Puccinia triticina (Pt) , virulence factor , ,glycoside hydrolase , ,plant immunity , ,wheat rust ," /> Puccinia triticina (Pt) , virulence factor , ,glycoside hydrolase , ,plant immunity , ,wheat rust ,"/> Puccinia triticina (Pt) , virulence factor , ,glycoside hydrolase , ,plant immunity , ,wheat rust ,"/> 小麦叶锈菌分泌性糖苷水解酶PtGH26_1调控叶锈菌致病性与寄主免疫反应
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Journal of Integrative Agriculture
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A secreted glycoside hydrolase of Puccinia triticina modulates fungal pathogenesis and host immunity

Yanan Lu1, Huimin Qian1, Mengting Li1, Shijia Zhao1, Yanhui Zhang1, Na Liu1, Daowen Wang2, Zhengqing Fu3, Guozhen Xing1#, Wenming Zheng1#, Chuang Li1, 2#

1State Key Laboratory of High-Efficiency Production of Wheat-Maize Double Cropping, College of Life Sciences, Henan Agricultural University, Zhengzhou, 450002, China

2State Key Laboratory of High-Efficiency Production of Wheat-Maize Double Cropping, College of Agronomy, Henan Agricultural University, Zhengzhou, 450002, China

3Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA

 Highlights 

1. A glycoside hydrolase PtGH26_1 corresponds with the pathogenesis of Puccinia triticina.

2. PtGH26_1 shows cellulase activity and is an effector protein that inhibits plant immune responses.

3. PtGH26_1 interacts with the Fantastic Four-like protein (TaFAF) in wheat, which positively regulates host resistance to Pt.

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摘要  

锈菌(Pucciniales)是一类专性寄生真菌,其中许多种类可导致作物发生严重病害。植物病原菌中的糖苷水解酶(GHs)在病菌突破植物防御体系中发挥关键作用。然而,目前对锈菌GH家族大部分成员的功能尚不清楚,解析其生物学功能是明确锈菌致病机制和发倔防控靶标分子的重要基础。本研究鉴定了一个小麦叶锈菌(Puccinia triticinaGH26家族基因(PtGH26_1),其在侵染寄主关键时期显著诱导表达。生物学功能分析显示PtGH26_1具有纤维素酶活性,包含分泌信号肽,定位于植物细胞质和细胞核。在本氏烟Nicotiana benthamiana叶片中瞬时表达PtGH26_1能够抑制促凋亡因子Bax诱导的细胞死亡、胼胝质沉积以及防御相关基因表达。PtGH26_1体外表达蛋白注射至小麦叶片后,可显著抑制小麦对叶锈菌的抗性减弱过敏反应。利用寄主诱导基因沉默技术(HIGS瞬时沉默PtGH26_1会抑制叶锈菌生长和致病,同时检测到受侵染小麦叶片活性氧积累增加,防御基因表达水平上升。通过酵母双杂交技术筛选发现PtGH26_1可靶向小麦Fantastic Four-like家族成员TaFAF,并通过双分子荧光互补(BiFC)、荧光素酶互补成像(LCI)和pull-down实验进一步确定了PtGH26_1和TaFAF存在直接互作。通过病毒诱导基因沉默技术VIGS在小麦中沉默TaFAF基因的表达能够导致小麦叶锈病抗性减弱活性氧积累减少防御相关基因表达水平下降,表明TaFAF在小麦抗叶锈菌过程中发挥正调控功能本研究明确了叶锈菌毒力因子PtGH26_1在致病机制中的功能,其通过参与穿透植物细胞壁屏障和抑制寄主免疫反应促进锈菌的侵染。



Abstract  

Many species of the obligate biotrophic rust fungi often cause destructive diseases on crops. Glycoside hydrolases (GHs) in phytopathogens have been widely recognized for their crucial roles in breaking through the plant's defense system. Despite this, the specific functions of most GHs in rust fungi remain largely uncharted. In this study, we examined a GH26 gene from the wheat leaf rust pathogen Puccinia triticina (Pt), designated PtGH26_1, which exhibited highly induced expression during critical stages of host infection. PtGH26_1 demonstrated cellulase activity and contained a functional signal peptide, localized to both the plant cytoplasm and nucleus. When transiently expressed, PtGH26_1 inhibited Bcl2-associated X protein (Bax)-induced cell death, callose deposition, and the expression of defense-related genes in Nicotiana benthamiana. Additionally, infiltrating PtGH26_1 protein into wheat leaves compromised resistance to Pt and lessened hypersensitive responses. Silencing PtGH26_1 through host-induced gene silencing impaired fungal growth and virulence of Pt, leading to increased production of reactive oxygen species and activation of defense-related genes in wheat. Moreover, PtGH26_1 was shown to target one member of the Fantastic Four-like proteins in wheat (TaFAF), which positively regulated host resistance to Pt. Consequently, our findings indicate that PtGH26_1 is a significant virulence factor, potentially involved in breaching the barrier of plant cell walls and modulating host immune responses during Pt infection.

Keywords:  Puccinia triticina (Pt) ')" href="#">

Puccinia triticina (Pt)       virulence factor              glycoside hydrolase              plant immunity              wheat rust   

Online: 15 November 2025  
Fund: 

The study was supported by the National Natural Science Foundation of China (32402328), the Henan Provincial Science and Technology Major Project of China (251100110300), and the Open Project Program of State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, NWAFU of China (SKLCSRHPKF04).

About author:  Yanan Lu, E-mail: luyanan1031@163.com; #Correspondence Chuang Li, E-mail: lichuang_heau@aliyun.com; Wenming Zheng, E-mail: wmzheng@henau.edu.cn; Guozhen Xing, E-mail: xingguozhen2014@henau.edu.cn
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Yanan Lu, Huimin Qian, Mengting Li, Shijia Zhao, Yanhui Zhang, Na Liu, Daowen Wang, Zhengqing Fu, Guozhen Xing, Wenming Zheng, Chuang Li. 2025. A secreted glycoside hydrolase of Puccinia triticina modulates fungal pathogenesis and host immunity. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.11.027

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