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Pan-centromere landscape and dynamic evolution in Brassica plants

Nature Plants volume 11, pages 2240–2253 (2025)Cite this article

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Abstract

The centromere paradox, in which functionally conserved centromeres exhibit rapid evolution, has long intrigued geneticists and evolutionary biologists. Despite its importance, the centromeric landscape remains poorly understood due to the lack of complete assemblies. Here we dissect the dynamic evolution of Brassica centromeres by generating telomere-to-telomere genome assemblies from seven morphotypes of B. rapa (AA) and the two tetraploids B. juncea (AABB) and B. napus (AACC). Pan-centromere analysis reveals that Brassica centromeres are extensively invaded by retrotransposons and show remarkable diversity in size and structure. While A- and C-genome centromeres feature distinct patterns of satellites, B-genome centromeres are devoid of satellites. The centromeric satellite expansion in the C-genome is reminiscent of the layered expansions observed in human centromeres. Accordingly, we propose a working model of centromere evolution reconstructing the key evolutionary events leading to current Brassica centromere structures. These insights will illuminate plant centromere evolution and guide the design of crop synthetic chromosomes.

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Fig. 1: Complete centromere landscape of the Chinese cabbage ‘Futian’ genome.
Fig. 2: The centromere diversity of the CEN176 array in B. rapa.
Fig. 3: The structure and diversity of the CEN238 array in Brassica.
Fig. 4: Centromere diversity in Brassica.
Fig. 5: Genomic and epigenetic organization within the centromeres.
Fig. 6: The proposed model of Brassica centromere evolution.

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Data availability

The raw sequencing data and the genome assembly have been deposited at the National Center for Biotechnology Information under project number PRJNA1116321.

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Acknowledgements

This work was supported by the Shandong Provincial Natural Science Foundation (grant no. SYS202206 to L.G.), the Taishan Scholars Program (L.G.) and the Natural Science Foundation for Distinguished Young Scholars of Shandong Province (grant no. ZR2023JQ010 to L.G.).

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Authors and Affiliations

  1. Shandong Key Laboratory of Precision Molecular Crop Design and Breeding, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences in Weifang, Shandong, China

    Weikai Chen, Jingxuan Wang, Shaoying Chen, Dian Meng, Yu Mu, Lugang Zhang & Li Guo

  2. Liaoning Key Laboratory of Genetics and Breeding for Cruciferous Vegetable Crops, College of Horticulture, Shenyang Agricultural University, Shenyang, China

    Hui Feng

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Contributions

L.G. conceived and supervised the project. W.C. performed the genome assemblies and pan-centromere analysis. J.W. performed the phylogenetic analysis. S.C. performed the DNA methylation analysis. D.M. conducted the CENH3 ChIP–seq experiment. H.F. provided the Chinese cabbage doubled haploid line ‘Futian’. Y.M. maintained the plant materials. L.Z. participated in the discussion of the results. W.C. and L.G. wrote the paper. All authors read and approved the final version of the paper.

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Correspondence to Li Guo.

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Extended data

Extended Data Fig. 1 Genome assembly statistics and validation.

a, Assembly statistics of the ten Brassica genome used in this study. The dashed lines represent the contig N50 index. b, c, Whole-genome coverage of HiFi reads across A1 Futian (b) and A5 turnip (c) genome assembly. The regions of telomere, centromeric CEN176 and CEN238 arrays, 45S rDNA and 5S rDNA arrays and organelle insertions were marked on the bottom track.

Extended Data Fig. 2 Genome assembly and centromere structure of the allotetraploid B. juncea (AABB).

a, Circos plot of the AB genome assembly. Quantitative tracks were calculated in 100-kb bins. Full descriptions for the tracks are also available in the main Fig. 1 legend. b, The structure of B03 centromere and statistics of CENH3 log2(ChIP/input), CpG and CHG methylation, Copia density, and Gypsy density. c, StainedGlass heatmap of the pairwise sequence identity (%) between 5-kb bins. A CEN176 satellite relict was identified at the boundary of B08 centromere.

Extended Data Fig. 3 Genome assembly and centromere structure of the allotetraploid B. napus (AACC).

a, Circos plot of the AC genome assembly. Quantitative tracks were calculated in 100-kb bins. Track from outer to inner: chromosomes (red: centromere), GC content, gene density, Gypsy density, Copia density, CEN176 density, rDNA density, CpG methylation level estimated by ONT reads and colour ribbons representing syntenic blocks. b, The structure of C02 centromere and statistics of satellite density (red, forward; blue, reverse orientation), satellite edit distance relative to CentBr1 and CentBr2, Copia density, and Gypsy density. c, StainedGlass heatmaps of the pairwise sequence identity (%) between 5-kb bins. Three representative centromeres of C subgenome were exhibited.

Extended Data Fig. 4 Dynamics of CEN176 satellites in Brassica crops.

a, A maximum-likelihood phylogenetic tree of 6,487 representative (>50 occurrences in the pan-centromere collection) CEN176 satellites. b, Pairwise edit distance of top one (the highest occurrences) CEN176 monomer in each family. c, Consensus sequences of the CEN176 satellites in each family. The asterisk indicates the distinct bases between two major groups (I and II). d, Copy number of the CEN176 satellites across each chromosome and each accession. Seventeen families are coloured according to the taxonomic groups.

Extended Data Fig. 5 Presence of rDNA-derived CEN238/CEN208 repeat array in B. rapa/S. alba.

a, A circos plot of tandem repeats identified in the S. alba draft genome assembly. Shading is coloured according to repeat length (bp). Histogram corresponds to repeat families with different lengths. b, Alignment of two 45S rDNA units in B. rapa and S. alba, respectively. The BrCEN238 and SalCEN208 were probably originated from subrepeat array of corresponding 45S rDNA. c, Genome collinearity between B. rapa and S. alba. The blue labels mark the chromosomes with rDNA-derived repeat array. d, Dot plots comparing the representative centromeres from B. rapa and S. alba assemblies. The black and blue boxes represent the BrCEN176/SalCEN178 and BrCEN238/SalCEN208 repeat arrays, respectively.

Extended Data Fig. 6 Sequence alignment of CENH3 proteins and centromeric satellites.

a, b, Sequence alignment of centromeric satellites (a) and CENH3 proteins (b) from A. thaliana, R. sativus, S. alba, S. arvensis, B. rapa B. oleracea, and B. nigra. The B. nigra and S. arvensis CENH3 proteins has a deletion (red box) corresponding to the fourth and fifth exons of BrCENH3.

Extended Data Fig. 7 Edit distance of centromeric satellites relative to CentBr1 and CentBr2.

The edit distances of centromeric satellites in C subgenome were calculated. The previous X5A assembly showed similar results except for the C04 centromere. The box in the lower right corner shows the proposed centromere evolution model in C sub/genome.

Extended Data Fig. 8 Phylogenetic analysis of intact Ale retrotransposons in Brassica crops.

a-c, Ale phylogeny across Brassica crops and R. sativus. Tree labels are coloured according to sample accession (a), position inside or outside the centromeres (b) and the LTR insertion time (c). Scale bar, 0.5 substitutions per site. d, The insertion time of Ale retrotransposons among different sample accessions. The edges and centerlines of the boxes represent the interquartile range and medians. A two-sided Wilcoxon test was used to determine the significant levels. The insertion time of centrophilic Ale in A genome was significantly younger than these in the B (P = 6.6 × 10−7) and C genomes (P = 9.21 × 10−37).

Extended Data Fig. 9 Genome rearrangements and centromere evolution of B. rapa and B. oleracea.

a, Karyotype evolution from previous reported ancestral genome to current B. rapa and B. oleracea genomes. Syntenic blocks are ‘painted’ with colours corresponding to ancestral chromosomes. Black bars represent ancestral centromeric regions. b, Chromosome alignments illustrate the emergence of centromeric CEN176 and CEN238 arrays in A and C sub/genome.

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Chen, W., Wang, J., Chen, S. et al. Pan-centromere landscape and dynamic evolution in Brassica plants. Nat. Plants 11, 2240–2253 (2025). https://doi.org/10.1038/s41477-025-02131-5

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