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Cis-regulatory elements are specific DNA sequences that control gene expression in a spatiotemporal manner, and variation within these elements represents a major source of phenotypic diversity and evolutionary innovation. Nevertheless, how regulatory elements evolve and shape gene expression remains poorly understood, particularly in plants. The well-resolved phylogeny of allopolyploid peanut (Arachis hypogaea) and its diploid progenitors,Arachis duranensisandArachis ipaensis, provides an ideal system to investigate the regulatory evolution at a lineage-specific level. By integrating comparative analyses of sequence similarity, chromatin accessibility, histone modifications, conserved noncoding sequences (CNSs), and gene expression, we reconstructed the evolutionary trajectories of Accessible Chromatin Regions (ACRs), where regulatory elements typically reside, and revealed their distinct contributions to homoeolog expression bias, unequal expressions between homoeologs. Most ACRs exhibited high sequence similarity, comparable chromatin accessibility, and conserved states for H3K4me3, H3K56ac, and H3K36me3, indicating regulatory stability after hybridization and polyploidization. However, a subset of novel ACRs emerged de novo from previously nonregulatory regions or through sequence mutations in preexisting ACRs, arising at different rates and evolutionary stages. Notably, even highly sequence-conserved ACRs exhibited substantial variation in chromatin accessibility, consistent with CNS composition differences and minor sequence variation, although causal relationships remain to be demonstrated. Our analyses further revealed a complex spectrum of CNS dynamics within the diploid-polyploid framework. Overall, our study provides empirical insights into the fine-scale evolution of plant regulatory landscapes and complements previous large-scale comparisons across distant lineages. 

Abstract Gene duplication is a major source of evolutionary innovation, enabling the emergence of novel expression patterns and functions. Leveraging single-cell genomics, we investigated the transcriptional and cis-regulatory landscapes of duplicated genes in cultivated soybean (Glycine max), which has undergone 2 rounds of whole-genome duplication. Our analysis revealed extensive diversity of transcriptional profiles within and across tissues among duplicated gene pairs. Within-tissue divergence was largely attributable to genetic variation in their associated accessible chromatin regions (ACRs), where cis-regulatory elements reside, whereas cross-tissue divergence was more likely shaped by dynamics in ACR chromatin accessibility profiles across tissues. Distinct duplication mechanisms also likely give rise to different types of cis-regulatory variants, contributing variably to transcriptional divergence. By comparing ACRs associated with gene sets derived from 2 rounds of whole-genome duplication and sharing a common ancestral gene, we found that most ACRs retained one or multiple corresponding duplicated sequences in which mutations gradually accumulated over time, while a subset likely arose de novo. Finally, we traced the evolution of cell-type-specific expression and cell-type-specific ACRs within duplicated gene sets, illustrating a powerful framework for identifying candidate regulatory regions driving cell-type-specific expression. Collectively, our findings highlight the important role of cis-regulatory evolution in shaping transcriptional divergence in a spatiotemporal manner, uncovered with the resolution of single-cell genomics.