The formation of polyploids significantly increases the complexity of transcriptional regulation, which is expected to be reflected in sophisticated higher-order chromatin structures. However, knowledge of three-dimensional (3D) genome structure and its dynamics during polyploidization remains poor. Here, we characterize 3D genome architectures for diploid and tetraploid cotton, and find the existence of A/B compartments and topologically associated domains (TADs). By comparing each subgenome in tetraploids with its extant diploid progenitor, we find that genome allopolyploidization has contributed to the switching of A/B compartments and the reorganization of TADs in both subgenomes. We also show that the formation of TAD boundaries during polyploidization preferentially occurs in open chromatin, coinciding with the deposition of active chromatin modification. Furthermore, analysis of inter-subgenomic chromatin interactions has revealed the spatial proximity of homoeologous genes, possibly associated with their coordinated expression. This study advances our understanding of chromatin organization in plants and sheds new light on the relationship between 3D genome evolution and transcriptional regulation.
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We thank K. Lindsey (Durham University) for revising this manuscript. This work was funded by the National Natural Science Foundation of China (31230056, 31301005), China Postdoctoral Science Foundation (2015M572169) and State Key Laboratory of Cotton Biology Open Fund (CB2016A08).
The authors declare no competing financial interests.
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Supplementary Figures 1–7 and Supplementary Tables 1–4
Identification of intergenic DHSs and enhancers in cotton
Summary of enhancer-associated lincRNAs in cotton
Summary of TADs in cotton
Summary of compartment switching in cotton
Summary of DEGs associated with changes of chromatin structures
Inter-chromosomal interactions in G. hirsutum
Inter-chromosomal interactions in G. barbadense
Homologous gene pairs with chromatin interactions in cotton
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Wang, M., Wang, P., Lin, M. et al. Evolutionary dynamics of 3D genome architecture following polyploidization in cotton. Nature Plants 4, 90–97 (2018). https://doi.org/10.1038/s41477-017-0096-3
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