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

Simon Michaeli (1) , Marion Clavel (1) , Esther Lechner (1) , Corrado Viotti (1) , Jian Wu (2) , Marieke Dubois (1, 3) , Thibaut Hacquard (1) , Benoît Derrien (1) , Esther Izquierdo (4) , Maxime Lecorbeiller (1) , Nathalie Bouteiller (5) , Julia de Cilia (1) , Veronique Ziegler-Graff (1) , Hervé Vaucheret (5) , Gad Galili (2) , Pascal Genschik (1)

1 IBMP - Institut de biologie moléculaire des plantes
2 Weizmann Institute of Science [Rehovot, Israël]
3 UGENT - Universiteit Gent = Ghent University [Belgium]
4 BPMP - Biochimie et Physiologie Moléculaire des Plantes
5 IJPB - Institut Jean-Pierre Bourgin

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 VSR P0 manipulates this pathway.

Keywords: autophagy; Arabidopsis; RNA silencing

Domains: Life Sciences [q-bio]

Simon Michaeli, Marion Clavel, Esther Lechner, Corrado Viotti, Jian Wu, 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), pp.22872 - 22883. ⟨10.1073/pnas.1912222116⟩. ⟨hal-03096615⟩