Evolutionary dynamics of 3D genome architecture following polyploidization in cotton

Abstract

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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Fig. 1: Global patterns of chromatin interactions in different cotton accessions.
Fig. 2: Active transcription in higher-order structures.
Fig. 3: Comparison of chromatin interactions between diploids and subgenomes of tetraploids.
Fig. 4: Reorganization of higher chromatin structures in cotton.
Fig. 5: Signals of open chromatin and chromatin modification marks at TAD boundaries.

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Acknowledgements

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).

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Authors

Contributions

X.Z., M.W. and Q.Y. conceived and designed the project. M.L., P.W. and Z.Y. performed the experiments and managed sequencing. M.W., C.S. and J.L. analysed the data. G.L. and L.T. contributed to manuscript discussion. M.W. wrote the manuscript draft. X.Z., Q.Y. and G.L. revised the manuscript.

Corresponding authors

Correspondence to Min Lin or Qingyong Yang or Xianlong Zhang.

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The authors declare no competing financial interests.

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Supplementary information

Supplementary Information

Supplementary Figures 1–7 and Supplementary Tables 1–4

Life Sciences Reporting Summary

Supplementary Table 5

Identification of intergenic DHSs and enhancers in cotton

Supplementary Table 6

Summary of enhancer-associated lincRNAs in cotton

Supplementary Table 7

Summary of TADs in cotton

Supplementary Table 8

Summary of compartment switching in cotton

Supplementary Table 9

Summary of DEGs associated with changes of chromatin structures

Supplementary Table 10

Inter-chromosomal interactions in G. hirsutum

Supplementary Table 11

Inter-chromosomal interactions in G. barbadense

Supplementary Table 12

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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