The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA

Thibaut Hacquard; Marion Clavel; Patricia Baldrich; Esther Lechner; Imma Pérez-Salamó; Mikhail Schepetilnikov; Benoît Derrien; Marieke Dubois; Philippe Hammann; Lauriane Kuhn; Danaé Brun; Nathalie Bouteiller; Nicolas Baumberger; Hervé Vaucheret; Blake C. Meyers; Pascal Genschik

doi:10.1016/j.celrep.2022.110671

The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA

Thibaut Hacquard, Marion Clavel, Patricia Baldrich, Esther Lechner, Imma Pérez-Salamó, Mikhail Schepetilnikov, Benoît Derrien, Marieke Dubois, Philippe Hammann, Lauriane Kuhn, Danaé Brun, Nathalie Bouteiller, Nicolas Baumberger, Hervé Vaucheret, Blake C. Meyers, Pascal Genschik

Research output: Contribution to journal › Article › peer-review

17 Scopus citations

Abstract

RNA silencing is a conserved mechanism in eukaryotes involved in development and defense against viruses. In plants, ARGONAUTE1 (AGO1) protein plays a central role in both microRNA- and small interfering RNA-directed silencing, and its expression is regulated at multiple levels. Here, we report that the F-box protein FBW2 assembles an SCF complex that selectively targets for proteolysis AGO1 when it is unloaded and mutated. Although FBW2 loss of function does not lead to strong growth or developmental defects, it significantly increases RNA-silencing activity. Interestingly, under conditions in which small-RNA accumulation is affected, the failure to degrade AGO1 in fbw2 mutants becomes more deleterious for the plant. Accordingly, the non-degradable AGO1 protein assembles high-molecular-weight complexes and binds illegitimate small RNA, leading to off-target cleavage. Therefore, control of AGO1 homeostasis by FBW2 plays an important role in quality control of RNA silencing.

Original language	English
Article number	110671
Journal	Cell Reports
Volume	39
Issue number	2
DOIs	https://doi.org/10.1016/j.celrep.2022.110671
State	Published - Apr 12 2022

Keywords

Arbidopsis
Argonaute proteins
CP: molecular biology
CP: plants
RNA cleavage
RNA silencing
proteolysis

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10.1016/j.celrep.2022.110671

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Hacquard, T., Clavel, M., Baldrich, P., Lechner, E., Pérez-Salamó, I., Schepetilnikov, M., Derrien, B., Dubois, M., Hammann, P., Kuhn, L., Brun, D., Bouteiller, N., Baumberger, N., Vaucheret, H., Meyers, B. C., & Genschik, P. (2022). The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA. Cell Reports, 39(2), Article 110671. https://doi.org/10.1016/j.celrep.2022.110671

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title = "The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA",

abstract = "RNA silencing is a conserved mechanism in eukaryotes involved in development and defense against viruses. In plants, ARGONAUTE1 (AGO1) protein plays a central role in both microRNA- and small interfering RNA-directed silencing, and its expression is regulated at multiple levels. Here, we report that the F-box protein FBW2 assembles an SCF complex that selectively targets for proteolysis AGO1 when it is unloaded and mutated. Although FBW2 loss of function does not lead to strong growth or developmental defects, it significantly increases RNA-silencing activity. Interestingly, under conditions in which small-RNA accumulation is affected, the failure to degrade AGO1 in fbw2 mutants becomes more deleterious for the plant. Accordingly, the non-degradable AGO1 protein assembles high-molecular-weight complexes and binds illegitimate small RNA, leading to off-target cleavage. Therefore, control of AGO1 homeostasis by FBW2 plays an important role in quality control of RNA silencing.",

keywords = "Arbidopsis, Argonaute proteins, CP: molecular biology, CP: plants, RNA cleavage, RNA silencing, proteolysis",

author = "Thibaut Hacquard and Marion Clavel and Patricia Baldrich and Esther Lechner and Imma P{\'e}rez-Salam{\'o} and Mikhail Schepetilnikov and Beno{\^i}t Derrien and Marieke Dubois and Philippe Hammann and Lauriane Kuhn and Dana{\'e} Brun and Nathalie Bouteiller and Nicolas Baumberger and Herv{\'e} Vaucheret and Meyers, {Blake C.} and Pascal Genschik",

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year = "2022",

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Hacquard, T, Clavel, M, Baldrich, P, Lechner, E, Pérez-Salamó, I, Schepetilnikov, M, Derrien, B, Dubois, M, Hammann, P, Kuhn, L, Brun, D, Bouteiller, N, Baumberger, N, Vaucheret, H, Meyers, BC & Genschik, P 2022, 'The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA', Cell Reports, vol. 39, no. 2, 110671. https://doi.org/10.1016/j.celrep.2022.110671

TY - JOUR

T1 - The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA

AU - Hacquard, Thibaut

AU - Clavel, Marion

AU - Baldrich, Patricia

AU - Lechner, Esther

AU - Pérez-Salamó, Imma

AU - Schepetilnikov, Mikhail

AU - Derrien, Benoît

AU - Dubois, Marieke

AU - Hammann, Philippe

AU - Kuhn, Lauriane

AU - Brun, Danaé

AU - Bouteiller, Nathalie

AU - Baumberger, Nicolas

AU - Vaucheret, Hervé

AU - Meyers, Blake C.

AU - Genschik, Pascal

PY - 2022/4/12

Y1 - 2022/4/12

N2 - RNA silencing is a conserved mechanism in eukaryotes involved in development and defense against viruses. In plants, ARGONAUTE1 (AGO1) protein plays a central role in both microRNA- and small interfering RNA-directed silencing, and its expression is regulated at multiple levels. Here, we report that the F-box protein FBW2 assembles an SCF complex that selectively targets for proteolysis AGO1 when it is unloaded and mutated. Although FBW2 loss of function does not lead to strong growth or developmental defects, it significantly increases RNA-silencing activity. Interestingly, under conditions in which small-RNA accumulation is affected, the failure to degrade AGO1 in fbw2 mutants becomes more deleterious for the plant. Accordingly, the non-degradable AGO1 protein assembles high-molecular-weight complexes and binds illegitimate small RNA, leading to off-target cleavage. Therefore, control of AGO1 homeostasis by FBW2 plays an important role in quality control of RNA silencing.

AB - RNA silencing is a conserved mechanism in eukaryotes involved in development and defense against viruses. In plants, ARGONAUTE1 (AGO1) protein plays a central role in both microRNA- and small interfering RNA-directed silencing, and its expression is regulated at multiple levels. Here, we report that the F-box protein FBW2 assembles an SCF complex that selectively targets for proteolysis AGO1 when it is unloaded and mutated. Although FBW2 loss of function does not lead to strong growth or developmental defects, it significantly increases RNA-silencing activity. Interestingly, under conditions in which small-RNA accumulation is affected, the failure to degrade AGO1 in fbw2 mutants becomes more deleterious for the plant. Accordingly, the non-degradable AGO1 protein assembles high-molecular-weight complexes and binds illegitimate small RNA, leading to off-target cleavage. Therefore, control of AGO1 homeostasis by FBW2 plays an important role in quality control of RNA silencing.

KW - Arbidopsis

KW - Argonaute proteins

KW - CP: molecular biology

KW - CP: plants

KW - RNA cleavage

KW - RNA silencing

KW - proteolysis

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DO - 10.1016/j.celrep.2022.110671

M3 - Article

C2 - 35417704

AN - SCOPUS:85128118518

SN - 2639-1856

VL - 39

JO - Cell Reports

JF - Cell Reports

IS - 2

M1 - 110671

ER -

The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA

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