J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (2): 208-227.DOI: 10.1111/jipb.13620

• Functional Omics and Systems Biology • Previous Articles     Next Articles

Increased long-distance and homo-trans interactions related to H3K27me3 in Arabidopsis hybrids

Zhaoxu Gao1†, Yanning Su1†, Le Chang1, Guanzhong Jiao1, Yang Ou1, Mei Yang1, Chao Xu1, Pengtao Liu1, Zejia Wang1, Zewen Qi2, Wenwen Liu1, Linhua Sun1, Guangming He1, Xing Wang Deng1,3* and Hang He1,3*   

  1. 1. School of Advanced Agriculture Sciences and School of Life Sciences, State Key Laboratory of Protein and Plant Gene Research, Peking University, Beijing 100871, China;
    2. College of Grassland Science, Beijing Forestry University, Beijing 100083, China;
    3. Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences in Weifang, Weifang 261325, China
    These authors contributed equally to this work.
    *Correspondences: Xing Wang Deng (deng@pku.edu.cn); Hang He (hehang@pku.edu.cn, Dr. He is fully responsible for the distribution of all materials associated with this article in the manuscript)
  • Received:2023-06-16 Accepted:2024-01-16 Online:2024-02-07 Published:2024-02-01

Abstract: In plants, the genome structure of hybrids changes compared with their parents, but the effects of these changes in hybrids remain elusive. Comparing reciprocal crosses between Col×C24 and C24×Col in Arabidopsis using high-throughput chromosome conformation capture assay (Hi-C) analysis, we found that hybrid three-dimensional (3D) chromatin organization had more long-distance interactions relative to parents, and this was mainly located in promoter regions and enriched in genes with heterosis-related pathways. The interactions between euchromatin and heterochromatin were increased, and the compartment strength decreased in hybrids. In compartment domain (CD) boundaries, the distal interactions were more in hybrids than their parents. In the hybrids of CURLY LEAF (clf) mutants clfCol×clfC24 and clfC24×clfCol, the heterosis phenotype was damaged, and the long-distance interactions in hybrids were fewer than in their parents with lower H3K27me3. ChIP-seq data revealed higher levels of H3K27me3 in the region adjacent to the CD boundary and the same interactional homo-trans sites in the wild-type (WT) hybrids, which may have led to more long-distance interactions. In addition, the differentially expressed genes (DEGs) located in the boundaries of CDs and loop regions changed obviously in WT, and the functional enrichment for DEGs was different between WT and clf in the long-distance interactions and loop regions. Our findings may therefore propose a new epigenetic explanation of heterosis in the Arabidopsis hybrids and provide new insights into crop breeding and yield increase.

Key words: 3D chromatin organization, H3K27me3, homo-trans, hybrids, long-distance interactions

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