Circadian oscillations in chromatin accessibility systematically orchestrate rhythmic gene transcription in soybean

In soybean (Glycine max (L) Merr.), the circadian clock orchestrates rhythmic molecular, metabolic, and physiological processes that determine yield potential and restrict cultivars to a narrow latitudinal range. However, the role of dynamic chromatin states in rhythmic transcription remains elusive. Here, we integrated time-series assay for transposase-accessible chromatin using sequencing, chromatin immunoprecipitation sequencing, and RNA-seq to map the genome-wide circadian chromatin accessibility landscape under free-running conditions in soybean. We identified 11 core co-oscillation groups (CCOGs), whose chromatin accessibility was synchronized with mRNA oscillations. Accessible chromatin regions (ACRs) within these CCOGs are enriched for binding motifs of the core circadian oscillators, which regulate the expression of their target genes. Two functionally distinct ACRs, which respectively regulate the circadian rhythmicity and stable expression of LATE ELONGATED HYPOCOTYL 1a (GmLHY1a), were characterized. Natural variants of these ACRs were correlated with the latitudinal adaptation of soybeans. In addition, mutations in core oscillator components, including GmLHYs and LUX ARRHYTHMO (GmLUXs), disrupt chromatin oscillation in CCOGs. For instance, altered chromatin accessibility was detected at key binding sites, such as the region where GmLHY1a interacts with the ACR associated with GmPIF4 (PHYTOCHROME INTERACTING FACTOR 4). Collectively, these findings reveal a mechanism wherein chromatin accessibility rhythms orchestrate genome-scale transcriptional programs and provide a large-scale, time-resolved, multi-omics resource to facilitate crop breeding for improved environmental adaptation.