Botrytis cinerea BcSSP protein is a late infection phase, cytotoxic effector

Authors: ZHU, WENJUN - Wuhan Institute Of Technology; YU, MENGZUE - Wuhan Institute Of Technology; XU, RAN - Wuhan Institute Of Technology; BI, KAI - Wuhan Institute Of Technology; XIONG, CHAO - Wuhan Institute Of Technology; LIU, ZHIGUO - Wuhan Institute Of Technology; SHARON, AMIR - Tel Aviv University; JIANG, DAOHONG - Huazhong Agricultural University; WU, MINGDE - Huazhong Agricultural University; GU, QIONGNAN - Hubei Academy Of Agricultural Sciences; GONG, LING - Hubei Academy Of Agricultural Sciences; Chen, Weidong; WEI, WEI - Washington State University

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/20/2022
Publication Date: 2/15/2022
Citation: Zhu, W., Yu, M., Xu, R., Bi, K., Xiong, C., Liu, Z., Sharon, A., Jiang, D., Wu, M., Gu, Q., Gong, L., Chen, W., Wei, W. 2022. Botrytis cinerea BcSSP protein is a late infection phase, cytotoxic effector. Journal of Experimental Botany. 24(8):3420-3435. https://doi.org/10.1111/1462-2920.15919.
DOI: https://doi.org/10.1111/1462-2920.15919

Interpretive Summary: Botrytis cinerea is a necrotrophic pathogen causing Botrytis blight on many economically important crops. Similar to Sclerotinia sclerotiorum, it secrets a large number of proteins during plant infection some of which interact with plant and modulate plant response to infection. Identifying and characterizing the functions of these secreted protein is very important in understanding the pathogenicity mechanisms of B. cinerea. We identified one of its secreted proteins as phytotoxic protein (BcPTP1) that is toxic to plants. BcPTP1 is a small protein with 90 amino acids with 10 cysteine residues. It can cause chlorosis and eventually lead to cell death. Its cysteine residues are important for its functions as mutating eight of the 10 cysteine residues abolished the toxic effect. However residual toxic activity is heat stable. The BcPTP1 gene is highly induced in the late infection stage, suggesting its role in lesion spreading. Deletion of the bcptp1 gene led to slightly smaller lesions on bean leaves. In summary, our findings show that BcPTP1 is a virulence factor that facilitates killing host cells and plays a role in lesion spreading during the late infection stage.

Technical Abstract: Botrytis cinerea is a broad-host-range necrotrophic phytopathogen responsible for serious crops diseases. To facilitate infection, B. cinerea secretes a large number of effectors that induce plant cell death. In screening secretome data of B. cinerea during infection stage, we identified a phytotoxic protein (BcPTP1) that can also induce immune resistance in plants. BcPTP1 is a small (90 aa), cysteine rich protein without any known domains. Transiently expression of BcPTP1 in leaves caused chlorosis that intensifies with time and eventually lead to cell death. Point mutations in eight of the 10 cysteine residues of BcPTP1 abolished the toxic effect, however residual toxic activity remained after heating the peptide, suggesting contribution of unknown epitopes to protein phytotoxic effect. The transcript level of the bcptp1 gene was low during the first 36 h after inoculation and increased sharply upon transition to the late infection stage, suggesting a role of BcPTP1 in lesion spreading. While statistically insignificant, deletion of the bcptp1 gene led to slightly smaller lesions on bean leaves. Further analyses indicated that BcPTP1 is internalized into plant cells after secreting into the apoplast and its phytotoxic effect is negatively regulated by the receptor-like kinases BAK1 and SOBIR1. Collectively, our findings show that BcPTP1 is a virulence factor that toxifies the host cells and facilitates lesion spreading during the late infection stage.