Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation

Authors: PEI, LIULING - Huazhong Agricultural University; HUANG, XIANHUI - Huazhong Agricultural University; LIU, ZHENPING - Huazhong Agricultural University; TIAN, XUEHAN - Huazhong Agricultural University; YOU, JIAQI - Huazhong Agricultural University; LI, JIANYING - Huazhong Agricultural University; Fang, David; LINDSEY, KEITH - University Of Durham; ZHU, LONGFU - Huazhong Agricultural University; ZHANG, XIANLONG - Huazhong Agricultural University; WANG, MAOJUN - Huazhong Agricultural University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/20/2022
Publication Date: 2/3/2022
Publication URL: https://handle.nal.usda.gov/10113/7665675
Citation: Pei, L., Huang, X., Liu, Z., Tian, X., You, J., Li, J., Fang, D.D., Lindsey, K., Zhu, L., Zhang, X., Wang, M. 2022. Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation. Genome Biology. 23:45. https://doi.org/10.1186/s13059-022-02616-y.
DOI: https://doi.org/10.1186/s13059-022-02616-y

Interpretive Summary: Plant growth and development is not only affected by genes but also by gene-gene interactions and chromatin compositions.Chromatin is the materials of which the chromosomes of organisms are composed. It consists of protein, RNA, and DNA. To understand the importance of chromatin in cotton fiber cell differentiation, we established the three-dimensional (3D) genome architecture of cotton fiber. We show that the subgenome-relayed switching of chromatin compartment from active to inactive was coupled with the silencing of developmentally repressed genes. We identified 10,571 topologically associating domains (TADs), of which 25.6% were specifically organized in different fiber development stages and 75.23% were subject to partition or fusion between two subgenomes. Notably, dissolution of TADs cliques showing long-range TAD-TAD interactions represented a prominent characteristic at the later developmental stage. This study sheds light on the spatial-temporally asymmetric chromatin structures of two subgenomes in cotton fiber and offers a new insight into the regulatory orchestration for cell differentiation in plants.

Technical Abstract: Despite remarkable advances in our knowledge of epigenetically mediated transcription programming of cell differentiation in plants, little is known about chromatin topology and its functional implications in this process. To interrogate the significance, we established the dynamic three-dimensional (3D) genome architecture of allotetraploid cotton fiber, representing a typical single cell undergoing staged development in plants. We show that the subgenome-relayed switching of chromatin compartment from active to inactive was coupled with the silencing of developmentally repressed genes, pinpointing subgenome-coordinated contribution to fiber development. We identified 10,571 topologically associating domains (TADs), of which 25.6% were specifically organized in different stages and 75.23% were subject to partition or fusion between two subgenomes. Notably, dissolution of intricate TAD cliques showing long-range TAD-TAD interactions represented a prominent characteristic at the later developmental stage. Dynamic chromatin loops were found to mediate the rewiring of gene regulatory networks that exhibited a significant difference between two subgenomes implicating expression bias of homoeologous genes. This study sheds light on the spatial-temporally asymmetric chromatin structures of two subgenomes in cotton fiber and offers a new insight into the regulatory orchestration for cell differentiation in plants.