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Peer-reviewedCC BY-NC 4.0Science Advances

Rapid activation kinetics of the NLR Swordholder underpin nonhost resistance to Phytophthora capsici in Nicotiana tabacum

  • Xiaowei Fu1,2
  • Xianglan Li1
  • Wenyi Zhu2
  • Yueyi Ren1
  • Tianli Li1
  • Chuyan Xia1
  • Xiaohua Dong1,2
  • Zhaojie Chen3
  • Jinding Liu1
  • Danyu Shen1
  • Li Wan4
  • Gan Ai1
1 more authors
  • Daolong Dou1
4 affiliations
  1. 1State Key Laboratory of Agricultural and Forestry Biosecurity, Academy for Advanced Interdisciplinary Studies, College of Plant Protection, Nanjing Agricultural University, Nanjing, China.
  2. 2Sanya Research Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya 572000, China.
  3. 3Guangxi Key Laboratory of Agric-Environment and Agric-Products Safety, College of Agriculture, Guangxi University, Nanning, Guangxi 530004, China.
  4. 4Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China.
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Abstract

Nonhost resistance (NHR) represents a durable phenomenon where plants resist nonadapted pathogens. While NHR holds substantial potential for engineering crops with broad-spectrum and durable resistance, its underlying molecular mechanism remains incompletely understood. The oomycete pathogen Phytophthora capsici is nonadapted to Nicotiana tabacum (Nt) but is virulent on the closely related Nicotiana benthamiana (Nb). Here, we demonstrated that both species encode the NLR Swordholder (Swh), which recognizes P. capsici AvrNt effector proteins. NtSwh restores NHR in ntswh mutants, whereas NbSwh confers only partial resistance. Mechanistically, NtSwh exhibits weaker autoinhibition mediated by its amino-terminal extension domains, enabling rapid immune signaling that prevent pathogen effector–mediated suppression; NbSwh’s stronger autoinhibition delays activation, permitting effector suppression. Heterologous expression of NtSwh in tomato enhances field resistance to P. capsici without yield penalty. These findings indicate that the kinetics of NLR can play a key role in defining NHR, in addition to the presence or absence of specific NLRs, providing insights into strategies for breeding durable crop immunity.

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Cite

BibTeXRIS
BibTeX
@article{fu2026rapid,
  title = {{Rapid activation kinetics of the NLR Swordholder underpin nonhost resistance to Phytophthora capsici in Nicotiana tabacum}},
  author = {Xiaowei Fu and Xianglan Li and Wenyi Zhu and Yueyi Ren and Tianli Li and Chuyan Xia and Xiaohua Dong and Zhaojie Chen and Jinding Liu and Danyu Shen and Li Wan and Gan Ai and Daolong Dou},
  journal = {Science Advances},
  year = {2026},
  month = nov,
  doi = {10.1126/sciadv.aej0978},
  url = {https://www.science.org/doi/abs/10.1126/sciadv.aej0978},
  note = {CC BY-NC 4.0},
}
RIS
TY  - JOUR
TI  - Rapid activation kinetics of the NLR Swordholder underpin nonhost resistance to Phytophthora capsici in Nicotiana tabacum
AU  - Xiaowei Fu
AU  - Xianglan Li
AU  - Wenyi Zhu
AU  - Yueyi Ren
AU  - Tianli Li
AU  - Chuyan Xia
AU  - Xiaohua Dong
AU  - Zhaojie Chen
AU  - Jinding Liu
AU  - Danyu Shen
AU  - Li Wan
AU  - Gan Ai
AU  - Daolong Dou
PY  - 2026
DA  - 2026/11/04
JO  - Science Advances
DO  - 10.1126/sciadv.aej0978
UR  - https://www.science.org/doi/abs/10.1126/sciadv.aej0978
AB  - Nonhost resistance (NHR) represents a durable phenomenon where plants resist nonadapted pathogens. While NHR holds substantial potential for engineering crops with broad-spectrum and durable resistance, its underlying molecular mechanism remains incompletely understood. The oomycete pathogen Phytophthora capsici is nonadapted to Nicotiana tabacum (Nt) but is virulent on the closely related Nicotiana benthamiana (Nb). Here, we demonstrated that both species encode the NLR Swordholder (Swh), which recognizes P. capsici AvrNt effector proteins. NtSwh restores NHR in ntswh mutants, whereas NbSwh confers only partial resistance. Mechanistically, NtSwh exhibits weaker autoinhibition mediated by its amino-terminal extension domains, enabling rapid immune signaling that prevent pathogen effector–mediated suppression; NbSwh’s stronger autoinhibition delays activation, permitting effector suppression. Heterologous expression of NtSwh in tomato enhances field resistance to P. capsici without yield penalty. These findings indicate that the kinetics of NLR can play a key role in defining NHR, in addition to the presence or absence of specific NLRs, providing insights into strategies for breeding durable crop immunity.
SN  - 2375-2548
ER  -