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Co-surveillance of ribosomal RNA by the exosome complex and nucleolar RNAi in C. elegans

Shimiao Liao, Xiangyang Chen, Ting Xu, Qile Jin, Zongxiu Xu, Demin Xu, Xufei Zhou, Chengming Zhu, Shouhong Guang, Xuezhu Feng
doi: https://doi.org/10.1101/2020.11.23.395020
Shimiao Liao
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Xiangyang Chen
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Ting Xu
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Qile Jin
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Zongxiu Xu
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Demin Xu
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Xufei Zhou
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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Chengming Zhu
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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  • For correspondence: zcm916@ustc.edu.cn sguang@ustc.edu.cn fengxz@ustc.edu.cn
Shouhong Guang
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
2CAS Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, Hefei, Anhui 230027, P.R. China
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  • For correspondence: zcm916@ustc.edu.cn sguang@ustc.edu.cn fengxz@ustc.edu.cn
Xuezhu Feng
1Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230027, P.R. China
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  • For correspondence: zcm916@ustc.edu.cn sguang@ustc.edu.cn fengxz@ustc.edu.cn
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Abstract

Eukaryotic cells express a wide variety of endogenous small regulatory RNAs that function in the nucleus. We previously found that erroneous rRNAs induce the generation of antisense ribosomal siRNAs (risiRNAs) which silence the expression of rRNAs via the nuclear RNAi defective (Nrde) pathway. To further understand the biological roles and mechanisms of this class of small regulatory RNAs, we conducted forward genetic screening to identify factors involved in risiRNA generation in Caenorhabditis elegans. We found that risiRNAs accumulated in the RNA exosome mutants. risiRNAs directed a NRDE-dependent silencing of pre-rRNAs in the nucleolus. In the presence of risiRNA, NRDE-2 accumulated in the nucleolus and colocalized with RNA polymerase I. risiRNA inhibited the transcription elongation of RNA polymerase I by decreasing RNAP I occupancy downstream of the site of RNAi. Meanwhile, exosome mislocalized from the nucleolus to nucleoplasm in suppressor of siRNA (susi) mutants, in which erroneous rRNAs accumulated. These results establish a novel model of rRNA surveillance by combining ribonuclease-mediated RNA degradation with small RNA-directed nucleolar RNAi system.

Competing Interest Statement

The authors have declared no competing interest.

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Posted November 24, 2020.
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Co-surveillance of ribosomal RNA by the exosome complex and nucleolar RNAi in C. elegans
Shimiao Liao, Xiangyang Chen, Ting Xu, Qile Jin, Zongxiu Xu, Demin Xu, Xufei Zhou, Chengming Zhu, Shouhong Guang, Xuezhu Feng
bioRxiv 2020.11.23.395020; doi: https://doi.org/10.1101/2020.11.23.395020
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Co-surveillance of ribosomal RNA by the exosome complex and nucleolar RNAi in C. elegans
Shimiao Liao, Xiangyang Chen, Ting Xu, Qile Jin, Zongxiu Xu, Demin Xu, Xufei Zhou, Chengming Zhu, Shouhong Guang, Xuezhu Feng
bioRxiv 2020.11.23.395020; doi: https://doi.org/10.1101/2020.11.23.395020

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