Comparison of dynamic 3D chromatin architecture uncovers heterosis for leaf size in Brassica napus

INTRODUCTION: Heterosis is the major event driving plant development and promoting crop breeding, but the molecular bases for this phenomenon remain elusive. OBJECTIVES: We aim to explore the effect of three-dimensional (3D) chromatin architecture on the underlying mechanism of heterosis. METHODS: Here, we constructed the North Carolina II (NC-II) population to select superior and inferior heterosis sets by comparing mid-parent heterosis (MPH) in Brassica napus. To decipher the impact of 3D chromatin architecture on the underlying mechanism of heterosis, we combined genetics, transcriptomics and 3D genomics approaches. RESULTS: We suggest that F1 hybrids with superior heterosis tend to contain more transcriptionally active A compartments compared with F1 hybrids with inferior heterosis, and approximately 19–21% compartment significantly altered in the F1 hybrids relative to the parental lines. Further analyses show that chromatin compartments correlate with genetic variance among parents, which may form the basis for differentially active chromatin compartments. Having more A compartments in F1 hybrids confers a more accessible chromatin circumstance, which promotes a higher proportion of highly expressed ELD (expression level dominance) genes in superior heterosis F1 hybrids (46–64%) compared with inferior heterosis F1 hybrids (22–31%). Moreover, genes related to hormones which affect plant growth, are more up-regulated with changes of 3D genome architecture, and we validate that increased hormone content contributes to cell proliferation and expansion by influencing the key genes of cell cycle thereby promoting leaf size. CONCLUSION: Dynamic 3D chromatin architecture correlates with genetic variance among parents and contributes to heterosis in Brassica napus.