3D Chromatin Architecture of Large Plant Genomes Determined by Local A/B Compartments

Abstract

The spatial organization of the genome plays an important role in the regulation of gene expression. However, the core structural features of animal genomes, such as topologically associated domains (TADs) and chromatin loops, are not prominent in the extremely compact Arabidopsis genome. In this study, we examine the chromatin architecture, as well as their DNA methylation, histone modifications, accessible chromatin, and gene expression, of maize, tomato, sorghum, foxtail millet, and rice with genome sizes ranging from 0.4 to 2.4 Gb. We found that these plant genomes can be divided into mammalian-like A/B compartments. At higher resolution, the chromosomes of these plants can be further partitioned to local A/B compartments that reflect their euchromatin, heterochromatin, and polycomb status. Chromatins in all these plants are organized into domains that are not conserved across species. They show similarity to the Drosophila compartment domains, and are clustered into active, polycomb, repressive, and intermediate types based on their transcriptional activities and epigenetic signatures, with domain border overlaps with the local A/B compartment junctions. In the large maize and tomato genomes, we observed extensive chromatin loops. However, unlike the mammalian chromatin loops that are enriched at the TAD border, plant chromatin loops are often formed between gene islands outside the repressive domains and are closely associated with active compartments. Our study indicates that plants have complex and unique 3D chromatin architectures, which require further study to elucidate their biological functions.

Genetic, epigenetic and genomic effects on variation of gene expression among grape varieties

“…Clusters of coregulated genes could arise as a result of different underlying molecular mechanisms. Attempts to identify higher‐order chromatin structures in plants, such as TADs, which have been successfully identified in Drosophila , mouse and humans, among others (Dixon et al ., ; Nora et al ., ; Sexton et al ., ), where clusters of coregulated genes have often been observed (Nora et al ., ), have not yet been very successful (Wang et al ., , ; Liu et al ., , ; Dong et al ., ). Also, examples of individual enhancers (Lower et al ., ; Jin et al ., ) or superenhancers (Novo et al ., ) that can exert their effects over several genes have not yet been reported for plants.…”

A critical evaluation of the role of ethylene and MADS transcription factors in the network controlling fleshy fruit ripening

“…Selected genes whose expression increases during ripening are listed in Table . Recent developments have focused on the importance of genome‐wide methylation status (Manning et al ., ; Zhong et al ., ) and chromatin histone marks (Dong et al ., ) for the expression of ripening genes, discussed later. The view that has emerged is of an interacting network of transcription factors and hormone biosynthesis and signaling genes that orchestrate a cascade of events, culminating in the expression of many hundreds, perhaps thousands, of genes that contribute to the ripening process (M. C. Liu et al ., , ; Giovannoni et al ., ; Shinozaki et al ., ).…”

Forces driving the three‐dimensional folding of eukaryotic genomes

“…On the basis of this new knowledge, whole‐genome conformation studies have been used to decipher how development or developmental disease (Dixon et al , ; Fraser et al , ; Lupiáñez et al , ; Franke et al , ; Bonev et al , ), cancer (Flavahan et al , ; Taberlay et al , ; Hnisz et al , ; Wu et al , ), DNA damage (Aymard et al , ; Canela et al , ), cellular aging (Criscione et al , ), and genetic variation (Javierre et al , ) impact on the structure and function of the genome. Needless to say that the advent of 3C technology (see overview in Denker & de Laat, ) has also provided insights into the higher order genomic organization of bacteria (e.g., Le & Laub, ; Lioy et al , ), fungi (e.g., Mizuguchi et al , ; Kim et al , ; Tanizawa et al , ), nematodes (e.g., Crane et al , ), the Plasmodium falciparum parasite (Ay et al , ), and plants (e.g., Dong et al , ). It is noteworthy that A‐/B‐compartments and TAD‐like structures can largely be identified across all organisms investigated to date.…”

“…Along the same lines, numerous organisms lack orthologues of CTCF, but do exhibit insulated TAD-like domains in Hi-C experiments; these include Caenorhabditis elegans (Crane et al, 2015), Arabidopsis thaliana (Dong et al, 2017), Schizosaccharomyces pombe (Mizuguchi et al, 2014), or Caulobacter crescentus and Escherichia coli (Le & Laub, 2016;Lioy et al, 2018). For example, in an elegant genome editing experiment, insertion of the strongly expressed rsaA bacterial gene in the middle of another TAD gave rise to a novel boundary, the strength of which was progressively diminished as the transcribed sequence of the inserted gene was shortened (Le & Laub, 2016).…”