An effector essential for virulence of necrotrophic fungi targets plant HIRs to inhibit host immunity

Xiaofan Liu, Huihui Zhao, Mingyun Yuan, Pengyue Li, Jiatao Xie, Yanping Fu, Bo Li, Xiao Yu, Tao Chen, Yang Lin, Weidong Chen, Daohong Jiang and Jiasen Cheng ()
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Xiaofan Liu: Huazhong Agricultural University
Huihui Zhao: Huazhong Agricultural University
Mingyun Yuan: Huazhong Agricultural University
Pengyue Li: Huazhong Agricultural University
Jiatao Xie: Huazhong Agricultural University
Yanping Fu: Huazhong Agricultural University
Bo Li: Huazhong Agricultural University
Xiao Yu: Huazhong Agricultural University
Tao Chen: Huazhong Agricultural University
Yang Lin: Huazhong Agricultural University
Weidong Chen: Washington State University
Daohong Jiang: Huazhong Agricultural University
Jiasen Cheng: Huazhong Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Phytopathogens often secrete effectors to enhance their infection of plants. In the case of Sclerotinia sclerotiorum, a necrotrophic phytopathogen, a secreted protein named SsPEIE1 (Sclerotinia sclerotiorum Plant Early Immunosuppressive Effector 1) plays a crucial role in its virulence. During the early stages of infection, SsPEIE1 is significantly up-regulated. Additionally, transgenic plants expressing SsPEIE1 exhibit increased susceptibility to different phytopathogens. Further investigations revealed that SsPEIE1 interacts with a plasma membrane protein known as hypersensitive induced reaction (HIR) that dampens immune responses. SsPEIE1 is required for S. sclerotiorum virulence on wild-type Arabidopsis but not on Arabidopsis hir4 mutants. Moreover, Arabidopsis hir2 and hir4 mutants exhibit suppressed pathogen-associated molecular pattern-triggered reactive oxygen species (ROS) bursts and salicylic acid (SA)-associated immune gene induction, all of which are phenocopied by the SsPEIE1 transgenic plants. We find that the oligomerization of AtHIR4 is essential for its role in mediating immunity, and that SsPEIE1 inhibits its oligomerization through competitively binding to AtHIR4. Remarkably, both Arabidopsis and rapeseed plants overexpress AtHIR4 display significantly increased resistance to S. sclerotiorum. In summary, these results demonstrate that SsPEIE1 inhibits AtHIR4 oligomerization-mediated immune responses by interacting with the key immune factor AtHIR4, thereby promoting S. sclerotiorum infection.

Date: 2024
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DOI: 10.1038/s41467-024-53725-0

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