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Gene expression and complex phenotypes are determined by the activity of cis-regulatory elements. However, an understanding of how extant genetic variants affect cis regulation remains limited. Here, we investigated the consequences of cis-regulatory diversity using single-cell genomics of more than 0.7 million nuclei across 172Zea mays(maize) inbreds. Our analyses pinpointed cis-regulatory elements distinct to domesticated maize and revealed how historical transposon activity has shaped the cis-regulatory landscape. Leveraging population genetics principles, we fine-mapped about 22,000 chromatin accessibility–associated genetic variants with widespread cell type–specific effects. Variants in TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR–binding sites were the most prevalent determinants of chromatin accessibility. Finally, integrating chromatin accessibility–associated variants, organismal trait variation, and population differentiation revealed how local adaptation has rewired regulatory networks in unique cellular contexts to alter maize flowering. 

Abstract Cis-regulatory elements (CREs) are essential for regulating gene expression, yet their evolutionary dynamics in plants remain elusive. Here we constructed a single-cell chromatin accessibility atlas forOryza sativafrom 103,911 nuclei representing 126 cell states across nine organs. Comparative genomics betweenO. sativaand 57,552 nuclei from four additional grass species (Zea mays,Sorghum bicolor,Panicum miliaceumandUrochloa fusca) revealed that chromatin accessibility conservation varies with cell-type specificity. Epidermal accessible chromatin regions in the leaf were less conserved compared to other cell types, indicating accelerated regulatory evolution in the L1-derived epidermal layer ofO. sativarelative to other species. Conserved accessible chromatin regions overlapping the repressive histone modification H3K27me3 were identified as potentially silencer-like CREs, as deleting these regions led to up-regulation of gene expression. This study provides a comprehensive epigenomic resource for the rice community, demonstrating the utility of a comparative genomics approach that highlights the dynamics of plant cell-type-specific CRE evolution. 

SUMMARY Cis‐regulatory elements (CREs) are important sequences for gene expression and for plant biological processes such as development, evolution, domestication, and stress response. However, studying CREs in plant genomes has been challenging. The totipotent nature of plant cells, coupled with the inability to maintain plant cell types in culture and the inherent technical challenges posed by the cell wall has limited our understanding of how plant cell types acquire and maintain their identities and respond to the environment via CRE usage. Advances in single‐cell epigenomics have revolutionized the field of identifying cell‐type‐specific CREs. These new technologies have the potential to significantly advance our understanding of plant CRE biology, and shed light on how the regulatory genome gives rise to diverse plant phenomena. However, there are significant biological and computational challenges associated with analyzing single‐cell epigenomic datasets. In this review, we discuss the historical and foundational underpinnings of plant single‐cell research, challenges, and common pitfalls in the analysis of plant single‐cell epigenomic data, and highlight biological challenges unique to plants. Additionally, we discuss how the application of single‐cell epigenomic data in various contexts stands to transform our understanding of the importance of CREs in plant genomes.