Plant 3D Chromatin Organization: Important Insights from Chromosome Conformation Capture Analyses of the Last 10 Years

Abstract

Over the past few decades, eukaryotic linear genomes and epigenomes have been widely and extensively studied for understanding gene expression regulation. More recently, the three-dimensional (3-D) chromatin organization was found to be important for determining genome functionality, finely tuning physiological processes for appropriate cellular responses. With the development of visualization techniques and chromatin conformation capture (3C)-based techniques, increasing evidence indicates that chromosomal architecture characteristics and chromatin domains with different epigenetic modification in the nucleus are correlated to transcriptional activities. Subsequent studies have further explored the intricate interplay between 3-D genome organization and the function of interacting regions. In this review, we summarize spatial distribution patterns of chromatin, including chromatin positioning, configurations and domains, with a particular focus on the effect of a unique form of interaction between a variety of factors that shapes the 3-D genome conformation in plants. We further discuss the methods, advantages and limitations of various chromatin conformation capture (3C)-based techniques, highlighting the applications of these technologies in plants to identify chromatin domains, and address their dynamic changes and functional implications in evolution, and adaptation to development and changing environmental conditions. Moreover, the future implications and emerging research directions of 3-D genome organization are discussed.

Understanding 3D Genome Organization and Its Effect on Transcriptional Gene Regulation Under Environmental Stress in Plant: A Chromatin Perspective

“…In Rabl configuration, the chromosomes are folded at the centromere making a polarized separation of centromeres and telomeres ( Figure 1A ). Such configuration is observed in diverse organisms (animals, yeasts, and plants) ( Huang Y. et al, 2020 ; Zhang and Wang, 2021 ). The existence of different chromosome configurations within an organism suggested its specificity in different cell types.…”

“…TADs are not reported in Arabidopsis because of the small genome size, as prominent TADs could not be detected in the species having smaller (<400 Mb) genomes ( Dong et al, 2017 ; Stam et al, 2019 ). However, the effect of genome size on TAD formation is still under debate ( Zhang and Wang, 2021 ). It is also speculated that TADs are displayed in plants having lower gene density/larger genome size ( Dogan and Liu, 2018 ).…”

“…( Eberharter and Becker, 2002 ; Clapier et al, 2017 ). Studies show the hierarchical organization of genomes, wherein chromosome territories (CTs) are at the top of the hierarchical structure, followed by the chromosome compartments, topologically associating domains (TADs) and gene body/chromatin loops ( Pecinka et al, 2004 ; Amano et al, 2009 ; Zhang and Wang, 2021 ). 3D genomics helps to decipher the spatial chromatin configurations and investigate their regulatory roles in gene expression ( Gonzalez-Sandoval and Gasser, 2016 ).…”

“…Chromatin architecture at the promoter region is more crucial for determining the level of gene expression ( Tannenbaum et al, 2018 ; Barragán-Rosillo et al, 2021 ). Advances in chromatin visualization, NGS, and 3C-based techniques have accumulated evidence for chromosome architecture, chromatin domains/loops and different epigenetic modifications to be correlated with transcriptional activities ( Zhang and Wang, 2021 ). Studies suggest a functional correlation among the changes in nuclear organization, stressful conditions, and the level of gene expression.…”

“…Tight coiling of chromatin (a default state) restricts transcriptional expression of the gene, which gets expressed when the nearby chromatin is loosened (remodeled) ( Bannister and Kouzarides, 2011 ). The accumulating datasets on epigenomics ( Kumar and Mohapatra, 2021 ) and the evident roles of genome architecture on the regulation of gene expression ( Zhang and Wang, 2021 ) indicate that 3D genomics would be an important player in deciphering the key regulators. Developmental and environmental stimuli affect epigenetic landscape and chromatin architecture, which are dynamic and modulate gene expression to cope with stress ( Bhadouriya et al, 2021 ).…”