LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis

Botryosphaeria dothidea infects hundreds of woody plants and causes a severe economic loss to apple production. In this study, we characterized BdLM1, a protein from B. dothidea that contains one LysM domain. BdLM1 expression was dramatically induced at 6 h post-inoculation in wounded apple fruit, s...

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Main Authors: He Zhang, Sheng-hui Wen, Pei-hang Li, Liu-yi Lu, Xu Yang, Chuan-jie Zhang, Li-yun Guo, Dongli Wang, Xiao-qiong Zhu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1320980/full
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author He Zhang
Sheng-hui Wen
Pei-hang Li
Liu-yi Lu
Xu Yang
Chuan-jie Zhang
Li-yun Guo
Dongli Wang
Xiao-qiong Zhu
Xiao-qiong Zhu
author_facet He Zhang
Sheng-hui Wen
Pei-hang Li
Liu-yi Lu
Xu Yang
Chuan-jie Zhang
Li-yun Guo
Dongli Wang
Xiao-qiong Zhu
Xiao-qiong Zhu
author_sort He Zhang
collection DOAJ
description Botryosphaeria dothidea infects hundreds of woody plants and causes a severe economic loss to apple production. In this study, we characterized BdLM1, a protein from B. dothidea that contains one LysM domain. BdLM1 expression was dramatically induced at 6 h post-inoculation in wounded apple fruit, strongly increased at 7 d post-inoculation (dpi), and peaked at 20 dpi in intact shoots. The knockout mutants of BdLM1 had significantly reduced virulence on intact apple shoots (20%), wounded apple shoots (40%), and wounded apple fruit (40%). BdLM1 suppressed programmed cell death caused by the mouse protein BAX through Agrobacterium-mediated transient expression in Nicotiana benthamiana, reduced H2O2 accumulation and callose deposition, downregulated resistance gene expression, and promoted Phytophthora nicotianae infection in N. benthamiana. Moreover, BdLM1 inhibited the active oxygen burst induced by chitin and flg22, bound chitin, and protected fungal hyphae against degradation by hydrolytic enzymes. Taken together, our results indicate that BdLM1 is an essential LysM effector required for the full virulence of B. dothidea and that it inhibits plant immunity. Moreover, BdLM1 could inhibit chitin-triggered plant immunity through a dual role, i.e., binding chitin and protecting fungal hyphae against chitinase hydrolysis.
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spelling doaj.art-b4ea9536b2754b9e83d375710669a7222024-01-08T04:54:02ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-01-011410.3389/fpls.2023.13209801320980LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysisHe Zhang0Sheng-hui Wen1Pei-hang Li2Liu-yi Lu3Xu Yang4Chuan-jie Zhang5Li-yun Guo6Dongli Wang7Xiao-qiong Zhu8Xiao-qiong Zhu9Department of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology and MARA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, ChinaSanya Institute of China Agricultural University, Sanya, ChinaBotryosphaeria dothidea infects hundreds of woody plants and causes a severe economic loss to apple production. In this study, we characterized BdLM1, a protein from B. dothidea that contains one LysM domain. BdLM1 expression was dramatically induced at 6 h post-inoculation in wounded apple fruit, strongly increased at 7 d post-inoculation (dpi), and peaked at 20 dpi in intact shoots. The knockout mutants of BdLM1 had significantly reduced virulence on intact apple shoots (20%), wounded apple shoots (40%), and wounded apple fruit (40%). BdLM1 suppressed programmed cell death caused by the mouse protein BAX through Agrobacterium-mediated transient expression in Nicotiana benthamiana, reduced H2O2 accumulation and callose deposition, downregulated resistance gene expression, and promoted Phytophthora nicotianae infection in N. benthamiana. Moreover, BdLM1 inhibited the active oxygen burst induced by chitin and flg22, bound chitin, and protected fungal hyphae against degradation by hydrolytic enzymes. Taken together, our results indicate that BdLM1 is an essential LysM effector required for the full virulence of B. dothidea and that it inhibits plant immunity. Moreover, BdLM1 could inhibit chitin-triggered plant immunity through a dual role, i.e., binding chitin and protecting fungal hyphae against chitinase hydrolysis.https://www.frontiersin.org/articles/10.3389/fpls.2023.1320980/fullapple ring rotagrobacterium-mediated infiltrationpathogen-associated molecular pattern (PAMP)lysin motif (LysM) effectorspathogenicity
spellingShingle He Zhang
Sheng-hui Wen
Pei-hang Li
Liu-yi Lu
Xu Yang
Chuan-jie Zhang
Li-yun Guo
Dongli Wang
Xiao-qiong Zhu
Xiao-qiong Zhu
LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
Frontiers in Plant Science
apple ring rot
agrobacterium-mediated infiltration
pathogen-associated molecular pattern (PAMP)
lysin motif (LysM) effectors
pathogenicity
title LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
title_full LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
title_fullStr LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
title_full_unstemmed LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
title_short LysM protein BdLM1 of Botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
title_sort lysm protein bdlm1 of botryosphaeria dothidea plays an important role in full virulence and inhibits plant immunity by binding chitin and protecting hyphae from hydrolysis
topic apple ring rot
agrobacterium-mediated infiltration
pathogen-associated molecular pattern (PAMP)
lysin motif (LysM) effectors
pathogenicity
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1320980/full
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