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Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology

View ORCID ProfileRohini R. Nair, Dimitry Zabezhinsky, Rita Gelin-Licht, Brian Haas, Michael C.A. Dyhr, View ORCID ProfileHannah S. Sperber, Chad Nusbaum, View ORCID ProfileJeffrey E. Gerst
doi: https://doi.org/10.1101/2020.06.28.175851
Rohini R. Nair
1Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel
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  • ORCID record for Rohini R. Nair
Dimitry Zabezhinsky
1Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel
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Rita Gelin-Licht
1Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel
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Brian Haas
2Broad Institute of MIT and Harvard, 415 Main St., Cambridge, MA 02142, USA
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Michael C.A. Dyhr
1Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel
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Hannah S. Sperber
1Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel
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  • ORCID record for Hannah S. Sperber
Chad Nusbaum
2Broad Institute of MIT and Harvard, 415 Main St., Cambridge, MA 02142, USA
3Cellarity Inc., 55 Cambridge Pkwy, Cambridge, MA 02142, USA
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Jeffrey E. Gerst
1Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel
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  • ORCID record for Jeffrey E. Gerst
  • For correspondence: jeffrey.gerst@weizmann.ac.il
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Abstract

Prokaryotes utilize polycistronic messages (operons) to co-translate proteins involved in the same biological process. Whether eukaryotes achieve similar regulation by selectively assembling monocistronic messages derived from different chromosomes is unclear. We employed transcript-specific RNA pulldowns and RNA-seq/RT-PCR to identify mRNAs that co-precipitate into ribonucleoprotein (RNP) particles in yeast. Consistent with the hypothesis of eukaryotic RNA operons, mRNAs encoding components of the mating pathway, heat shock proteins, and mitochondrial outer membrane proteins multiplex in trans to form discrete mRNP particles, termed transperons. Chromatin-capture experiments reveal that genes encoding multiplexed mRNAs physically interact, thus, RNA assembly may result from co-regulated gene expression. Transperon assembly and function depends upon H4 histones and their depletion leads to defects in RNA multiplexing, resulting in decreased pheromone responsiveness and mating, and increased heat shock sensitivity. We propose that intergenic associations and non-canonical H4 histone functions contribute to transperon formation in eukaryotic cells to regulate cell physiology.

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Competing Interest Statement

The authors have declared no competing interest.

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Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
Rohini R. Nair, Dimitry Zabezhinsky, Rita Gelin-Licht, Brian Haas, Michael C.A. Dyhr, Hannah S. Sperber, Chad Nusbaum, Jeffrey E. Gerst
bioRxiv 2020.06.28.175851; doi: https://doi.org/10.1101/2020.06.28.175851
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Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
Rohini R. Nair, Dimitry Zabezhinsky, Rita Gelin-Licht, Brian Haas, Michael C.A. Dyhr, Hannah S. Sperber, Chad Nusbaum, Jeffrey E. Gerst
bioRxiv 2020.06.28.175851; doi: https://doi.org/10.1101/2020.06.28.175851

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