Pervasive and context-dependent homeologous expression remodeling in intersubspecific diploid F1 hybrids and segmental allotetraploids of rice.

Allopolyploidy combines hybridization and whole-genome doubling (WGD), yet their impacts on homeologous expression asymmetry across tissues and environments remain to be fully understood. Using Oryza sativa ssp. japonica Nipponbare and ssp. indica 9311, we generated reciprocal F1 hybrids and their genome-doubled segmental allotetraploids, and profiled leaf and root transcriptomes under normal, cold, and low-nitrogen conditions. For each tissue and condition, an in silico 1:1 mixture of parental transcriptome reads was used as a reference for parental expression state. Reciprocal F1 hybrids consistently reduced parental homeologous expression differences and maintained narrow, near-equal homeolog expression across tissues and conditions, consistent with trans-regulatory buffering. Segmental allotetraploids augmented parental homeologous expression bias with strong tissue and condition dependence, as well as maternally biased parent-of-origin effects. In F1 hybrids, most expression-biased homeolog pairs inherited the parental bias direction, whereas segmental allotetraploids underwent extensive de novo reprogramming. Condition-dependent homeolog expression-biased gene sets showed more detectable functional enrichments in segmental allotetraploids than in F1 hybrids, highlighting stress- and signaling-related functions under cold in leaves and transport- and energy-related processes under low nitrogen in roots. Representative cloned cold- and nitrate-related genes showed locus-, tissue-, and genotype-dependent homeologous expression and total-expression patterns, with only partial concordance with stress-related phenotypes. Together, our results provide insights into how hybridization and WGD exert contrasting effects on homeolog regulation and suggest that regulatory flexibility may contribute to subsequent allopolyploid evolution.