A tripartite rheostat controls self-regulated host plant resistance to insects

Jianping Guo, Huiying Wang, Wei Guan, Qin Guo, Jing Wang, Jing Yang, Yaxin Peng, Junhan Shan, Mingyang Gao, Shaojie Shi, Xinxin Shangguan, Bingfang Liu, Shengli Jing, Jing Zhang, Chunxue Xu, Jin Huang, Weiwei Rao, Xiaohong Zheng, Di Wu, Cong Zhou, Bo Du, Rongzhi Chen, Lili Zhu, Yuxian Zhu, Linda L. Walling, Qifa Zhang and Guangcun He ()
Additional contact information
Jianping Guo: Wuhan University
Huiying Wang: Wuhan University
Wei Guan: Wuhan University
Qin Guo: Wuhan University
Jing Wang: Wuhan University
Jing Yang: Wuhan University
Yaxin Peng: Wuhan University
Junhan Shan: Wuhan University
Mingyang Gao: Wuhan University
Shaojie Shi: Wuhan University
Xinxin Shangguan: Wuhan University
Bingfang Liu: Wuhan University
Shengli Jing: Wuhan University
Jing Zhang: Wuhan University
Chunxue Xu: Wuhan University
Jin Huang: Wuhan University
Weiwei Rao: Wuhan University
Xiaohong Zheng: Wuhan University
Di Wu: Wuhan University
Cong Zhou: Wuhan University
Bo Du: Wuhan University
Rongzhi Chen: Wuhan University
Lili Zhu: Wuhan University
Yuxian Zhu: Wuhan University
Linda L. Walling: University of California
Qifa Zhang: Hubei Hongshan Laboratory
Guangcun He: Wuhan University

Nature, 2023, vol. 618, issue 7966, 799-807

Abstract: Abstract Plants deploy receptor-like kinases and nucleotide-binding leucine-rich repeat receptors to confer host plant resistance (HPR) to herbivores1. These gene-for-gene interactions between insects and their hosts have been proposed for more than 50 years2. However, the molecular and cellular mechanisms that underlie HPR have been elusive, as the identity and sensing mechanisms of insect avirulence effectors have remained unknown. Here we identify an insect salivary protein perceived by a plant immune receptor. The BPH14-interacting salivary protein (BISP) from the brown planthopper (Nilaparvata lugens Stål) is secreted into rice (Oryza sativa) during feeding. In susceptible plants, BISP targets O. satvia RLCK185 (OsRLCK185; hereafter Os is used to denote O. satvia-related proteins or genes) to suppress basal defences. In resistant plants, the nucleotide-binding leucine-rich repeat receptor BPH14 directly binds BISP to activate HPR. Constitutive activation of Bph14-mediated immunity is detrimental to plant growth and productivity. The fine-tuning of Bph14-mediated HPR is achieved through direct binding of BISP and BPH14 to the selective autophagy cargo receptor OsNBR1, which delivers BISP to OsATG8 for degradation. Autophagy therefore controls BISP levels. In Bph14 plants, autophagy restores cellular homeostasis by downregulating HPR when feeding by brown planthoppers ceases. We identify an insect saliva protein sensed by a plant immune receptor and discover a three-way interaction system that offers opportunities for developing high-yield, insect-resistant crops.

Date: 2023
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DOI: 10.1038/s41586-023-06197-z

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