Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution

Abstract DNA-based evolutionary comparisons of regulatory genomic elements enable insight into functional changes driven in cis, partially overcoming tissue inaccessibility. Here, we harnessed adult and fetal cortex single-cell ATAC-seq datasets to uncover DNA substitutions specific to the human and...

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Main Authors: Emre Caglayan, Genevieve Konopka
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60665-w
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author Emre Caglayan
Genevieve Konopka
author_facet Emre Caglayan
Genevieve Konopka
author_sort Emre Caglayan
collection DOAJ
description Abstract DNA-based evolutionary comparisons of regulatory genomic elements enable insight into functional changes driven in cis, partially overcoming tissue inaccessibility. Here, we harnessed adult and fetal cortex single-cell ATAC-seq datasets to uncover DNA substitutions specific to the human and human-ancestral lineages within apes. We found that fetal microglia identity is evolutionarily divergent in all lineages, whereas other cell types are conserved. Using multiomic datasets, we further identified genes linked to multiple lineage-divergent gene regulatory elements and implicated biological pathways associated with these divergent features. We also uncovered patterns of transcription factor binding site evolution across lineages and identified expansion of bHLH-PAS transcription factor targets in human-hominin lineages, and MEF2 transcription factor targets in the ape lineage. Finally, conserved features were more enriched in brain disease variants, whereas there was no distinct enrichment of brain disease variants on the human lineage compared to its ancestral lineages. Our study identifies ancestral evolutionary patterns of the human brain epigenome at cellular resolution.
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spelling doaj-art-bddf087e619148259f01b14840c68eaa2025-08-20T03:03:33ZengNature PortfolioNature Communications2041-17232025-07-0116111210.1038/s41467-025-60665-wDecoding DNA sequence-driven evolution of the human brain epigenome at cellular resolutionEmre Caglayan0Genevieve Konopka1Department of Neuroscience, UT Southwestern Medical CenterDepartment of Neuroscience, UT Southwestern Medical CenterAbstract DNA-based evolutionary comparisons of regulatory genomic elements enable insight into functional changes driven in cis, partially overcoming tissue inaccessibility. Here, we harnessed adult and fetal cortex single-cell ATAC-seq datasets to uncover DNA substitutions specific to the human and human-ancestral lineages within apes. We found that fetal microglia identity is evolutionarily divergent in all lineages, whereas other cell types are conserved. Using multiomic datasets, we further identified genes linked to multiple lineage-divergent gene regulatory elements and implicated biological pathways associated with these divergent features. We also uncovered patterns of transcription factor binding site evolution across lineages and identified expansion of bHLH-PAS transcription factor targets in human-hominin lineages, and MEF2 transcription factor targets in the ape lineage. Finally, conserved features were more enriched in brain disease variants, whereas there was no distinct enrichment of brain disease variants on the human lineage compared to its ancestral lineages. Our study identifies ancestral evolutionary patterns of the human brain epigenome at cellular resolution.https://doi.org/10.1038/s41467-025-60665-w
spellingShingle Emre Caglayan
Genevieve Konopka
Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution
Nature Communications
title Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution
title_full Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution
title_fullStr Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution
title_full_unstemmed Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution
title_short Decoding DNA sequence-driven evolution of the human brain epigenome at cellular resolution
title_sort decoding dna sequence driven evolution of the human brain epigenome at cellular resolution
url https://doi.org/10.1038/s41467-025-60665-w
work_keys_str_mv AT emrecaglayan decodingdnasequencedrivenevolutionofthehumanbrainepigenomeatcellularresolution
AT genevievekonopka decodingdnasequencedrivenevolutionofthehumanbrainepigenomeatcellularresolution