Chromatin spatial organization of wild type and mutant peanuts reveals high-resolution genomic architectures and interaction alterations

Authors: ZHANG, X - Henan Agricultural University; PANDEY, MANISH - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; WANG, J - University Of Florida; ZHAO, K - Henan Agricultural University; MA, X - Henan Agricultural University; LI, Z - Henan Agricultural University; ZHAO, K - Henan Agricultural University; GONG, F - Henan Agricultural University; Guo, Baozhu; VARSHNEY, R - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; YIN, D - Henan Agricultural University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/1/2021
Publication Date: 11/16/2021
Publication URL: https://handle.nal.usda.gov/10113/7567339
Citation: Zhang, X., Pandey, M.K., Wang, J., Zhao, K., Ma, X., Li, Z., Zhao, K., Gong, F., Guo, B., Varshney, R.K., Yin, D. 2021. Chromatin spatial organization of wild type and mutant peanuts reveals high-resolution genomic architectures and interaction alterations. Genome Biology. 22:315. https://doi.org/10.1186/s13059-021-02520-x.
DOI: https://doi.org/10.1186/s13059-021-02520-x

Interpretive Summary: The three-dimensional (3D) chromatin organization provides critical foundation to reveal the gene expression regulation and cellular homeostasis. Here, we present the first 3D genome architecture map and chromatin compartments in a mutant and a wild type of allotetraploid peanut lines, which illustrated the A/B compartments, topologically associated domains (TADs), and widespread chromatin interactions. The greater proportion of peanut chromosomal arms (52.3%) had active regions (A compartment) showing higher gene density and higher transcriptional levels. The analysis revealed 2.0% chromosomal region switching from inactive to active regions (B-to-A) in mutant line harboring 58 differentially expressed genes enriched in flavonoid biosynthesis and circadian rhythm-plant. The mutant peanut line showed higher number of genome-wide cis-interactions (11493 in A-subgenome and 16058 in B-subgenome) than those in its wild-type with specific cis-interactions (14890) enriched in chr.03, chr.14, and chr.15. The 3D maps revealed genome-wide 485 merges, 207 splits, and 167 rearrangements among TADs between the wild-type and mutant lines. The analysis also identified a new TAD in the mutant which generated different chromatin loops, harboring a specific AP2EREBP-binding motif in the upstream of GA2ox, which upregulates the expression of GA2ox gene and decreases active gibberellins (GAs) content, and eventually making the mutant plant dwarf. This study not only provides the first genome-wide characterization of 3D genome structure and chromatin accessibility in peanut, but also improved understanding of relationship between chromatin organization and gene regulation in plants.

Technical Abstract: Chromatin, the main carrier of genetic information, is folded to confined spatial structure within a preferred but not fixed chromosome territory in the nucleus. Lack of information on the chromatin spatial organization and chromosome structures in the plant genome could make it so difficult to understand the gene regulation and cellular homeostasis. This study applied the high-throughput chromosome conformation capture technology and assay for transposase-accessible chromatin sequencing provided opportunity to decipher the three-dimensional (3D) genome architecture and to dissect the relationship between the chromatin organization and gene expression in various biological processes in peanut using two peanut lines, the wild-type and its dwarf mutant, including gene express profiles of different tissues, chromatin accessibility, and 3D genome architecture. The integrative analyses provided great insights into the 3D genome architecture and chromatin accessibility in peanut, aiming to reveal the multiple layer of coordinated regulation of genes involved in important biological processes in plants, which may help further for peanut research community to explore and understand genome compartmentalization in gene regulation for agronomic, stress tolerance, and quality traits and features.