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The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b.

Identifieur interne : 000D64 ( Main/Exploration ); précédent : 000D63; suivant : 000D65

The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b.

Auteurs : Guanghui Kong [République populaire de Chine] ; Yao Zhao [République populaire de Chine] ; Maofeng Jing [République populaire de Chine] ; Jie Huang [République populaire de Chine] ; Jin Yang [République populaire de Chine] ; Yeqiang Xia [République populaire de Chine] ; Liang Kong [République populaire de Chine] ; Wenwu Ye [République populaire de Chine] ; Qin Xiong [République populaire de Chine] ; Yongli Qiao [République populaire de Chine] ; Suomeng Dong [République populaire de Chine] ; Wenbo Ma [États-Unis] ; Yuanchao Wang [République populaire de Chine]

Source :

RBID : pubmed:26317500

Descripteurs français

English descriptors

Abstract

Plant pathogens secrete an arsenal of effector proteins to impair host immunity. Some effectors possess enzymatic activities that can modify their host targets. Previously, we demonstrated that a Phytophthora sojae RXLR effector Avr3b acts as a Nudix hydrolase when expressed in planta; and this enzymatic activity is required for full virulence of P. sojae strain P6497 in soybean (Glycine max). Interestingly, recombinant Avr3b produced by E. coli does not have the hydrolase activity unless it was incubated with plant protein extracts. Here, we report the activation of Avr3b by a prolyl-peptidyl isomerase (PPIase), cyclophilin, in plant cells. Avr3b directly interacts with soybean cyclophilin GmCYP1, which activates the hydrolase activity of Avr3b in a PPIase activity-dependent manner. Avr3b contains a putative Glycine-Proline (GP) motif; which is known to confer cyclophilin-binding in other protein substrates. Substitution of the Proline (P132) in the putative GP motif impaired the interaction of Avr3b with GmCYP1; as a result, the mutant Avr3bP132A can no longer be activated by GmCYP1, and is also unable to promote Phytophthora infection. Avr3b elicits hypersensitive response (HR) in soybean cultivars producing the resistance protein Rps3b, but Avr3bP132A lost its ability to trigger HR. Furthermore, silencing of GmCYP1 rendered reduced cell death triggered by Avr3b, suggesting that GmCYP1-mediated Avr3b maturation is also required for Rps3b recognition. Finally, cyclophilins of Nicotiana benthamiana can also interact with Avr3b and activate its enzymatic activity. Overall, our results demonstrate that cyclophilin is a "helper" that activates the enzymatic activity of Avr3b after it is delivered into plant cells; as such, cyclophilin is required for the avirulence and virulence functions of Avr3b.

DOI: 10.1371/journal.ppat.1005139
PubMed: 26317500
PubMed Central: PMC4552650


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<country xml:lang="fr">République populaire de Chine</country>
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<term>Amino Acid Sequence (MeSH)</term>
<term>Blotting, Western (MeSH)</term>
<term>Cyclophilins (immunology)</term>
<term>Cyclophilins (metabolism)</term>
<term>Host-Parasite Interactions (physiology)</term>
<term>Immunoprecipitation (MeSH)</term>
<term>Molecular Sequence Data (MeSH)</term>
<term>Phytophthora (immunology)</term>
<term>Phytophthora (metabolism)</term>
<term>Phytophthora (pathogenicity)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (parasitology)</term>
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<term>Plant Proteins (immunology)</term>
<term>Plant Proteins (metabolism)</term>
<term>Pyrophosphatases (immunology)</term>
<term>Pyrophosphatases (metabolism)</term>
<term>Soybeans (parasitology)</term>
<term>Two-Hybrid System Techniques (MeSH)</term>
<term>Virulence (MeSH)</term>
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<term>Cyclophilines (immunologie)</term>
<term>Cyclophilines (métabolisme)</term>
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<term>Immunité des plantes (physiologie)</term>
<term>Immunoprécipitation (MeSH)</term>
<term>Interactions hôte-parasite (physiologie)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Maladies des plantes (parasitologie)</term>
<term>Phytophthora (immunologie)</term>
<term>Phytophthora (métabolisme)</term>
<term>Phytophthora (pathogénicité)</term>
<term>Protéines végétales (immunologie)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Pyrophosphatases (immunologie)</term>
<term>Pyrophosphatases (métabolisme)</term>
<term>Soja (parasitologie)</term>
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<term>Technique de Western (MeSH)</term>
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<term>Plant Proteins</term>
<term>Pyrophosphatases</term>
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<term>Cyclophilines</term>
<term>Maladies des plantes</term>
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<term>Protéines végétales</term>
<term>Pyrophosphatases</term>
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<term>Plant Diseases</term>
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<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Cyclophilines</term>
<term>Phytophthora</term>
<term>Protéines végétales</term>
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<term>Soja</term>
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<term>Plant Diseases</term>
<term>Soybeans</term>
</keywords>
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<term>Phytophthora</term>
</keywords>
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<term>Phytophthora</term>
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<term>Interactions hôte-parasite</term>
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<term>Host-Parasite Interactions</term>
<term>Plant Immunity</term>
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<term>Virulence</term>
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<term>Immunoprécipitation</term>
<term>Séquence d'acides aminés</term>
<term>Technique de Western</term>
<term>Techniques de double hybride</term>
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<div type="abstract" xml:lang="en">Plant pathogens secrete an arsenal of effector proteins to impair host immunity. Some effectors possess enzymatic activities that can modify their host targets. Previously, we demonstrated that a Phytophthora sojae RXLR effector Avr3b acts as a Nudix hydrolase when expressed in planta; and this enzymatic activity is required for full virulence of P. sojae strain P6497 in soybean (Glycine max). Interestingly, recombinant Avr3b produced by E. coli does not have the hydrolase activity unless it was incubated with plant protein extracts. Here, we report the activation of Avr3b by a prolyl-peptidyl isomerase (PPIase), cyclophilin, in plant cells. Avr3b directly interacts with soybean cyclophilin GmCYP1, which activates the hydrolase activity of Avr3b in a PPIase activity-dependent manner. Avr3b contains a putative Glycine-Proline (GP) motif; which is known to confer cyclophilin-binding in other protein substrates. Substitution of the Proline (P132) in the putative GP motif impaired the interaction of Avr3b with GmCYP1; as a result, the mutant Avr3bP132A can no longer be activated by GmCYP1, and is also unable to promote Phytophthora infection. Avr3b elicits hypersensitive response (HR) in soybean cultivars producing the resistance protein Rps3b, but Avr3bP132A lost its ability to trigger HR. Furthermore, silencing of GmCYP1 rendered reduced cell death triggered by Avr3b, suggesting that GmCYP1-mediated Avr3b maturation is also required for Rps3b recognition. Finally, cyclophilins of Nicotiana benthamiana can also interact with Avr3b and activate its enzymatic activity. Overall, our results demonstrate that cyclophilin is a "helper" that activates the enzymatic activity of Avr3b after it is delivered into plant cells; as such, cyclophilin is required for the avirulence and virulence functions of Avr3b. </div>
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<AbstractText>Plant pathogens secrete an arsenal of effector proteins to impair host immunity. Some effectors possess enzymatic activities that can modify their host targets. Previously, we demonstrated that a Phytophthora sojae RXLR effector Avr3b acts as a Nudix hydrolase when expressed in planta; and this enzymatic activity is required for full virulence of P. sojae strain P6497 in soybean (Glycine max). Interestingly, recombinant Avr3b produced by E. coli does not have the hydrolase activity unless it was incubated with plant protein extracts. Here, we report the activation of Avr3b by a prolyl-peptidyl isomerase (PPIase), cyclophilin, in plant cells. Avr3b directly interacts with soybean cyclophilin GmCYP1, which activates the hydrolase activity of Avr3b in a PPIase activity-dependent manner. Avr3b contains a putative Glycine-Proline (GP) motif; which is known to confer cyclophilin-binding in other protein substrates. Substitution of the Proline (P132) in the putative GP motif impaired the interaction of Avr3b with GmCYP1; as a result, the mutant Avr3bP132A can no longer be activated by GmCYP1, and is also unable to promote Phytophthora infection. Avr3b elicits hypersensitive response (HR) in soybean cultivars producing the resistance protein Rps3b, but Avr3bP132A lost its ability to trigger HR. Furthermore, silencing of GmCYP1 rendered reduced cell death triggered by Avr3b, suggesting that GmCYP1-mediated Avr3b maturation is also required for Rps3b recognition. Finally, cyclophilins of Nicotiana benthamiana can also interact with Avr3b and activate its enzymatic activity. Overall, our results demonstrate that cyclophilin is a "helper" that activates the enzymatic activity of Avr3b after it is delivered into plant cells; as such, cyclophilin is required for the avirulence and virulence functions of Avr3b. </AbstractText>
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<ForeName>Guanghui</ForeName>
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<LastName>Zhao</LastName>
<ForeName>Yao</ForeName>
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<ForeName>Maofeng</ForeName>
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<ForeName>Yuanchao</ForeName>
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<name sortKey="Zhao, Yao" sort="Zhao, Yao" uniqKey="Zhao Y" first="Yao" last="Zhao">Yao Zhao</name>
</country>
<country name="États-Unis">
<region name="Californie">
<name sortKey="Ma, Wenbo" sort="Ma, Wenbo" uniqKey="Ma W" first="Wenbo" last="Ma">Wenbo Ma</name>
</region>
</country>
</tree>
</affiliations>
</record>

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