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The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1

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Abstract
RNA silencing is a major antiviral defense mechanism in plants and invertebrates. Plant ARGONAUTE1 (AGO1) is pivotal in RNA silencing, and hence is a major target for counteracting viral suppressors of RNA-silencing proteins (VSRs). P0 from Turnip yellows virus (TuYV) is a VSR that was previously shown to trigger AGO1 degradation via an autophagy-like process. However, the identity of host proteins involved and the cellular site at which AGO1 and P0 interact were unknown. Here we report that P0 and AGO1 associate on the endoplasmic reticulum (ER), resulting in their loading into ER-associated vesicles that are mobilized to the vacuole in an ATG5- and ATG7-dependent manner. We further identified ATG8-Interacting proteins 1 and 2 (ATI1 and ATI2) as proteins that associate with P0 and interact with AGO1 on the ER up to the vacuole. Notably, ATI1 and ATI2 belong to an endogenous degradation pathway of ER-associated AGO1 that is significantly induced following P0 expression. Accordingly, ATI1 and ATI2 deficiency causes a significant increase in posttranscriptional gene silencing (PTGS) activity. Collectively, we identify ATI1 and ATI2 as components of an ER-associated AGO1 turnover and proper PTGS maintenance and further show how the V512 P0 manipulates this pathway.
Keywords
Multidisciplinary, RNA silencing, autophagy, Arabidopsis, SELECTIVE AUTOPHAGY, SILENCING SUPPRESSOR, SMALL RNAS, ARGONAUTE COMPLEXES, 26S PROTEASOME, ARABIDOPSIS, TRAFFICKING, BIOGENESIS, MECHANISMS, INHIBITION

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MLA
Michaeli, Simon, et al. “The Viral F-Box Protein P0 Induces an ER-Derived Autophagy Degradation Pathway for the Clearance of Membrane-Bound AGO1.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 45, 2019, pp. 22872–83, doi:10.1073/pnas.1912222116.
APA
Michaeli, S., Clavel, M., Lechner, E., Viotti, C., Wu, J., Dubois, M., … Genschik, P. (2019). The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(45), 22872–22883. https://doi.org/10.1073/pnas.1912222116
Chicago author-date
Michaeli, Simon, Marion Clavel, Esther Lechner, Corrado Viotti, Jian Wu, Marieke Dubois, Thibaut Hacquard, et al. 2019. “The Viral F-Box Protein P0 Induces an ER-Derived Autophagy Degradation Pathway for the Clearance of Membrane-Bound AGO1.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (45): 22872–83. https://doi.org/10.1073/pnas.1912222116.
Chicago author-date (all authors)
Michaeli, Simon, Marion Clavel, Esther Lechner, Corrado Viotti, Jian Wu, Marieke Dubois, Thibaut Hacquard, Benoît Derrien, Esther Izquierdo, Maxime Lecorbeiller, Nathalie Bouteiller, Julia De Cilia, Véronique Ziegler-Graff, Hervé Vaucheret, Gad Galili, and Pascal Genschik. 2019. “The Viral F-Box Protein P0 Induces an ER-Derived Autophagy Degradation Pathway for the Clearance of Membrane-Bound AGO1.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (45): 22872–22883. doi:10.1073/pnas.1912222116.
Vancouver
1.
Michaeli S, Clavel M, Lechner E, Viotti C, Wu J, Dubois M, et al. The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2019;116(45):22872–83.
IEEE
[1]
S. Michaeli et al., “The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 45, pp. 22872–22883, 2019.
@article{8646752,
  abstract     = {{RNA silencing is a major antiviral defense mechanism in plants and invertebrates. Plant ARGONAUTE1 (AGO1) is pivotal in RNA silencing, and hence is a major target for counteracting viral suppressors of RNA-silencing proteins (VSRs). P0 from Turnip yellows virus (TuYV) is a VSR that was previously shown to trigger AGO1 degradation via an autophagy-like process. However, the identity of host proteins involved and the cellular site at which AGO1 and P0 interact were unknown. Here we report that P0 and AGO1 associate on the endoplasmic reticulum (ER), resulting in their loading into ER-associated vesicles that are mobilized to the vacuole in an ATG5- and ATG7-dependent manner. We further identified ATG8-Interacting proteins 1 and 2 (ATI1 and ATI2) as proteins that associate with P0 and interact with AGO1 on the ER up to the vacuole. Notably, ATI1 and ATI2 belong to an endogenous degradation pathway of ER-associated AGO1 that is significantly induced following P0 expression. Accordingly, ATI1 and ATI2 deficiency causes a significant increase in posttranscriptional gene silencing (PTGS) activity. Collectively, we identify ATI1 and ATI2 as components of an ER-associated AGO1 turnover and proper PTGS maintenance and further show how the V512 P0 manipulates this pathway.}},
  author       = {{Michaeli, Simon and Clavel, Marion and Lechner, Esther and Viotti, Corrado and Wu, Jian and Dubois, Marieke and Hacquard, Thibaut and Derrien, Benoît and Izquierdo, Esther and Lecorbeiller, Maxime and Bouteiller, Nathalie and De Cilia, Julia and Ziegler-Graff, Véronique and Vaucheret, Hervé and Galili, Gad and Genschik, Pascal}},
  issn         = {{0027-8424}},
  journal      = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}},
  keywords     = {{Multidisciplinary,RNA silencing,autophagy,Arabidopsis,SELECTIVE AUTOPHAGY,SILENCING SUPPRESSOR,SMALL RNAS,ARGONAUTE COMPLEXES,26S PROTEASOME,ARABIDOPSIS,TRAFFICKING,BIOGENESIS,MECHANISMS,INHIBITION}},
  language     = {{eng}},
  number       = {{45}},
  pages        = {{22872--22883}},
  title        = {{The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1}},
  url          = {{http://dx.doi.org/10.1073/pnas.1912222116}},
  volume       = {{116}},
  year         = {{2019}},
}

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