Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants

• Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. • Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan...

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Veröffentlicht in:	The New phytologist Jg. 225; H. 4; S. 1746 - 1761
Hauptverfasser:	Li, Fangfang, Zhang, Mingzhen, Zhang, Changwei, Zhou, Xueping
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	England Wiley 01.02.2020 Wiley Subscription Services, Inc
Schlagworte:	Autophagy Autophagy - physiology autophagy pathway Begomovirus C1 protein cell nucleolus Cytoplasm Defence mechanisms Defense mechanisms Degradation Exports Geminiviridae Geminiviridae - metabolism geminivirus Gene Expression Regulation, Plant - immunology Genes Infections leaf curling Leaf-curl Mutation Nicotiana - virology Nicotiana benthamiana nuclear autophagy Nuclear Proteins - genetics Nuclear Proteins - metabolism Nuclear transport Nucleocapsid Proteins - metabolism Nucleoli Pathogenicity Pathogens Phagocytosis physiological transport Plant Diseases - virology plant diseases and disorders Plant Proteins - genetics Plant Proteins - metabolism plant viruses Protein transport Proteins solanaceous plants Solanum lycopersicum Solanum lycopersicum - virology Tomatoes Translocation Viral infections viral proteins Viruses solanaceous plants degradation nuclear autophagy autophagy pathway C1 protein geminivirus
ISSN:	0028-646X, 1469-8137, 1469-8137
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Abstract	• Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. • Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy-related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1-mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy-related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. • The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. • Taken together, these data suggest that a new type of nuclear autophagy-mediated degradation of viral proteins through an exportin1-dependent nuclear export pathway restricts virus infection in plants.
AbstractList	Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy-related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1-mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy-related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. Taken together, these data suggest that a new type of nuclear autophagy-mediated degradation of viral proteins through an exportin1-dependent nuclear export pathway restricts virus infection in plants.Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy-related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1-mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy-related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. Taken together, these data suggest that a new type of nuclear autophagy-mediated degradation of viral proteins through an exportin1-dependent nuclear export pathway restricts virus infection in plants. Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy-related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1-mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy-related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. Taken together, these data suggest that a new type of nuclear autophagy-mediated degradation of viral proteins through an exportin1-dependent nuclear export pathway restricts virus infection in plants. • Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. • Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy-related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1-mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy-related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. • The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. • Taken together, these data suggest that a new type of nuclear autophagy-mediated degradation of viral proteins through an exportin1-dependent nuclear export pathway restricts virus infection in plants. Summary Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy‐related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1‐mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy‐related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. Taken together, these data suggest that a new type of nuclear autophagy‐mediated degradation of viral proteins through an exportin1‐dependent nuclear export pathway restricts virus infection in plants. Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants. Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy‐related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1‐mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy‐related genes (ATGs) ATG8h , ATG5 , or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants. The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants. Taken together, these data suggest that a new type of nuclear autophagy‐mediated degradation of viral proteins through an exportin1‐dependent nuclear export pathway restricts virus infection in plants.
Author	Zhang, Changwei Zhang, Mingzhen Li, Fangfang Zhou, Xueping
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Snippet	• Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However,... Summary Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens.... Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However,...
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SubjectTerms	Autophagy Autophagy - physiology autophagy pathway Begomovirus C1 protein cell nucleolus Cytoplasm Defence mechanisms Defense mechanisms Degradation Exports Geminiviridae Geminiviridae - metabolism geminivirus Gene Expression Regulation, Plant - immunology Genes Infections leaf curling Leaf-curl Mutation Nicotiana - virology Nicotiana benthamiana nuclear autophagy Nuclear Proteins - genetics Nuclear Proteins - metabolism Nuclear transport Nucleocapsid Proteins - metabolism Nucleoli Pathogenicity Pathogens Phagocytosis physiological transport Plant Diseases - virology plant diseases and disorders Plant Proteins - genetics Plant Proteins - metabolism plant viruses Protein transport Proteins solanaceous plants Solanum lycopersicum Solanum lycopersicum - virology Tomatoes Translocation Viral infections viral proteins Viruses
Title	Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants
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