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

Authors: LIU, XIAOFAN - Huazhong Agricultural University; ZHAO, HUIHUI - Huazhong Agricultural University; YUAN, MINGYUN - Huazhong Agricultural University; LI, PENGYUE - Huazhong Agricultural University; XIE, JIATAO - Huazhong Agricultural University; FU, YANGPING - Huazhong Agricultural University; LI, BO - Huazhong Agricultural University; YU, XIAO - Huazhong Agricultural University; CHEN, TAO - Huazhong Agricultural University; LIN, YANG - Huazhong Agricultural University; Chen, Weidong; JIANG, DAOHONG - Huazhong Agricultural University; CHENG, JIASEN - Huazhong Agricultural University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/20/2024
Publication Date: 10/30/2024
Citation: Liu, X., Zhao, H., Yuan, M., Li, P., Xie, J., Fu, Y., Li, B., Yu, X., Chen, T., Lin, Y., Chen, W., Jiang, D., Cheng, J. 2024. An effector essential for virulence of necrotrophic fungi targets plant HIRs to inhibit host immunity. Nature Communications. 15. Article 9391. https://doi.org/10.1038/s41467-024-53725-0.
DOI: https://doi.org/10.1038/s41467-024-53725-0

Interpretive Summary: The plant pathogen Sclerotinia sclerotiorum secretes numerous proteins and some of these proteins effect plant response to infection. Because such host plant-pathogen interactions play crucial roles in disease development, thorough understanding of the interactions is important for devising management strategies. Despite intensive investigations of Sclerotinia biology and pathogenesis, the roles of many of the secreted Sclerotinia effector proteins are still unknown. In this study we investigated a Sclerotinia effector called Sclerotinia sclerotiorum plant early immunosuppressive effector 1 (SsPEIE1). Production of SsPEIE1 was significantly greater during plant infection and increased plant susceptibility to infection. We show that SsPEIE1 interacts with a plant membrane protein known as hypersensitive induced reaction (HIR). HIR proteins are regulators of plant immune responses. Overexpression of Arabidopsis AtHIR4 in either Arabidopsis or oilseed rape significantly increased plant resistance to Sclerotinia.

Technical 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 more susceptibility to phytopathogens. To gain a deeper understanding of how SsPEIE1 interferes with plant immunity, we conducted further investigations. We show that SsPEIE1 interacts with a plasma membrane protein known as hypersensitive induced reaction (HIR). HIR proteins serve as positive regulators of plant immune responses. Remarkably, both Arabidopsis and rapeseed plants that overexpress AtHIR4 displayed significantly increased resistance to S. sclerotiorum. It was also observed that AtHIR4 forms homodimers, and the dimmer formation is crucial for its role in mediating immunity. Intriguingly, SsPEIE1 competes with AtHIR4 for interaction and effectively inhibits the self-interaction in homodimer formation of AtHIR4. In summary, our results demonstrate that SsPEIE1 inhibits the homodimer-mediated immune response by interacting with AtHIR4 in the early stages of infection and promotes S. sclerotiorum infection.