The near-complete genome assembly of allotetraploid Pennisetum purpureum ‘Purple’ reveals the genetic and epigenetic landscape of centromeres

Abstract

Drastic karyotype changes are a major evolutionary force, potentially involving centromere position, number, distribution, or strength alterations. Yet, the genetic and epigenetic landscape of centromeres, especially in allopolyploid plants during subgenome reshuffling, remains poorly understood. Here, we present a near-complete chromosome-scale genome assembly of the allotetraploid Pennisetum purpureum ‘Purple’, resolving all 14 centromeres. We find that subgenome-biased expansion of six LTR retrotransposons drives architectural divergence between subgenomes. Centromeric satellite repeats (CentPs) show rapid sequence divergence across subgenomes and chromosomes, with CENH3 preferentially binding conserved higher order repeats. Intriguingly, centromeric retrotransposons in Pennisetum (CRPs) are evolutionarily younger compared to their noncentromeric counterparts, coupled with marked subgenome B-biased amplification. Notably, CRP insertions flanking CentP satellites correlate with elevated satellite DNA polymorphism, supporting a model wherein CentP homogenization processes actively purge retrotransposons from centromeric arrays. Despite rapid sequence diversification of centromeric repeats, the epigenetic landscapes remain evolutionarily conserved in the centromeres of two subgenomes. Additionally, comparative analyses across Pennisetum species demonstrate rapid species- and chromosome-level turnover of CentPs and CRPs. Overall, our study illuminates the genetic and epigenetic plasticity of centromeres in allopolyploids, revealing how centromeric repeats adapt post-subgenome reshuffling.

Acknowledgements

We thank Juying Wu (Institute of Grassland, Flower and Ecology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China) and Linkai Huang (College of Grassland Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China) for providing plant materials for this study. This work was supported by funds from the National Natural Science Foundation of China (32001605), the Natural Science Foundation of Fujian Province, China (2025 J01332), and the Open Project of State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources (SKLCUSA-b202408). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Authors contributions

Y.J.H. and Z.L.Z. conceived the project. X.Y.L. performed experiments. Y.J.H., J.B.L., J.X., and Z.L.Z. analyzed data. Y.J.H., J.B.L., Z.L.Z, S.Z., J.X., Z.H.D., and X.X.Z. interpreted data analyses. Y.J.H. wrote the manuscript with contributions from all authors. All authors read and approved the final manuscript.

Data availability

The whole-genome sequencing data (including Illumina short reads, HiFi reads, and Hi-C interaction reads), ChIP-seq data, and transcriptomes of different tissues used in this study have been deposited at the National Genomics Data Center (NGDC) under accession number PRJCA034549. The raw reads used in this study are available under the following accession numbers (ChIP-seq data: CRA021877; RNA-seq data: CRA021875; Illumina WGS data: CRA021874; HiFi data: CRA021873; Hi-C data: CRA021871). The genome assembly and gene annotation data for P. purpureum ‘Purple’ have been deposited at the Genome Warehouse (GWH) under accession number GWHFIJS00000000.1.

Conflicts of interest statement

The authors declare that they have no conflict of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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