Dynamic homoeolog expression partitioning contributes to soil-driven adaptive plasticity in allopolyploid Leymus...

Allopolyploidy plays a pivotal role in plant adaptation. Leymus chinensis, a perennial allotetraploid grass, thrives across diverse and often harsh soil environments in northern China, yet the genetic basis underpinning its remarkable ecological flexibility remains largely unexplored. Here, we leveraged the recently published chromosome-level reference genome of L. chinensis together with comparative transcriptomic profiling on clonal replicates cultivated in four distinct soil types: forest, farmland, sandy, and saline-alkaline. We identified 13 289 high-confidence homoeologous gene pairs, which showed extensive gene-level homoeologous expression partitioning, both between tissues (leaf vs. root) and among the soil conditions. Functional enrichment analyses supported a soil-adaptive model of homoeolog expression partitioning along an edaphic gradient from nutrient-rich to stressful soils. The Ns-Xm homoeolog pairs showing expression partitioning exhibited significantly elevated Ka and Ka/Ks ratios, particularly among soil-responsive genes, consistent with relaxed purifying selection and greater protein-coding divergence accumulated over evolutionary time. A subset of these genes exhibited pronounced expression bias reversal, with the dominant homoeolog switching across tissues or soil conditions. The dynamic homoeologous expression partitioning also contributes to total expression variation, thereby facilitating rapid transcriptional responses and context-dependent functional adjustments. In addition, our cis-motif feature analysis of homoeolog promoters revealed that combined variation in motif presence, copy number, and positional proximity to the translation start site may influence transcription factor recruitment and downstream tissue- and environment-specific subgenomic partitioning. Together, this study provides new insights to our understanding of how allopolyploidy achieves developmental and environmental adaptation through homoeolog and total level expression plasticity.