The dynamic genetic determinants of increased transcriptional divergence in spermatids

Jasper Panten, Tobias Heinen, Christina Ernst, Nils Eling, Rebecca E. Wagner, Maja Satorius, John C. Marioni, Oliver Stegle () and Duncan T. Odom ()
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Jasper Panten: German Cancer Research Centre (DKFZ)
Tobias Heinen: German Cancer Research Centre (DKFZ)
Christina Ernst: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Nils Eling: University of Zurich, Department of Quantitative Biomedicine
Rebecca E. Wagner: Heidelberg University
Maja Satorius: German Cancer Research Centre (DKFZ)
John C. Marioni: University of Cambridge
Oliver Stegle: German Cancer Research Centre (DKFZ)
Duncan T. Odom: German Cancer Research Centre (DKFZ)

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract Cis-genetic effects are key determinants of transcriptional divergence in discrete tissues and cell types. However, how cis- and trans-effects act across continuous trajectories of cellular differentiation in vivo is poorly understood. Here, we quantify allele-specific expression during spermatogenic differentiation at single-cell resolution in an F1 hybrid mouse system, allowing for the comprehensive characterisation of cis- and trans-genetic effects, including their dynamics across cellular differentiation. Collectively, almost half of the genes subject to genetic regulation show evidence for dynamic cis-effects that vary during differentiation. Our system also allows us to robustly identify dynamic trans-effects, which are less pervasive than cis-effects. In aggregate, genetic effects were strongest in round spermatids, which parallels their increased transcriptional divergence we identified between species. Our approach provides a comprehensive quantification of the variability of genetic effects in vivo, and demonstrates a widely applicable strategy to dissect the impact of regulatory variants on gene regulation in dynamic systems.

Date: 2024
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DOI: 10.1038/s41467-024-45133-1

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