rRNA intermediates coordinate the formation of nucleolar vacuoles in C. elegans

Demin Xu; Xiangyang Chen; Yan Kuang; Minjie Hong; Ting Xu; Ke Wang; Xinya Huang; Chuanhai Fu; Ke Ruan; Chengming Zhu; Xuezhu Feng; Shouhong Guang

doi:10.1016/j.celrep.2023.112915

rRNA intermediates coordinate the formation of nucleolar vacuoles in C. elegans

Cell Rep. 2023 Aug 29;42(8):112915. doi: 10.1016/j.celrep.2023.112915. Epub 2023 Aug 1.

Authors

Demin Xu¹, Xiangyang Chen¹, Yan Kuang¹, Minjie Hong¹, Ting Xu¹, Ke Wang¹, Xinya Huang¹, Chuanhai Fu¹, Ke Ruan¹, Chengming Zhu², Xuezhu Feng³, Shouhong Guang⁴

Affiliations

¹ Department of Obstetrics and Gynecology, The First Affiliated Hospital of USTC, The USTC RNA Institute, Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, Biomedical Sciences and Health Laboratory of Anhui Province, University of Science and Technology of China, Hefei, Anhui 230027, China.
² Department of Obstetrics and Gynecology, The First Affiliated Hospital of USTC, The USTC RNA Institute, Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, Biomedical Sciences and Health Laboratory of Anhui Province, University of Science and Technology of China, Hefei, Anhui 230027, China. Electronic address: zcm916@ustc.edu.cn.
³ Department of Obstetrics and Gynecology, The First Affiliated Hospital of USTC, The USTC RNA Institute, Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, Biomedical Sciences and Health Laboratory of Anhui Province, University of Science and Technology of China, Hefei, Anhui 230027, China. Electronic address: fengxz@ustc.edu.cn.
⁴ Department of Obstetrics and Gynecology, The First Affiliated Hospital of USTC, The USTC RNA Institute, Ministry of Education Key Laboratory for Membraneless Organelles & Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, Biomedical Sciences and Health Laboratory of Anhui Province, University of Science and Technology of China, Hefei, Anhui 230027, China; CAS Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, Hefei, Anhui 230027, China. Electronic address: sguang@ustc.edu.cn.

PMID: 37537842
DOI: 10.1016/j.celrep.2023.112915

Abstract

The nucleolus is the most prominent membraneless organelle within the nucleus. How the nucleolar structure is regulated is poorly understood. Here, we identified two types of nucleoli in C. elegans. Type I nucleoli are spherical and do not have visible nucleolar vacuoles (NoVs), and rRNA transcription and processing factors are evenly distributed throughout the nucleolus. Type II nucleoli contain vacuoles, and rRNA transcription and processing factors exclusively accumulate in the periphery rim. The NoV contains nucleoplasmic proteins and is capable of exchanging contents with the nucleoplasm. The high-order structure of the nucleolus is dynamically regulated in C. elegans. Faithful rRNA processing is important to prohibit NoVs. The depletion of 27SA₂ rRNA processing factors resulted in NoV formation. The inhibition of RNA polymerase I (RNAPI) transcription and depletion of two conserved nucleolar factors, nucleolin and fibrillarin, prohibits the formation of NoVs. This finding provides a mechanism to coordinate structure maintenance and gene expression.

Keywords: CP: Cell biology; CP: Molecular biology; RNAPI; nucleolus; phase transition; rRNA; reshaping; ring; vacuole.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Caenorhabditis elegans* / genetics
Caenorhabditis elegans* / metabolism
Cell Nucleolus / metabolism
Cell Nucleus / metabolism
Nuclear Proteins* / metabolism
RNA, Ribosomal / metabolism
Vacuoles / metabolism

Substances

Nuclear Proteins
RNA, Ribosomal

Grants and funding

P40 OD010440/OD/NIH HHS/United States