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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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).

Author information

Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

    • Maojun Wang
    • , Pengcheng Wang
    • , Min Lin
    • , Zhengxiu Ye
    • , Guoliang Li
    • , Lili Tu
    • , Chao Shen
    • , Jianying Li
    • , Qingyong Yang
    •  & Xianlong Zhang
  2. Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, China

    • Min Lin
    • , Guoliang Li
    •  & Qingyong Yang

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Min Lin or Qingyong Yang or Xianlong Zhang.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–7 and Supplementary Tables 1–4

  2. Life Sciences Reporting Summary

  3. Supplementary Table 5

    Identification of intergenic DHSs and enhancers in cotton

  4. Supplementary Table 6

    Summary of enhancer-associated lincRNAs in cotton

  5. Supplementary Table 7

    Summary of TADs in cotton

  6. Supplementary Table 8

    Summary of compartment switching in cotton

  7. Supplementary Table 9

    Summary of DEGs associated with changes of chromatin structures

  8. Supplementary Table 10

    Inter-chromosomal interactions in G. hirsutum

  9. Supplementary Table 11

    Inter-chromosomal interactions in G. barbadense

  10. Supplementary Table 12

    Homologous gene pairs with chromatin interactions in cotton

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DOI

https://doi.org/10.1038/s41477-017-0096-3

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