An atypical Phytophthora sojae RxLR effector manipulates host vesicle trafficking to promote infection
In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an at...
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Published in | PLoS pathogens Vol. 17; no. 11; p. e1010104 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
01.11.2021
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Abstract | In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an atypical RxLR effector PsAvh181 secreted by
Phytophthora sojae
, inhibits the secretion of plant defense-related apoplastic proteins. PsAvh181 localizes to plant plasma membrane and essential for
P
.
sojae
infection. By co-immunoprecipitation assay followed by liquid chromatography-tandem mass spectrometry analyses, we identified the soybean GmSNAP-1 as a candidate host target of PsAvh181.
GmSNAP-1
encodes a soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein, which associates with GmNSF of the SNARE complex functioning in vesicle trafficking. PsAvh181 binds to GmSNAP-1
in vivo
and
in vitro
. PsAvh181 interferes with the interaction between GmSNAP-1 and GmNSF, and blocks the secretion of apoplastic defense-related proteins, such as pathogenesis-related protein PR-1 and apoplastic proteases. Taken together, these data show that an atypical
P
.
sojae
RxLR effector suppresses host apoplastic immunity by manipulating the host SNARE complex to interfere with host vesicle trafficking pathway. |
---|---|
AbstractList | In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an atypical RxLR effector PsAvh181 secreted by Phytophthora sojae, inhibits the secretion of plant defense-related apoplastic proteins. PsAvh181 localizes to plant plasma membrane and essential for P. sojae infection. By co-immunoprecipitation assay followed by liquid chromatography-tandem mass spectrometry analyses, we identified the soybean GmSNAP-1 as a candidate host target of PsAvh181. GmSNAP-1 encodes a soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein, which associates with GmNSF of the SNARE complex functioning in vesicle trafficking. PsAvh181 binds to GmSNAP-1 in vivo and in vitro. PsAvh181 interferes with the interaction between GmSNAP-1 and GmNSF, and blocks the secretion of apoplastic defense-related proteins, such as pathogenesis-related protein PR-1 and apoplastic proteases. Taken together, these data show that an atypical P. sojae RxLR effector suppresses host apoplastic immunity by manipulating the host SNARE complex to interfere with host vesicle trafficking pathway. In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an atypical RxLR effector PsAvh181 secreted by Phytophthora sojae, inhibits the secretion of plant defense-related apoplastic proteins. PsAvh181 localizes to plant plasma membrane and essential for P. sojae infection. By co-immunoprecipitation assay followed by liquid chromatography-tandem mass spectrometry analyses, we identified the soybean GmSNAP-1 as a candidate host target of PsAvh181. GmSNAP-1 encodes a soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein, which associates with GmNSF of the SNARE complex functioning in vesicle trafficking. PsAvh181 binds to GmSNAP-1 in vivo and in vitro. PsAvh181 interferes with the interaction between GmSNAP-1 and GmNSF, and blocks the secretion of apoplastic defense-related proteins, such as pathogenesis-related protein PR-1 and apoplastic proteases. Taken together, these data show that an atypical P. sojae RxLR effector suppresses host apoplastic immunity by manipulating the host SNARE complex to interfere with host vesicle trafficking pathway.In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an atypical RxLR effector PsAvh181 secreted by Phytophthora sojae, inhibits the secretion of plant defense-related apoplastic proteins. PsAvh181 localizes to plant plasma membrane and essential for P. sojae infection. By co-immunoprecipitation assay followed by liquid chromatography-tandem mass spectrometry analyses, we identified the soybean GmSNAP-1 as a candidate host target of PsAvh181. GmSNAP-1 encodes a soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein, which associates with GmNSF of the SNARE complex functioning in vesicle trafficking. PsAvh181 binds to GmSNAP-1 in vivo and in vitro. PsAvh181 interferes with the interaction between GmSNAP-1 and GmNSF, and blocks the secretion of apoplastic defense-related proteins, such as pathogenesis-related protein PR-1 and apoplastic proteases. Taken together, these data show that an atypical P. sojae RxLR effector suppresses host apoplastic immunity by manipulating the host SNARE complex to interfere with host vesicle trafficking pathway. In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an atypical RxLR effector PsAvh181 secreted by Phytophthora sojae , inhibits the secretion of plant defense-related apoplastic proteins. PsAvh181 localizes to plant plasma membrane and essential for P . sojae infection. By co-immunoprecipitation assay followed by liquid chromatography-tandem mass spectrometry analyses, we identified the soybean GmSNAP-1 as a candidate host target of PsAvh181. GmSNAP-1 encodes a soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein, which associates with GmNSF of the SNARE complex functioning in vesicle trafficking. PsAvh181 binds to GmSNAP-1 in vivo and in vitro . PsAvh181 interferes with the interaction between GmSNAP-1 and GmNSF, and blocks the secretion of apoplastic defense-related proteins, such as pathogenesis-related protein PR-1 and apoplastic proteases. Taken together, these data show that an atypical P . sojae RxLR effector suppresses host apoplastic immunity by manipulating the host SNARE complex to interfere with host vesicle trafficking pathway. P . sojae secretes RxLR effectors to modulate host plant immunity. PsAvh181, an atypical RxLR effector of P . sojae , contributes to the full virulence of P . sojae . However, the mechanism by which PsAvh181 modulates plant immunity remains unknown. We found that PsAvh181 localizes to the plant plasma membrane to inhibit the secretion of apoplastic defense-related proteins such as GmGIP1, P69B and PR1. We screened target proteins of PsAvh181 by coimmunoprecipitation and liquid chromatography-tandem mass spectrometry analyses. It was found that PsAvh181 binds to a soybean soluble N-ethylmaleimide sensitive factor (NSF) attachment protein (GmSNAP-1), which is an important component of the SNAP receptor (SNARE) complex and plays a significant role in vesicle trafficking. Further investigation showed that PsAvh181 interferes the interaction between GmSNAP-1 and GmNSF, thus blocking the secretion of defense-related proteins and thereby modulating plant immunity. Our results reveal how a P . sojae effector suppresses plant immunity by inhibiting the secretion of apoplastic defense-related proteins. In plants, the apoplast is a critical battlefield for plant-microbe interactions. Plants secrete defense-related proteins into the apoplast to ward off the invasion of pathogens. How microbial pathogens overcome plant apoplastic immunity remains largely unknown. In this study, we reported that an atypical RxLR effector PsAvh181 secreted by Phytophthora sojae , inhibits the secretion of plant defense-related apoplastic proteins. PsAvh181 localizes to plant plasma membrane and essential for P . sojae infection. By co-immunoprecipitation assay followed by liquid chromatography-tandem mass spectrometry analyses, we identified the soybean GmSNAP-1 as a candidate host target of PsAvh181. GmSNAP-1 encodes a soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein, which associates with GmNSF of the SNARE complex functioning in vesicle trafficking. PsAvh181 binds to GmSNAP-1 in vivo and in vitro . PsAvh181 interferes with the interaction between GmSNAP-1 and GmNSF, and blocks the secretion of apoplastic defense-related proteins, such as pathogenesis-related protein PR-1 and apoplastic proteases. Taken together, these data show that an atypical P . sojae RxLR effector suppresses host apoplastic immunity by manipulating the host SNARE complex to interfere with host vesicle trafficking pathway. |
Audience | Academic |
Author | Li, Haiyang Xu, Yuanpeng Ye, Wenwu Yang, Bo Zheng, Xiaobo Guo, Baodian Wang, Yuanchao Wang, Haonan Zhu, Jinyi Duan, Kaixuan Wang, Yan |
AuthorAffiliation | 1 Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China 3 Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China Imperial College London, UNITED KINGDOM 2 Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing, China |
AuthorAffiliation_xml | – name: 2 Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing, China – name: Imperial College London, UNITED KINGDOM – name: 3 Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China – name: 1 Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34843607$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_3389_fmicb_2022_1040302 crossref_primary_10_1094_MPMI_05_23_0054_CR crossref_primary_10_3390_jof9010012 crossref_primary_10_31083_j_fbe1601009 crossref_primary_10_3389_fmicb_2023_1119016 crossref_primary_10_1111_ppa_13713 crossref_primary_10_1146_annurev_micro_032421_121423 crossref_primary_10_1371_journal_ppat_1012542 crossref_primary_10_1016_j_fbr_2022_10_002 crossref_primary_10_1146_annurev_phyto_021622_123232 crossref_primary_10_1111_nph_18470 |
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SubjectTerms | Analysis Apoplast Battlefields Biology and Life Sciences Control Development and progression Diagnosis Glycine max - immunology Glycine max - metabolism Glycine max - parasitology Host-Pathogen Interactions Immunity Immunoprecipitation Infections Liquid chromatography Localization Mass spectrometry Mass spectroscopy Microorganisms Microscopy N-Ethylmaleimide-sensitive protein N-Ethylmaleimide-Sensitive Proteins - genetics N-Ethylmaleimide-Sensitive Proteins - metabolism Pathogenesis Pathogens Phytophthora diseases Phytophthora infestans - physiology Phytophthora sojae Plant defenses Plant Diseases - immunology Plant Diseases - parasitology Plant proteins Plant Proteins - genetics Plant Proteins - metabolism Plant-pathogen relationships Plasma Protein Interaction Domains and Motifs Proteins SNAP receptors SNARE Proteins - genetics SNARE Proteins - metabolism Soybeans Virulence Virulence Factors - genetics Virulence Factors - metabolism |
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Title | An atypical Phytophthora sojae RxLR effector manipulates host vesicle trafficking to promote infection |
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