Inter- and intraspecific constraint of accessible chromatins maps regulatory loci involved in maize speciation and domestication

Comparative genomic studies have the capability to find genes that are either under evolutionary constraint for organismal living or specialized for trait innovations. Meanwhile, there is a growing body of evidence suggesting that evolutionary constraint can also happen on non-coding regulatory sequences, exerting profound effects on fitness traits. However, the majority of these evidences originate from primate studies and has yet to be thoroughly explored in plants. In this study, we adopt assay for transposase-accessible chromatin using sequencing (ATAC-seq) to profile the inter- and intraspecific constraint of over 80,000 maize accessible chromatin regions (ACRs). Our findings reveal that ACRs exhibit accelerated evolution over coding genes, resulting in approximately one-third of ACRs that specifically existed in maize lineage and exerting prominent transcriptional effects on genes associated with speciation. We highlight the role of transposable elements (TEs) in driving intraspecific innovation of ACRs, and uncover hundreds of candidate ACRs that likely involved in the transcriptional rewiring of genes during maize domestication. Furthermore, we demonstrate the importance of accessible chromatins in maintaining maize subgenome dominance and controlling complex trait variations. Our work establishes a new framework for analyzing the evolutionary trajectory of extensive plant regulatory sequences, and offers some candidate loci for downstream exploration and application during maize breeding.