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Nucleo-cytosolic Shuttling of ARGONAUTE1 Prompts a Revised Model of the Plant MicroRNA Pathway.

  • Bologna NG Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland.
  • Iselin R Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland.
  • Abriata LA Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland; Swiss Institute of Bioinformatics, Lausanne 1015, Switzerland.
  • Sarazin A Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland.
  • Pumplin N Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland; Department of Plant Sciences, University of California, Davis, California 95616, USA.
  • Jay F Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland.
  • Grentzinger T Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland.
  • Dal Peraro M Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland; Swiss Institute of Bioinformatics, Lausanne 1015, Switzerland.
  • Voinnet O Department of Biology, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, Zürich 8092, Switzerland. Electronic address: voinneto@ethz.ch.
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  • 2018-02-06
Published in:
  • Molecular cell. - 2018
Active Transport, Cell Nucleus
Arabidopsis
Arabidopsis Proteins
Argonaute Proteins
Cell Nucleus
Cytosol
Gene Expression Regulation, Plant
MicroRNAs
Models, Molecular
Protein Transport
Subcellular Fractions
English Unlike in metazoans, plant microRNAs (miRNAs) undergo stepwise nuclear maturation before engaging cytosolic, sequence-complementary transcripts in association with the silencing effector protein ARGONAUTE1 (AGO1). Since their discovery, how and under which form plant miRNAs translocate to the cytosol has remained unclear, as has their sub-cellular AGO1 loading site(s). Here, we show that the N termini of all plant AGO1s contain a nuclear-localization (NLS) and nuclear-export signal (NES) that, in Arabidopsis thaliana (At), enables AtAGO1 nucleo-cytosolic shuttling in a Leptomycin-B-inhibited manner, diagnostic of CRM1(EXPO1)/NES-dependent nuclear export. Nuclear-only AtAGO1 contains the same 2'O-methylated miRNA cohorts as its nucleo-cytosolic counterpart, but it preferentially interacts with the miRNA loading chaperone HSP90. Furthermore, mature miRNA translocation and miRNA-mediated silencing both require AtAGO1 nucleo-cytosolic shuttling. These findings lead us to propose a substantially revised view of the plant miRNA pathway in which miRNAs are matured, methylated, loaded into AGO1 in the nucleus, and exported to the cytosol as AGO1:miRNA complexes in a CRM1(EXPO1)/NES-dependent manner.
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  • English
Open access status
bronze
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https://sonar.ch/global/documents/98954
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