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

Abstract

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

Global transcriptome analysis of allopolyploidization reveals large-scale repression of the D-subgenome in synthetic hexaploid wheat

“…The results from this study, showing preponderance of triad-specific bias trends across developmental stages, suggest the spatial and temporal variability of HEB, leading to different bias trends through developmental stages, in addition to stress responsive patterns. In allopolyploid cotton, a study analysing the fiber development, revealed the changes in chromatin architecture in the different developmental stages and their influence on gene regulatory networks (GRNs) leading to HEB 55 . This highlights the potential role of dynamic variation in 3D chromatin architecture in bringing about spatiotemporal differences in HEB.…”

Chromatin remodeling analysis reveals the RdDM pathway responds to low‐phosphorus stress in maize

“…Specifically, in rice leaf mesophyll tissues, the count of trans interactions was higher than that of cis interactions. In a study focusing on cotton fibers, it was also observed that the number of trans interactions exceeded the number of cis interactions specifically at 20 days post‐anthesis (Pei et al., 2022). These findings indicate significant variations in the ratio of cis / trans interactions across different samples.…”

“…Upon perceiving environmental changes and developmental signals, both global and local chromatin rearrangements may occur, accompanied by changes in the gene transcription levels (Probst & Mittelsten, 2015; Rosa et al., 2013). With the advent of new techniques, an increasing number of studies have been conducted on chromatin conformation (Pei et al., 2022; Yuan et al., 2022; Zhang, Pandey, et al., 2021). Microimaging techniques based on fluorescence in situ hybridization, such as fluorescence labeling imaging and ChromEMT tomography (Cremer & Cremer, 2001; Ou et al., 2017), and high‐throughput sequencing techniques based on chromatin conformation capture and chromatin‐interaction capture, such as high‐throughput chromosome conformation capture (Hi‐C) and ChIA‐PET (Fullwood et al., 2009; Lieberman‐Aiden et al., 2009), are the two main methods used to study the three‐dimensional (3D) structure of genomes.…”

Synergistic interplay of redox homeostasis and polysaccharide synthesis promotes cotton fiber elongation

“…The trees were beautified and annotated using the iTOL online tool (https://itol.embl.de/). Collection of published RNA‐seq data from multiple tissues of G. hirsutum TM‐1 (Texas Marker‐1) and calculation of gene expression levels used the same pipeline as previously reported (Pei et al., 2022), followed by visualization of a clustered heatmap using R package pheatmap (version 1.0.12).…”