Serveur d'exploration Phytophthora

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Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor.

Identifieur interne : 000B48 ( Main/Exploration ); précédent : 000B47; suivant : 000B49

Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor.

Auteurs : Lina Yang ; Hazel Mclellan ; Shaista Naqvi ; Qin He ; Petra C. Boevink ; Miles Armstrong ; Licida M. Giuliani ; Wei Zhang ; Zhendong Tian ; Jiasui Zhan ; Eleanor M. Gilroy ; Paul R J. Birch

Source :

RBID : pubmed:26966171

Descripteurs français

English descriptors

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.

DOI: 10.1104/pp.16.00178
PubMed: 26966171
PubMed Central: PMC4854710


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<name sortKey="Armstrong, Miles" sort="Armstrong, Miles" uniqKey="Armstrong M" first="Miles" last="Armstrong">Miles Armstrong</name>
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<name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name>
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<nlm: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.).</nlm:affiliation>
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<name sortKey="Tian, Zhendong" sort="Tian, Zhendong" uniqKey="Tian Z" first="Zhendong" last="Tian">Zhendong Tian</name>
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<nlm: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.).</nlm:affiliation>
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<name sortKey="Zhan, Jiasui" sort="Zhan, Jiasui" uniqKey="Zhan J" first="Jiasui" last="Zhan">Jiasui Zhan</name>
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<name sortKey="Gilroy, Eleanor M" sort="Gilroy, Eleanor M" uniqKey="Gilroy E" first="Eleanor M" last="Gilroy">Eleanor M. Gilroy</name>
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<name sortKey="Birch, Paul R J" sort="Birch, Paul R J" uniqKey="Birch P" first="Paul R J" last="Birch">Paul R J. Birch</name>
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<nlm: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.</nlm:affiliation>
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<title xml:lang="en">Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor.</title>
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<name sortKey="Yang, Lina" sort="Yang, Lina" uniqKey="Yang L" first="Lina" last="Yang">Lina Yang</name>
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<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<name sortKey="Mclellan, Hazel" sort="Mclellan, Hazel" uniqKey="Mclellan H" first="Hazel" last="Mclellan">Hazel Mclellan</name>
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<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<name sortKey="Naqvi, Shaista" sort="Naqvi, Shaista" uniqKey="Naqvi S" first="Shaista" last="Naqvi">Shaista Naqvi</name>
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<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<name sortKey="He, Qin" sort="He, Qin" uniqKey="He Q" first="Qin" last="He">Qin He</name>
<affiliation>
<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<name sortKey="Boevink, Petra C" sort="Boevink, Petra C" uniqKey="Boevink P" first="Petra C" last="Boevink">Petra C. Boevink</name>
<affiliation>
<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<author>
<name sortKey="Armstrong, Miles" sort="Armstrong, Miles" uniqKey="Armstrong M" first="Miles" last="Armstrong">Miles Armstrong</name>
<affiliation>
<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<name sortKey="Giuliani, Licida M" sort="Giuliani, Licida M" uniqKey="Giuliani L" first="Licida M" last="Giuliani">Licida M. Giuliani</name>
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<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
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<author>
<name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name>
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<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
</affiliation>
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<author>
<name sortKey="Tian, Zhendong" sort="Tian, Zhendong" uniqKey="Tian Z" first="Zhendong" last="Tian">Zhendong Tian</name>
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<nlm: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.).</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
</affiliation>
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<author>
<name sortKey="Zhan, Jiasui" sort="Zhan, Jiasui" uniqKey="Zhan J" first="Jiasui" last="Zhan">Jiasui Zhan</name>
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<author>
<name sortKey="Gilroy, Eleanor M" sort="Gilroy, Eleanor M" uniqKey="Gilroy E" first="Eleanor M" last="Gilroy">Eleanor M. Gilroy</name>
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<wicri:noCountry code="subField">Z.T.).</wicri:noCountry>
</affiliation>
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<author>
<name sortKey="Birch, Paul R J" sort="Birch, Paul R J" uniqKey="Birch P" first="Paul R J" last="Birch">Paul R J. Birch</name>
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<nlm: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.</nlm:affiliation>
<wicri:noCountry code="subField">Z.T.)</wicri:noCountry>
</affiliation>
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<series>
<title level="j">Plant physiology</title>
<idno type="eISSN">1532-2548</idno>
<imprint>
<date when="2016" type="published">2016</date>
</imprint>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Cell Death (genetics)</term>
<term>Disease Susceptibility (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Host-Pathogen Interactions (physiology)</term>
<term>Phytophthora infestans (metabolism)</term>
<term>Phytophthora infestans (pathogenicity)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (MeSH)</term>
<term>Plant Leaves (microbiology)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Protein Domains (MeSH)</term>
<term>Solanum tuberosum (genetics)</term>
<term>Solanum tuberosum (immunology)</term>
<term>Solanum tuberosum (microbiology)</term>
<term>Tobacco (genetics)</term>
<term>Tobacco (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Domaines protéiques (MeSH)</term>
<term>Feuilles de plante (microbiologie)</term>
<term>Immunité des plantes (MeSH)</term>
<term>Interactions hôte-pathogène (physiologie)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Mort cellulaire (génétique)</term>
<term>Phytophthora infestans (métabolisme)</term>
<term>Phytophthora infestans (pathogénicité)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Prédisposition aux maladies (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Solanum tuberosum (génétique)</term>
<term>Solanum tuberosum (immunologie)</term>
<term>Solanum tuberosum (microbiologie)</term>
<term>Tabac (génétique)</term>
<term>Tabac (métabolisme)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Cell Death</term>
<term>Solanum tuberosum</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Mort cellulaire</term>
<term>Protéines végétales</term>
<term>Solanum tuberosum</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Solanum tuberosum</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Solanum tuberosum</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Phytophthora infestans</term>
<term>Plant Proteins</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Feuilles de plante</term>
<term>Maladies des plantes</term>
<term>Solanum tuberosum</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
<term>Plant Leaves</term>
<term>Solanum tuberosum</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Phytophthora infestans</term>
<term>Protéines végétales</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Phytophthora infestans</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Interactions hôte-pathogène</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Host-Pathogen Interactions</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Disease Susceptibility</term>
<term>Gene Expression Regulation, Plant</term>
<term>Plant Immunity</term>
<term>Plants, Genetically Modified</term>
<term>Protein Domains</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Domaines protéiques</term>
<term>Immunité des plantes</term>
<term>Prédisposition aux maladies</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Végétaux génétiquement modifiés</term>
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<front>
<div type="abstract" xml:lang="en">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.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">26966171</PMID>
<DateCompleted>
<Year>2018</Year>
<Month>02</Month>
<Day>23</Day>
</DateCompleted>
<DateRevised>
<Year>2019</Year>
<Month>01</Month>
<Day>11</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>171</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2016</Year>
<Month>05</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor.</ArticleTitle>
<Pagination>
<MedlinePgn>645-57</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.16.00178</ELocationID>
<Abstract>
<AbstractText>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.</AbstractText>
<CopyrightInformation>© 2016 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Yang</LastName>
<ForeName>Lina</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>McLellan</LastName>
<ForeName>Hazel</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">0000-0003-4490-7053</Identifier>
<AffiliationInfo>
<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.).</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Naqvi</LastName>
<ForeName>Shaista</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<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.).</Affiliation>
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<LastName>He</LastName>
<ForeName>Qin</ForeName>
<Initials>Q</Initials>
<Identifier Source="ORCID">0000-0002-4957-2785</Identifier>
<AffiliationInfo>
<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.).</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>Boevink</LastName>
<ForeName>Petra C</ForeName>
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<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.).</Affiliation>
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</Author>
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<LastName>Armstrong</LastName>
<ForeName>Miles</ForeName>
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<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.).</Affiliation>
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<LastName>Giuliani</LastName>
<ForeName>Licida M</ForeName>
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<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.).</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Wei</ForeName>
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<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.).</Affiliation>
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<Author ValidYN="Y">
<LastName>Tian</LastName>
<ForeName>Zhendong</ForeName>
<Initials>Z</Initials>
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