Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants

Bacterial fruit blotch (BFB), caused by <i>Acidovorax citrulli</i>, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of <i>A. citrulli</i> is not well understood. Plant pathogenic bacteria of...

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Main Authors: Xiaoxiao Zhang, Mei Zhao, Jie Jiang, Linlin Yang, Yuwen Yang, Shanshan Yang, Ron Walcott, Dewen Qiu, Tingchang Zhao
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/17/6050
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author Xiaoxiao Zhang
Mei Zhao
Jie Jiang
Linlin Yang
Yuwen Yang
Shanshan Yang
Ron Walcott
Dewen Qiu
Tingchang Zhao
author_facet Xiaoxiao Zhang
Mei Zhao
Jie Jiang
Linlin Yang
Yuwen Yang
Shanshan Yang
Ron Walcott
Dewen Qiu
Tingchang Zhao
author_sort Xiaoxiao Zhang
collection DOAJ
description Bacterial fruit blotch (BFB), caused by <i>Acidovorax citrulli</i>, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of <i>A. citrulli</i> is not well understood. Plant pathogenic bacteria often suppress the plant immune response by secreting effector proteins. Thus, identifying <i>A. citrulli</i> effector proteins and determining their functions may improve our understanding of the underlying pathogenetic mechanisms. In this study, a novel effector, AopN, which is localized on the cell membrane of <i>Nicotiana benthamiana,</i> was identified. The functional analysis revealed that AopN significantly inhibited the flg22-induced reactive oxygen species burst. AopN induced a programmed cell death (PCD) response. Unlike its homologous protein, the ability of AopN to induce PCD was dependent on two motifs of unknown functions (including DUP4129 and Cpta_toxin), but was not dependent on LXXLL domain. More importantly, the virulence of the <i>aopN</i> mutant of <i>A. citrulli</i> in <i>N. benthamiana</i> significantly decreased, indicating that it was a core effector. Further analysis revealed that AopN interacted with watermelon ClHIPP and ClLTP, which responds to <i>A. citrulli</i> strain Aac5 infection at the transcription level. Collectively, these findings indicate that AopN suppresses plant immunity and activates the effector-triggered immunity pathway.
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spelling doaj.art-71654e47c24a45f4a95292407fbb23d52023-11-20T11:01:44ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-08-012117605010.3390/ijms21176050Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in PlantsXiaoxiao Zhang0Mei Zhao1Jie Jiang2Linlin Yang3Yuwen Yang4Shanshan Yang5Ron Walcott6Dewen Qiu7Tingchang Zhao8State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaDepartment of Plant Pathology, University of Georgia, Athens, GA 30602, USAState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaInstitute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100193, ChinaDepartment of Plant Pathology, University of Georgia, Athens, GA 30602, USAState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaBacterial fruit blotch (BFB), caused by <i>Acidovorax citrulli</i>, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of <i>A. citrulli</i> is not well understood. Plant pathogenic bacteria often suppress the plant immune response by secreting effector proteins. Thus, identifying <i>A. citrulli</i> effector proteins and determining their functions may improve our understanding of the underlying pathogenetic mechanisms. In this study, a novel effector, AopN, which is localized on the cell membrane of <i>Nicotiana benthamiana,</i> was identified. The functional analysis revealed that AopN significantly inhibited the flg22-induced reactive oxygen species burst. AopN induced a programmed cell death (PCD) response. Unlike its homologous protein, the ability of AopN to induce PCD was dependent on two motifs of unknown functions (including DUP4129 and Cpta_toxin), but was not dependent on LXXLL domain. More importantly, the virulence of the <i>aopN</i> mutant of <i>A. citrulli</i> in <i>N. benthamiana</i> significantly decreased, indicating that it was a core effector. Further analysis revealed that AopN interacted with watermelon ClHIPP and ClLTP, which responds to <i>A. citrulli</i> strain Aac5 infection at the transcription level. Collectively, these findings indicate that AopN suppresses plant immunity and activates the effector-triggered immunity pathway.https://www.mdpi.com/1422-0067/21/17/6050AopNprogrammed cell death<i>Acidovorax citrulli</i>plant pathogeneffector-triggered immunity
spellingShingle Xiaoxiao Zhang
Mei Zhao
Jie Jiang
Linlin Yang
Yuwen Yang
Shanshan Yang
Ron Walcott
Dewen Qiu
Tingchang Zhao
Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants
International Journal of Molecular Sciences
AopN
programmed cell death
<i>Acidovorax citrulli</i>
plant pathogen
effector-triggered immunity
title Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants
title_full Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants
title_fullStr Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants
title_full_unstemmed Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants
title_short Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants
title_sort identification and functional analysis of aopn an i acidovorax citrulli i effector that induces programmed cell death in plants
topic AopN
programmed cell death
<i>Acidovorax citrulli</i>
plant pathogen
effector-triggered immunity
url https://www.mdpi.com/1422-0067/21/17/6050
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