A cis-regulatory atlas in maize at single-cell resolution

Abstract

Cis-regulatory elements (CREs) encode the genomic blueprints of spatiotemporal gene expression programs enabling highly specialized cell functions. To identify CREs at cell-type resolution in Zea mays, we implemented single-cell sequencing of Assay for Transposase Accessible Chromatin (scATAC-seq) in seedlings, embryonic roots, crown roots, axillary buds, and pistillate and staminate inflorescence. We describe 92 states of chromatin accessibility across 165,913 putative CREs and 52 known cell types. Patterns of transcription factor (TF) motif accessibility predicted cell identity with high accuracy, uncovered putative non-cell autonomous TFs, and revealed TF motifs underlying higher-order chromatin interactions. Comparison of maize and Arabidopsis thaliana developmental trajectories identified TF motifs with conserved patterns of accessibility. Cell type-specific CREs were enriched with enhancer activity, phenotype-associated genetic variants, and signatures of breeding-era selection. These data, along with companion software, Socrates, afford a comprehensive framework for understanding cellular heterogeneity, evolution, and cis-regulatory grammar of cell-type specification in a major crop.