Nuclear gene proximity and protein interactions shape transcript covariations in mammalian single cells

Marcel Tarbier, Sebastian D. Mackowiak, João Frade, Silvina Catuara-Solarz, Inna Biryukova, Eleni Gelali, Diego Bárcena Menéndez, Luis Zapata, Stephan Ossowski, Magda Bienko, Caroline J. Gallant and Marc R. Friedländer ()
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Marcel Tarbier: Stockholm University
Sebastian D. Mackowiak: Stockholm University
João Frade: The Barcelona Institute for Science and Technology
Silvina Catuara-Solarz: The Barcelona Institute for Science and Technology
Inna Biryukova: Stockholm University
Eleni Gelali: Karolinska Institute
Diego Bárcena Menéndez: The Barcelona Institute for Science and Technology
Luis Zapata: The Barcelona Institute for Science and Technology
Stephan Ossowski: The Barcelona Institute for Science and Technology
Magda Bienko: Karolinska Institute
Caroline J. Gallant: Uppsala University
Marc R. Friedländer: Stockholm University

Nature Communications, 2020, vol. 11, issue 1, 1-12

Abstract: Abstract Single-cell RNA sequencing studies on gene co-expression patterns could yield important regulatory and functional insights, but have so far been limited by the confounding effects of differentiation and cell cycle. We apply a tailored experimental design that eliminates these confounders, and report thousands of intrinsically covarying gene pairs in mouse embryonic stem cells. These covariations form a network with biological properties, outlining known and novel gene interactions. We provide the first evidence that miRNAs naturally induce transcriptome-wide covariations and compare the relative importance of nuclear organization, transcriptional and post-transcriptional regulation in defining covariations. We find that nuclear organization has the greatest impact, and that genes encoding for physically interacting proteins specifically tend to covary, suggesting importance for protein complex formation. Our results lend support to the concept of post-transcriptional RNA operons, but we further present evidence that nuclear proximity of genes may provide substantial functional regulation in mammalian single cells.

Date: 2020
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DOI: 10.1038/s41467-020-19011-5

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