title: Pseudomonas syringae Effector Avirulence Protein E Localizes to the Host Plasma Membrane and Down-Regulates the Expression of the NONRACE-SPECIFIC DISEASE RESISTANCE1/HARPIN-INDUCED1-LIKE13 Gene Required for Antibacterial Immunity in Arabidopsis.
abstract: Many bacterial pathogens of plants and animals deliver effector proteins into host cells to promote infection. Elucidation of how pathogen effector proteins function not only is critical for understanding bacterial pathogenesis but also provides a useful tool in discovering the functions of host genes. In this study, we characterized the Pseudomonas syringae pv tomato DC3000 effector protein Avirulence Protein E (AvrE), the founding member of a widely distributed, yet functionally enigmatic, bacterial effector family. We show that AvrE is localized in the plasma membrane (PM) and PM-associated vesicle-like structures in the plant cell. AvrE contains two physically interacting domains, and the amino-terminal portion contains a PM-localization signal. Genome-wide microarray analysis indicates that AvrE, as well as the functionally redundant effector Hypersensitive response and pathogenicity-dependent Outer Protein M1, down-regulates the expression of the NONRACE-SPECIFIC DISEASE RESISTANCE1/HARPIN-INDUCED1-LIKE13 (NHL13) gene in Arabidopsis (Arabidopsis thaliana). Mutational analysis shows that NHL13 is required for plant immunity, as the nhl13 mutant plant displayed enhanced disease susceptibility. Our results defined the action site of one of the most important bacterial virulence proteins in plants and the antibacterial immunity function of the NHL13 gene.
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Xiu-Fang
authors.initials: XF
authors.lastname: Xin
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Kinya
authors.initials: K
authors.lastname: Nomura
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Xinhua
authors.initials: X
authors.lastname: Ding
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Xujun
authors.initials: X
authors.lastname: Chen
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Kun
authors.initials: K
authors.lastname: Wang
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Kyaw
authors.initials: K
authors.lastname: Aung
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Francisco
authors.identifier: http://orcid.org/0000-0002-3922-6328
authors.initials: F
authors.lastname: Uribe
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Bruce
authors.initials: B
authors.lastname: Rosa
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Jian
authors.initials: J
authors.lastname: Yao
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.).
authors.forename: Jin
authors.initials: J
authors.lastname: Chen
authors.affiliation: Department of Energy Plant Research Laboratory (X.-F.X., K.N., X.D., X.C., K.A., F.U., B.R., J.Y., J.C., S.Y.H.), Department of Plant Biology (X.-F.X.), Department of Biochemistry and Molecular Biology (K.W.), and Howard Hughes Medical Institute (S.Y.H.), Michigan State University, East Lansing, Michigan 48824;State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai'an, 271018 Shandong, China (X.D.);Key Laboratory of Plant Pathology, Department of Plant Pathology, China Agricultural University, Beijing 100193, China (X.C.);Genome Institute, Washington University, St. Louis, Missouri 63108 (B.R.); andDepartment of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008 (J.Y.) hes@msu.edu.
authors.forename: Sheng Yang
authors.identifier: http://orcid.org/0000-0003-1308-498X
authors.initials: SY
authors.lastname: He
mesh_terms: D000900:Anti-Bacterial Agents / Q000378:metabolism; D017360:Arabidopsis; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001426:Bacterial Proteins / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism*; D015536:Down-Regulation; D017343:Genes, Plant; D057865:Plant Immunity; D018515:Plant Leaves / Q000166:cytology; D030821:Plants, Genetically Modified; D017434:Protein Structure, Tertiary; D021381:Protein Transport; D044224:Pseudomonas syringae / Q000472:pathogenicity*; D017384:Sequence Deletion; D014774:Virulence
chemical_list: D000900:Anti-Bacterial Agents; D029681:Arabidopsis Proteins; C110610:AvrE protein, Pseudomonas syringae; D001426:Bacterial Proteins