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Ribosome stalling caused by the Argonaute-microRNA-SGS3 complex regulates the production of secondary siRNAs in plants

View ORCID ProfileHiro-oki Iwakawa, Andy Y.W. Lam, View ORCID ProfileAkira Mine, Tomoya Fujita, Kaori Kiyokawa, Manabu Yoshikawa, Atsushi Takeda, View ORCID ProfileShintaro Iwasaki, View ORCID ProfileYukihide Tomari
doi: https://doi.org/10.1101/2020.09.10.288902
Hiro-oki Iwakawa
1Laboratory of RNA Function, Institute for Quantitative Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
2JST, PRESTO, Saitama 332-0012, Japan
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  • For correspondence: iwakawa@iqb.u-tokyo.ac.jp
Andy Y.W. Lam
1Laboratory of RNA Function, Institute for Quantitative Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
3Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
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Akira Mine
2JST, PRESTO, Saitama 332-0012, Japan
4Ritsumeikan Global Innovation Research Organization, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan
5Department of Biotechnology, Graduate School of Life Sciences, Ritsumeikan University, Shiga 525-8577, Japan
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Tomoya Fujita
6RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, Saitama, 351-0198 Japan
7School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Kanagawa, 226-8503 Japan
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Kaori Kiyokawa
1Laboratory of RNA Function, Institute for Quantitative Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
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Manabu Yoshikawa
8Division of Plant and Microbial Sciences, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai Tsukuba, Ibaraki 305-8602, Japan
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Atsushi Takeda
4Ritsumeikan Global Innovation Research Organization, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan
5Department of Biotechnology, Graduate School of Life Sciences, Ritsumeikan University, Shiga 525-8577, Japan
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Shintaro Iwasaki
3Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
6RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, Saitama, 351-0198 Japan
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Yukihide Tomari
1Laboratory of RNA Function, Institute for Quantitative Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
3Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
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Abstract

The path of ribosomes on mRNAs can be impeded by various obstacles. One such example is halting of ribosome movement by microRNAs, though the exact mechanism and physiological role remain unclear. Here, we find that ribosome stalling caused by the Argonaute-microRNA-SGS3 complex regulates the production of secondary small interfering RNAs (siRNAs) in plants. We show that the double-stranded RNA-binding protein SGS3 directly interacts with the 3′ end of the microRNA in an Argonaute protein, resulting in ribosome stalling. Importantly, microRNA-mediated ribosome stalling positively correlates with efficient production of secondary siRNAs from target mRNAs. Our results illustrate a role for paused ribosomes in regulation of small RNA function that may have broad biological implications across the plant kingdom.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Title, abstract and text updated.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 05, 2021.
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Ribosome stalling caused by the Argonaute-microRNA-SGS3 complex regulates the production of secondary siRNAs in plants
Hiro-oki Iwakawa, Andy Y.W. Lam, Akira Mine, Tomoya Fujita, Kaori Kiyokawa, Manabu Yoshikawa, Atsushi Takeda, Shintaro Iwasaki, Yukihide Tomari
bioRxiv 2020.09.10.288902; doi: https://doi.org/10.1101/2020.09.10.288902
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Ribosome stalling caused by the Argonaute-microRNA-SGS3 complex regulates the production of secondary siRNAs in plants
Hiro-oki Iwakawa, Andy Y.W. Lam, Akira Mine, Tomoya Fujita, Kaori Kiyokawa, Manabu Yoshikawa, Atsushi Takeda, Shintaro Iwasaki, Yukihide Tomari
bioRxiv 2020.09.10.288902; doi: https://doi.org/10.1101/2020.09.10.288902

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