title: Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor.
abstract: Plant pathogens deliver effectors to manipulate host processes. We know little about how fungal and oomycete effectors target host proteins to promote susceptibility, yet such knowledge is vital to understand crop disease. We show that either transient expression in Nicotiana benthamiana, or stable transgenic expression in potato (Solanum tuberosum), of the Phytophthora infestans RXLR effector Pi02860 enhances leaf colonization by the pathogen. Expression of Pi02860 also attenuates cell death triggered by the P. infestans microbe-associated molecular pattern INF1, indicating that the effector suppresses pattern-triggered immunity. However, the effector does not attenuate cell death triggered by Cf4/Avr4 coexpression, showing that it does not suppress all cell death activated by cell surface receptors. Pi02860 interacts in yeast two-hybrid assays with potato NPH3/RPT2-LIKE1 (NRL1), a predicted CULLIN3-associated ubiquitin E3 ligase. Interaction of Pi02860 in planta was confirmed by coimmunoprecipitation and bimolecular fluorescence complementation assays. Virus-induced gene silencing of NRL1 in N. benthamiana resulted in reduced P. infestans colonization and accelerated INF1-mediated cell death, indicating that this host protein acts as a negative regulator of immunity. Moreover, whereas NRL1 virus-induced gene silencing had no effect on the ability of the P. infestans effector Avr3a to suppress INF1-mediated cell death, such suppression by Pi02860 was significantly attenuated, indicating that this activity of Pi02860 is mediated by NRL1. Transient overexpression of NRL1 resulted in the suppression of INF1-mediated cell death and enhanced P. infestans leaf colonization, demonstrating that NRL1 acts as a susceptibility factor to promote late blight disease.
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Lina
authors.initials: L
authors.lastname: Yang
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Hazel
authors.identifier: 0000-0003-4490-7053
authors.initials: H
authors.lastname: McLellan
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Shaista
authors.initials: S
authors.lastname: Naqvi
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Qin
authors.identifier: 0000-0002-4957-2785
authors.initials: Q
authors.lastname: He
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Petra C
authors.initials: PC
authors.lastname: Boevink
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Miles
authors.initials: M
authors.lastname: Armstrong
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Licida M
authors.initials: LM
authors.lastname: Giuliani
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Wei
authors.identifier: 0000-0003-2723-8257
authors.initials: W
authors.lastname: Zhang
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Zhendong
authors.identifier: 0000-0002-3271-5372
authors.initials: Z
authors.lastname: Tian
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.) jiasui.zhan@fafu.edu.cn paul.birch@hutton.ac.uk.
authors.forename: Jiasui
authors.initials: J
authors.lastname: Zhan
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.).
authors.forename: Eleanor M
authors.identifier: 0000-0002-5301-4268
authors.initials: EM
authors.lastname: Gilroy
authors.affiliation: Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y., J.Z.);Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., S.N., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., S.N., Q.H., P.C.B., M.A., L.M.G., E.M.G., P.R.J.B.);Division of Plant Science, School of Life Science, University of Dundee, Invergowrie, Dundee DD2 5DA, United Kingdom (L.Y., H.M., Q.H., M.A., P.R.J.B.); andKey Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei 430070, China (Q.H., W.Z., Z.T.) jiasui.zhan@fafu.edu.cn paul.birch@hutton.ac.uk.
authors.forename: Paul R J
authors.initials: PR
authors.lastname: Birch
mesh_terms: D016923:Cell Death / Q000235:genetics; D004198:Disease Susceptibility; D018506:Gene Expression Regulation, Plant; D054884:Host-Pathogen Interactions / Q000502:physiology*; D055750:Phytophthora infestans / Q000378:metabolism / Q000472:pathogenicity*; D010935:Plant Diseases / Q000382:microbiology; D057865:Plant Immunity; D018515:Plant Leaves / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified; D000072417:Protein Domains; D011198:Solanum tuberosum / Q000235:genetics / Q000276:immunology / Q000382:microbiology*; D014026:Nicotiana / Q000235:genetics / Q000378:metabolism
chemical_list: D010940:Plant Proteins