Evolutionary patterns and functional effects of 3D chromatin structures in butterflies with extensive genome rearrangements

Botong Zhou, Ping Hu, Guichun Liu, Zhou Chang, Zhiwei Dong, Zihe Li, Yuan Yin, Zunzhe Tian, Ge Han, Wen Wang () and Xueyan Li ()
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Botong Zhou: Northwestern Polytechnical University
Ping Hu: Chinese Academy of Sciences
Guichun Liu: Chinese Academy of Sciences
Zhou Chang: Chinese Academy of Sciences
Zhiwei Dong: Chinese Academy of Sciences
Zihe Li: Northwestern Polytechnical University
Yuan Yin: University of Electronic Science and Technology of China
Zunzhe Tian: Northwestern Polytechnical University
Ge Han: Northwestern Polytechnical University
Wen Wang: Northwestern Polytechnical University
Xueyan Li: Chinese Academy of Sciences

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Chromosome rearrangements may distort 3D chromatin architectures and thus change gene regulation, yet how 3D chromatin structures evolve in insects is largely unknown. Here, we obtain chromosome-level genomes for four butterfly species, Graphium cloanthus, Graphium sarpedon, Graphium eurypylus with 2n = 30, 40, and 60, respectively, and Papilio bianor with 2n = 60. Together with large-scale Hi-C data, we find that inter-chromosome rearrangements very rarely disrupted the pre-existing 3D chromatin structure of ancestral chromosomes. However, some intra-chromosome rearrangements changed 3D chromatin structures compared to the ancestral configuration. We find that new TADs and subTADs have emerged across the rearrangement sites where their adjacent compartments exhibit uniform types. Two intra-chromosome rearrangements altered Rel and lft regulation, potentially contributing to wing patterning differentiation and host plant choice. Notably, butterflies exhibited chromatin loops between Hox gene cluster ANT-C and BX-C, unlike Drosophila. Our CRISPR-Cas9 experiments in butterflies confirm that knocking out the CTCF binding site of the loops in BX-C affected the phenotypes regulated by Antp in ANT-C, resulting in legless larva. Our results reveal evolutionary patterns of insect 3D chromatin structures and provide evidence that 3D chromatin structure changes can play important roles in the evolution of traits.

Date: 2024
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DOI: 10.1038/s41467-024-50529-0

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