Decoding gene regulation in the fly brain

Jasper Janssens, Sara Aibar, Ibrahim Ihsan Taskiran, Joy N. Ismail, Alicia Estacio Gomez, Gabriel Aughey, Katina I. Spanier, Florian V. Rop, Carmen Bravo González-Blas, Marc Dionne, Krista Grimes, Xiao Jiang Quan, Dafni Papasokrati, Gert Hulselmans, Samira Makhzami, Maxime Waegeneer, Valerie Christiaens, Tony Southall and Stein Aerts ()
Additional contact information
Jasper Janssens: VIB Center for Brain & Disease Research
Sara Aibar: VIB Center for Brain & Disease Research
Ibrahim Ihsan Taskiran: VIB Center for Brain & Disease Research
Joy N. Ismail: VIB Center for Brain & Disease Research
Alicia Estacio Gomez: Imperial College London
Gabriel Aughey: Imperial College London
Katina I. Spanier: VIB Center for Brain & Disease Research
Florian V. Rop: VIB Center for Brain & Disease Research
Carmen Bravo González-Blas: VIB Center for Brain & Disease Research
Marc Dionne: Imperial College London
Krista Grimes: Imperial College London
Xiao Jiang Quan: VIB Center for Brain & Disease Research
Dafni Papasokrati: VIB Center for Brain & Disease Research
Gert Hulselmans: VIB Center for Brain & Disease Research
Samira Makhzami: VIB Center for Brain & Disease Research
Maxime Waegeneer: VIB Center for Brain & Disease Research
Valerie Christiaens: VIB Center for Brain & Disease Research
Tony Southall: Imperial College London
Stein Aerts: VIB Center for Brain & Disease Research

Nature, 2022, vol. 601, issue 7894, 630-636

Abstract: Abstract The Drosophila brain is a frequently used model in neuroscience. Single-cell transcriptome analysis1–6, three-dimensional morphological classification7 and electron microscopy mapping of the connectome8,9 have revealed an immense diversity of neuronal and glial cell types that underlie an array of functional and behavioural traits in the fly. The identities of these cell types are controlled by gene regulatory networks (GRNs), involving combinations of transcription factors that bind to genomic enhancers to regulate their target genes. Here, to characterize GRNs at the cell-type level in the fly brain, we profiled the chromatin accessibility of 240,919 single cells spanning 9 developmental timepoints and integrated these data with single-cell transcriptomes. We identify more than 95,000 regulatory regions that are used in different neuronal cell types, of which 70,000 are linked to developmental trajectories involving neurogenesis, reprogramming and maturation. For 40 cell types, uniquely accessible regions were associated with their expressed transcription factors and downstream target genes through a combination of motif discovery, network inference and deep learning, creating enhancer GRNs. The enhancer architectures revealed by DeepFlyBrain lead to a better understanding of neuronal regulatory diversity and can be used to design genetic driver lines for cell types at specific timepoints, facilitating their characterization and manipulation.

Date: 2022
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DOI: 10.1038/s41586-021-04262-z

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