Wheat chromatin architecture is organized in genome territories and transcription factories

Abstract

Background: Polyploidy is ubiquitous in eukaryotic plant and fungal lineages, and it leads to the coexistence of several copies of similar or related genomes in one nucleus. In plants, polyploidy is considered a major factor in successful domestication. However, polyploidy challenges chromosome folding architecture in the nucleus to establish functional structures. Results: We examine the hexaploid wheat nuclear architecture by integrating RNA-seq, ChIP-seq, ATAC-seq, Hi-C, and Hi-ChIP data. Our results highlight the presence of three levels of large-scale spatial organization: the arrangement into genome territories, the diametrical separation between facultative and constitutive heterochromatin, and the organization of RNA polymerase II around transcription factories. We demonstrate the micro-compartmentalization of transcriptionally active genes determined by physical interactions between genes with specific euchromatic histone modifications. Both intra-and interchromosomal RNA polymerase-associated contacts involve multiple genes displaying similar expression levels. Conclusions: Our results provide new insights into the physical chromosome organization of a polyploid genome, as well as on the relationship between epigenetic marks and chromosome conformation to determine a 3D spatial organization of gene expression, a key factor governing gene transcription in polyploids.

Homology-mediated inter-chromosomal interactions in hexaploid wheat lead to specific subgenome territories following polyploidization and introgression

“…A similar two diagonal pattern was also reported for barley [ 27 ] and reflects the Rabl configuration [ 28 ], in which chromosomes fold back with centromeres and telomeres clustering at the opposite sides of the nucleus, leading to the adjacency of long and short arms. These results are consistent with the findings of earlier cytological studies [ 28 , 29 ] and recent Hi-C report in CS [ 3 ].

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“…The resulting tetraploid wheat hybridized with goatgrass ( Aegilops tauschii ; DD, 2n = 2x = 14) to produce an ancestral hexaploid wheat species approximately 10,000 years ago. In previous studies, genomic in situ hybridization (GISH) and Hi-C data revealed that the three subgenomes of hexaploid wheat tend to localize to specific nuclear territories [ 3 – 5 ]. Additionally, interactions are more common between subgenomes A and B than between subgenomes A and D or B and D. These findings indicate that the higher-order chromosomal organization may be maintained following tetraploidization and hexaploidization processes [ 3 ].…”

“…In plants, chromosomal loops have been detected in all species characterized in high-throughput chromatin conformation capture studies, including Arabidopsis [ 12 – 15 ], rice [ 24 ], maize [ 25 , 26 ], and cotton [ 17 ], suggesting that they may have conserved biological functions [ 19 ]. A recent Hi-C study involving the wheat cultivar Chinese Spring (CS) revealed the highly coordinated expression of loop-connected genes [ 3 ]. Therefore, the relationship between chromosomal loops with TADs and their potential regulatory roles in common wheat are interesting issues for further investigation.…”

Where the Wild Things Are: Transposable Elements as Drivers of Structural and Functional Variations in the Wheat Genome

“…The wheat group offers an ideal system to study the evolution of polyploidy due to the ability to conduct comparative analyses between available species with different ploidy levels and since newly formed wheat allopolyploids can be easily produced in the greenhouse (Li et al, 2018). In light of the recent developments in wheat genomics, the examination of new models based on whole genome sequencing, epigenetic, and 3D analysis (Concia et al, 2020) is now technically possible for newly synthesized allopolyploids. Studies of TE dynamics in newly synthesized wheat allopolyploids might deepen our understanding of the effect of perturbation on host: TE dynamics (Roessler et al, 2018) and on the possible effect of the 3D genome organization on TEs insertion sites and propagation across the nucleus (Bousios et al, 2020).…”

Genomic, Transcriptomic and Epigenomic Tools to Study the Domestication of Plants and Animals: A Field Guide for Beginners

“…An extended synthesis framework should also be considered to understand domestication, as these new studies are helping us understand niche construction and the emergence of domesticated phenotypes (Piperno, 2017). Other potential lines of work remain to be addressed in domestication studies, such as the changes in the chromatin architecture (e.g., Concia et al, 2020), the use of comparative proteomic atlases (e.g., Jiang Y. et al, 2019) and the analysis of cell-type divergences during development using single-cell RNA-seq data (Arendt et al, 2016). The use of this multi-omic approaches will help us create and compare developmental atlases (e.g., Walley et al, 2016) between wild and domesticated taxa to understand how morphology diverged during domestication.…”