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NIa-Pro of sugarcane mosaic virus targets Corn Cysteine Protease 1 (CCP1) to undermine salicylic acid-mediated defense in maize

文献类型： 外文期刊

作者： Yuan, Wen 1 ; Chen, Xi 1 ; Du, Kaitong 1 ; Jiang, Tong 1 ; Li, Mengfei 1 ; Cao, Yanyong 3 ; Li, Xiangdong 4 ; Doehlemann, Gunther 5 ; Fan, Zaifeng 1 ; Zhou, Tao 1 ;

作者机构： 1.China Agr Univ, Dept Plant Pathol, State Key Lab Maize Biobreeding, Key Lab Pest Monitoring & Green Management, Beijing, Peoples R China

2.China Agr Univ, Dept Plant Pathol, Key Lab Pest Monitoring & Green Management, Minist Agr & Rural Affairs, Beijing, Peoples R China

3.Henan Acad Agr Sci, Cereal Crops Inst, Zhengzhou, Peoples R China

4.Shandong Agr Univ, Dept Plant Pathol, Tai An, Peoples R China

5.Univ Cologne, Inst Plant Sci & Cluster Excellence Plant Sci CEPL, Ctr Mol Biosci, Cologne, Germany

期刊名称：PLOS PATHOGENS （ 影响因子：6.7； 五年影响因子：6.7 ）

ISSN： 1553-7366

年卷期： 2024 年 20 卷 3 期

页码：

收录情况： SCI

摘要： Papain-like cysteine proteases (PLCPs) play pivotal roles in plant defense against pathogen invasions. While pathogens can secrete effectors to target and inhibit PLCP activities, the roles of PLCPs in plant-virus interactions and the mechanisms through which viruses neutralize PLCP activities remain largely uncharted. Here, we demonstrate that the expression and activity of a maize PLCP CCP1 (Corn Cysteine Protease), is upregulated following sugarcane mosaic virus (SCMV) infection. Transient silencing of CCP1 led to a reduction in PLCP activities, thereby promoting SCMV infection in maize. Furthermore, the knockdown of CCP1 resulted in diminished salicylic acid (SA) levels and suppressed expression of SA-responsive pathogenesis-related genes. This suggests that CCP1 plays a role in modulating the SA signaling pathway. Interestingly, NIa-Pro, the primary protease of SCMV, was found to interact with CCP1, subsequently inhibiting its protease activity. A specific motif within NIa-Pro termed the inhibitor motif was identified as essential for its interaction with CCP1 and the suppression of its activity. We have also discovered that the key amino acids responsible for the interaction between NIa-Pro and CCP1 are crucial for the virulence of SCMV. In conclusion, our findings offer compelling evidence that SCMV undermines maize defense mechanisms through the interaction of NIa-Pro with CCP1. Together, these findings shed a new light on the mechanism(s) controlling the arms races between virus and plant. PLCPs perform crucial roles in plant defense against invasions by pathogens. While pathogens can secrete effectors that target and inhibit PLCP activities, the functions of PLCPs in plant-virus interactions and the mechanisms by which viruses counteract PLCP activities remain largely unexplored. In this study, we demonstrate that a maize PLCP termed CCP1 confers resistance to SCMV infection via SA signaling pathway. Conversely, SCMV NIa-Pro interacts with CCP1 and inhibits its protease activity to allow efficient viral infection. Furthermore, we have discovered that the critical amino acids responsible for the interaction between NIa-Pro and CCP1 are crucial for the virulence of SCMV.

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