1093/nar/gkag1058/9002629},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - Microsatellite expansion redirects chromatin modifiers to confer insect resistance to Bt bioinsecticides
AU  - Chunzheng Ouyang
AU  - Kaiyue Sun
AU  - Fu Wang
AU  - Fan Ye
AU  - Liuhong Zhu
AU  - Lina Dong
AU  - Yang Bai
AU  - Zhouqiang Cheng
AU  - Mingmei Wu
AU  - Neil Crickmore
AU  - Xuguo Zhou
AU  - Youjun Zhang
AU  - Zhaojiang Guo
PY  - 2026
DA  - 2026/10/27
JO  - Nucleic Acids Research
DO  - 10.1093/nar/gkag1058
UR  - https://academic.oup.com/nar/article/doi/10.1093/nar/gkag1058/9002629
AB  - Microsatellites are highly mutable genomic elements, yet their role in adaptive gene regulation in insects remains poorly understood. Here, we show that a tetranucleotide (ATGT) microsatellite expansion in the promoter of ABCC2, a key Bacillus thuringiensis (Bt) toxin receptor gene, epigenetically silences its expression and confers resistance to Bt Cry1Ac toxin in Plutella xylostella (L.). Mechanistically, long repeats (≥27 units) in Cry1Ac-resistant strains preferentially recruit the histone methyltransferase E(z), promoting H3K27me2/3 deposition, chromatin compaction, and transcriptional silencing, whereas short repeats in susceptible strains maintain open chromatin through Tip60-mediated H4K5 acetylation. This repeat expansion alone is sufficient to repress ABCC2, thereby conferring Bt resistance, while repeat length, chromatin state, and associated phenotypes partially revert under relaxed selection. These findings define a previously uncharacterized cis-acting element dynamically orchestrating insecticide resistance-associated gene expression and identify microsatellite-driven chromatin remodeling as a general and plastic regulatory strategy underlying rapid xenobiotic-resistance evolution in insects.
SN  - 0305-1048
SN  - 1362-4962
ER  -