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Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization

Nature Plants volume 5, pages 822–832 (2019)Cite this article

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Abstract

The non-random three-dimensional (3D) organization of the genome in the nucleus is critical to gene regulation and genome function. Using high-throughput chromatin conformation capture, we generated chromatin interaction maps for Brassica rapa and Brassica oleracea at a high resolution and characterized the conservation and divergence of chromatin organization in these two species. Large-scale chromatin structures, including A/B compartments and topologically associating domains, are notably conserved between B. rapa and B. oleracea, yet their KNOT structures are highly divergent. We found that genes retained in less fractionated subgenomes exhibited stronger interaction strengths, and diploidization-resistant duplicates retained in pairs or triplets are more likely to be colocalized in both B. rapa and B. oleracea. These observations suggest that spatial constraint in duplicated genes is correlated to their biased retention in the diploidization process. In addition, we found strong similarities in the epigenetic modification and Gene Ontology terms of colocalized paralogues, which were largely conserved across B. rapa and B. oleracea, indicating functional constraints on their 3D positioning in the nucleus. This study presents an investigation of the spatial organization of genomes in Brassica and provides insights on the role of 3D organization in the genome evolution of this genus.

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Fig. 1: Global patterns of chromatin in Hi-C contact maps.
Fig. 2: Chromosomal landscape of genomic features and chromatin modifications.
Fig. 3: TAD profiles in B. rapa and B. oleracea.
Fig. 4: Evolutionary conservation of compartment status and TAD boundaries across B. rapa and B. oleracea.
Fig. 5: Comparison of interaction levels across the three subgenomes.
Fig. 6: Colocalization frequency of interchromosomal paralogues retained after WGT and comparison of histone modification and DNA methylation levels and GO patterns between colocalized and non-colocalized paralogues.

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Data availability

All sequencing data generated for this study have been submitted to the NCBI Sequence Read Archive under accession number PRJNA521833.

Code availability

The script used to generate the distance-normalized O/E matrix is available in the Supplementary Information.

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Acknowledgements

We acknowledge the technical assistance of Igenebook (Wuhan) for ChIP-seq library construction. This work was funded by the National Natural Science Foundation of China (grant no. 31801052), the National Key Program for Research and Development (grant no. 2016YFD0100202), the National Natural Science Foundation of China (grant no. 31670779), the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (grant no. CAAS-ASTIP-2015-OCRI) and the Fundamental Research Funds for Central Non-profit Scientific Institution (grant no. 1610172018011).

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Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan, China

    Ting Xie, Fu-Gui Zhang, Ji-Hong Hu & Xiao-Ming Wu

  2. Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, China

    Hong-Yu Zhang

  3. Department of Biochemistry and Molecular Biology, College of Medicine, Pennsylvania State University, Hershey, PA, USA

    Xiao-Tao Wang

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  1. Ting Xie
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Contributions

T.X. and H.-Y.Z. conceived and designed the research. F.-G.Z., X.-M.W. and J.-H.H. prepared the DNA samples and performed the experiments. T.X., X.-T.W. and J.-H.H analysed the data. T.X. wrote the manuscript with input from H.-Y.Z., F.-G.Z. and X.-T.W.

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Correspondence to Ting Xie.

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Peer review information: Nature Plants thanks Chang Liu, Martin Mascher and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–8 and Supplementary Tables 1–3, and Supplementary Tables 7 and 8.

Reporting Summary

cal_obs_exp.py

A custom script for the distance-normalized matrix calculation in this study.

Supplementary Table 4

A/B compartments identified in B. rapa and B. oleracea.

Supplementary Table 5

TADs identified in B. rapa and B. oleracea.

Supplementary Table 6

Interaction scores and expression levels of the paralogues retained from WGT.

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Xie, T., Zhang, FG., Zhang, HY. et al. Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization. Nat. Plants 5, 822–832 (2019). https://doi.org/10.1038/s41477-019-0479-8

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