Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
- Weizmann Institute of Science, Israel
- Broad Institute of MIT and Harvard, United States
Abstract
Prokaryotes utilize polycistronic messages (operons) to co-translate proteins involved in the same biological processes. Whether eukaryotes achieve similar regulation by selectively assembling and translating monocistronic messages derived from different chromosomes is unknown. We employed transcript-specific RNA pulldowns and RNA-seq/RT-PCR to identify yeast mRNAs that co-precipitate as ribonucleoprotein (RNP) complexes. 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, forming discrete mRNP complexes (called transperons). Chromatin-capture and allele tagging 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 histone H4 and depletion leads to defects in RNA multiplexing, decreased pheromone responsiveness and mating, and increased heat shock sensitivity. We propose that intergenic associations and non-canonical histone H4 functions contribute to transperon formation in eukaryotic cells and regulate cell physiology.
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Funding
German-Israeli Foundation for Scientific Research and Development (I-1190-96.13/2012)
- Jeffrey E Gerst
Minerva Foundation (711130)
- Jeffrey E Gerst
Astrachan Olga Klein Fund, Weizmann Institute
- Jeffrey E Gerst
National Institutes of Health (NHGRI U54HG00306)
- Chad Nusbaum
Israel Council of Higher Education
- Rita Gelin-Licht
Israel Science Foundation (578/18)
- Jeffrey E Gerst
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Nair et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
eLife 10:e66050.
https://doi.org/10.7554/eLife.66050
