Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility

<i>Puccinia striiformis</i> f. sp. <i>tritici</i> is an obligate biotrophic fungus that causes destructive stripe rust disease in wheat. During infection, <i>Pst</i> secretes virulence effectors via a specific infection structure—the haustorium—inside host cells t...

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Main Authors: Haibin Zhao, Jiangyu Huang, Xiaoyan Zhao, Ligang Yu, Xiaodong Wang, Congcong Zhao, Hojjatollah Rabbani nasab, Chunlei Tang, Xiaojie Wang
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/13/1/94
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author Haibin Zhao
Jiangyu Huang
Xiaoyan Zhao
Ligang Yu
Xiaodong Wang
Congcong Zhao
Hojjatollah Rabbani nasab
Chunlei Tang
Xiaojie Wang
author_facet Haibin Zhao
Jiangyu Huang
Xiaoyan Zhao
Ligang Yu
Xiaodong Wang
Congcong Zhao
Hojjatollah Rabbani nasab
Chunlei Tang
Xiaojie Wang
author_sort Haibin Zhao
collection DOAJ
description <i>Puccinia striiformis</i> f. sp. <i>tritici</i> is an obligate biotrophic fungus that causes destructive stripe rust disease in wheat. During infection, <i>Pst</i> secretes virulence effectors via a specific infection structure—the haustorium—inside host cells to disturb host immunity and promote fungal colonization and expansion. Hence, the identification and functional analyses of <i>Pst</i> effectors are of great significance in deciphering the <i>Pst</i> pathogenicity mechanism. Here, we identified one candidate <i>Pst</i> effector Pst_9302 that could suppress Bax-triggered cell death in <i>Nicotiana benthamiana</i>. qRT-PCR analyses showed that the transcript levels of <i>Pst_9302</i> were highly increased during the early infection stages of <i>Pst</i>. The transient expression of <i>Pst_9302</i> in wheat via the type-three secretion system (T3SS) significantly inhibited the callose deposition induced by <i>Pseudomonas syringae</i> EtHAn. During wheat–<i>Pst</i> interaction, <i>Pst_9302</i> overexpression suppressed reactive oxygen species (ROS) accumulation and cell death caused by the avirulent <i>Pst</i> race CYR23. The host-induced gene silencing (HIGS) of <i>Pst_9302</i> resulted in decreased <i>Pst</i> pathogenicity with reduced infection area. The results suggest that Pst_9302 plays a virulence role in suppressing plant immunity and promoting <i>Pst</i> pathogenicity. Moreover, wheat voltage-dependent anion channel 1 protein (TaVDAC1) was identified as candidate Pst_9302-interacting proteins by yeast two-hybrid (Y2H) screening. Pull-down assays using the His-Pst_9302 and GST-TaVDAC1 protein verified their interactions. These results suggest that Pst_9302 may modulate wheat TaVDAC1 to regulate plant immunity.
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spelling doaj.art-b4e16c7e61d646f89be36ceffc08841a2024-01-10T15:06:15ZengMDPI AGPlants2223-77472023-12-011319410.3390/plants13010094Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote SusceptibilityHaibin Zhao0Jiangyu Huang1Xiaoyan Zhao2Ligang Yu3Xiaodong Wang4Congcong Zhao5Hojjatollah Rabbani nasab6Chunlei Tang7Xiaojie Wang8State Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress, Plant Protection Department, Golestan Agricultural and Natural Resource Research and Education Center, Gorgan P.O. Box 49156-77555, IranState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Xianyang 712100, China<i>Puccinia striiformis</i> f. sp. <i>tritici</i> is an obligate biotrophic fungus that causes destructive stripe rust disease in wheat. During infection, <i>Pst</i> secretes virulence effectors via a specific infection structure—the haustorium—inside host cells to disturb host immunity and promote fungal colonization and expansion. Hence, the identification and functional analyses of <i>Pst</i> effectors are of great significance in deciphering the <i>Pst</i> pathogenicity mechanism. Here, we identified one candidate <i>Pst</i> effector Pst_9302 that could suppress Bax-triggered cell death in <i>Nicotiana benthamiana</i>. qRT-PCR analyses showed that the transcript levels of <i>Pst_9302</i> were highly increased during the early infection stages of <i>Pst</i>. The transient expression of <i>Pst_9302</i> in wheat via the type-three secretion system (T3SS) significantly inhibited the callose deposition induced by <i>Pseudomonas syringae</i> EtHAn. During wheat–<i>Pst</i> interaction, <i>Pst_9302</i> overexpression suppressed reactive oxygen species (ROS) accumulation and cell death caused by the avirulent <i>Pst</i> race CYR23. The host-induced gene silencing (HIGS) of <i>Pst_9302</i> resulted in decreased <i>Pst</i> pathogenicity with reduced infection area. The results suggest that Pst_9302 plays a virulence role in suppressing plant immunity and promoting <i>Pst</i> pathogenicity. Moreover, wheat voltage-dependent anion channel 1 protein (TaVDAC1) was identified as candidate Pst_9302-interacting proteins by yeast two-hybrid (Y2H) screening. Pull-down assays using the His-Pst_9302 and GST-TaVDAC1 protein verified their interactions. These results suggest that Pst_9302 may modulate wheat TaVDAC1 to regulate plant immunity.https://www.mdpi.com/2223-7747/13/1/94<i>Puccinia striiformis</i> f. sp. <i>tritici</i>effectorHIGSVDAC1plant immunity
spellingShingle Haibin Zhao
Jiangyu Huang
Xiaoyan Zhao
Ligang Yu
Xiaodong Wang
Congcong Zhao
Hojjatollah Rabbani nasab
Chunlei Tang
Xiaojie Wang
Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility
Plants
<i>Puccinia striiformis</i> f. sp. <i>tritici</i>
effector
HIGS
VDAC1
plant immunity
title Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility
title_full Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility
title_fullStr Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility
title_full_unstemmed Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility
title_short Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility
title_sort stripe rust effector pst 9302 inhibits wheat immunity to promote susceptibility
topic <i>Puccinia striiformis</i> f. sp. <i>tritici</i>
effector
HIGS
VDAC1
plant immunity
url https://www.mdpi.com/2223-7747/13/1/94
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