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Monoallelically-expressed Noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

Qinyu Hao, Minxue Liu, Swapna Vidhur Daulatabad, Saba Gaffari, View ORCID ProfileRajneesh Srivastava, You Jin Song, Shivang Bhaskar, Anurupa Moitra, Hazel Mangan, Elizabeth Tseng, Rachel B. Gilmore, Susan M. Freier, Xin Chen, Chengliang Wang, Sui Huang, Stormy Chamberlain, Hong Jin, Jonas Korlach, Brian McStay, Saurabh Sinha, View ORCID ProfileSarath Chandra Janga, Supriya G. Prasanth, View ORCID ProfileKannanganattu V. Prasanth
doi: https://doi.org/10.1101/2022.07.04.498693
Qinyu Hao
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Minxue Liu
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Swapna Vidhur Daulatabad
2Department of BioHealth Informatics, School of Informatics and Computing, IUPUI, Indianapolis, IN, USA
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Saba Gaffari
3Department of Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Rajneesh Srivastava
2Department of BioHealth Informatics, School of Informatics and Computing, IUPUI, Indianapolis, IN, USA
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  • ORCID record for Rajneesh Srivastava
You Jin Song
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Shivang Bhaskar
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Anurupa Moitra
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Hazel Mangan
4Centre for Chromosome Biology, School of Natural Sciences, National University of Ireland Galway, Galway H91 W2TY, Ireland
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Elizabeth Tseng
5Pacific Biosciences, Menlo Park, CA 94025, U.S.A.
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Rachel B. Gilmore
6Department of Genetics and Genome Sciences, University of Connecticut School of Medicine, Farmington, CT 06030, USA.
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Susan M. Freier
7Ionis Pharmaceuticals Inc., Carlsbad, California 92008, USA.
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Xin Chen
8Department of Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Chengliang Wang
9Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Sui Huang
10Department of Cell and Molecular Biology, Northwestern University, Chicago, IL-60611, USA
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Stormy Chamberlain
6Department of Genetics and Genome Sciences, University of Connecticut School of Medicine, Farmington, CT 06030, USA.
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Hong Jin
8Department of Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
9Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, IL, USA
11Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA;
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Jonas Korlach
5Pacific Biosciences, Menlo Park, CA 94025, U.S.A.
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Brian McStay
4Centre for Chromosome Biology, School of Natural Sciences, National University of Ireland Galway, Galway H91 W2TY, Ireland
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Saurabh Sinha
3Department of Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL, USA
12Cancer Center at Illinois, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Sarath Chandra Janga
2Department of BioHealth Informatics, School of Informatics and Computing, IUPUI, Indianapolis, IN, USA
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Supriya G. Prasanth
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
12Cancer Center at Illinois, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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Kannanganattu V. Prasanth
1Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
12Cancer Center at Illinois, University of Illinois at Urbana-Champaign, Urbana, IL, USA
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  • For correspondence: kumarp@illinois.edu
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ABSTRACT

Out of the several hundred copies of rRNA genes that are arranged in the nucleolar organizing regions (NOR) of the five human acrocentric chromosomes, ∼50% remain transcriptionally inactive. NOR-associated sequences and epigenetic modifications contribute to differential expression of rRNAs. However, the mechanism(s), controlling the dosage of active versus inactive rRNA genes in mammals is yet to be determined. We have discovered a family of ncRNAs, SNULs (Single NUcleolus Localized RNA), which form constrained sub-nucleolar territories on individual NORs and influences rRNA expression. Individual members of the SNULs monoallelically associate with specific NOR-containing chromosome. SNULs share sequence similarity to pre-rRNA and localize in the sub-nucleolar compartment with pre-rRNA. Finally, SNULs control rRNA expression by influencing pre-rRNA sorting to the DFC compartment and pre-rRNA processing. Our study discovered a novel class of ncRNAs that by forming constrained nucleolar territories on individual NORs contribute to rRNA expression.

Competing Interest Statement

The authors have declared no competing interest.

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 4.0 International license.
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Posted July 04, 2022.
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Monoallelically-expressed Noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression
Qinyu Hao, Minxue Liu, Swapna Vidhur Daulatabad, Saba Gaffari, Rajneesh Srivastava, You Jin Song, Shivang Bhaskar, Anurupa Moitra, Hazel Mangan, Elizabeth Tseng, Rachel B. Gilmore, Susan M. Freier, Xin Chen, Chengliang Wang, Sui Huang, Stormy Chamberlain, Hong Jin, Jonas Korlach, Brian McStay, Saurabh Sinha, Sarath Chandra Janga, Supriya G. Prasanth, Kannanganattu V. Prasanth
bioRxiv 2022.07.04.498693; doi: https://doi.org/10.1101/2022.07.04.498693
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Monoallelically-expressed Noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression
Qinyu Hao, Minxue Liu, Swapna Vidhur Daulatabad, Saba Gaffari, Rajneesh Srivastava, You Jin Song, Shivang Bhaskar, Anurupa Moitra, Hazel Mangan, Elizabeth Tseng, Rachel B. Gilmore, Susan M. Freier, Xin Chen, Chengliang Wang, Sui Huang, Stormy Chamberlain, Hong Jin, Jonas Korlach, Brian McStay, Saurabh Sinha, Sarath Chandra Janga, Supriya G. Prasanth, Kannanganattu V. Prasanth
bioRxiv 2022.07.04.498693; doi: https://doi.org/10.1101/2022.07.04.498693

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