LHP1-mediated conditional repression of subgenome-diversified defenses is responsible for the high plasticity of allopolyploid wheat

High plasticity of common wheat is attributed to the captured and polyploidization-promoted diversity. However, uncontrolled subgenome diversification can lead to hybrid conflict and dysgenesis, resulting in decreased diversity. How genomic diversity is maintained and interpreted to increase plasticity is unclear. By data-mining from the binding of 193 genome-wide trans-factors and genetic perturbations in common wheat, we identified LHP1 as a major regulator of subgenome-diversified defense genes, enhancer RNAs, and metabolite synthesis-related gene clusters via H3K27me3. Stripe rust infection leads to a global decrease in LHP1-mediated H3K27me3, deprivation of which enhances common wheat stripe rust resistance. We also revealed the consistency between subgenome diversity and population diversity, potentially promoted by LHP1, implying the recent diversification preferentially occurred in the captured subgenome-diversified regions regulated by LHP1. Thus, common wheat benefitted from multi-faced role of LHP1 in promoting sequence diversity and repressing subgenome-diversified defenses; this constraint is eliminated by pathogen infections, enabling timely release and fixation of favorable variations, conferring the evolutionary advantage and high plasticity of common wheat. Overall design: To elucidate how genomic diversity is maintained and interpreted to increase plasticity in common wheat, we obtained gene expression profiles, H3K27me3, LHP1 and eRNA in wild type (JW1) and lhp1-abd mutant.