Evolutionary dynamics of 3D genome architecture following polyploidization in cotton

Abstract

The formation of polyploids significantly increases the complexity of transcriptional regulation, which is expected to be reflected in sophisticated higher-order chromatin structures. However, knowledge of three-dimensional (3D) genome structure and its dynamics during polyploidization remains poor. Here, we characterize 3D genome architectures for diploid and tetraploid cotton, and find the existence of A/B compartments and topologically associated domains (TADs). By comparing each subgenome in tetraploids with its extant diploid progenitor, we find that genome allopolyploidization has contributed to the switching of A/B compartments and the reorganization of TADs in both subgenomes. We also show that the formation of TAD boundaries during polyploidization preferentially occurs in open chromatin, coinciding with the deposition of active chromatin modification. Furthermore, analysis of inter-subgenomic chromatin interactions has revealed the spatial proximity of homoeologous genes, possibly associated with their coordinated expression. This study advances our understanding of chromatin organization in plants and sheds new light on the relationship between 3D genome evolution and transcriptional regulation.

The causes and consequences of subgenome dominance in hybrids and recent polyploids

“…DNA methylation patterns are stable and largely heritable, but higher‐level chromatin modifications such as histone acetylation or phosphorylation are more dynamic. Recent work in cotton was the first to look at three‐dimensional chromatin dynamics in allopolyploid and diploid progenitors and identified widespread reorganization of topologically associated domains in cotton that was associated with changes in methylation and chromatin status (Wang et al ., ). Shifts in chromatin accessibility and DNA methylation significantly impact gene regulation and expression, and may be central to the establishment of subgenome dominance.…”

Chromatin Dynamics upon DNA Damage

“…It has been proposed that TADs are formed through a dynamics process of loop extrusion [10], and it has been proposed that cohesin and CTCF proteins are associated with the dynamics formation of TADs and loops [11]. Chromatin organization in TADs is not found in all organisms: for example, TADs appear to be absent in A. thaliana (genome size 135 Mb) [12,13] but present in other plants [14]; in M. pneumonia, bacterial TAD-like domains of 15-33 kb (named chromosomal interaction domains, CIDs) have been described [15]. In Saccharomyces cerevisiae yeast, the primary level of organization appears to be shorter than TADs, with domains of 1-5 genes forming compact gene crumples, or globules, rather than loops [16], although the conclusion that TADs and loops are absent in budding yeast remains contentious [17,18].…”

The importance and prevalence of allopolyploidy in Aotearoa New Zealand

“…Intermediacy in polyploids was described in the seminal works by Stebbins (1947Stebbins ( , 1950, who later asserted the inefficiency of selection in duplicated genomes, deeming polyploids to be evolutionary dead-ends (Stebbins 1971). Stebbins' view, the 'dead-end hypothesis', has seen increasing opposition through subsequent discoveries of recurrent polyploidy (Soltis and Soltis 1999), substantial dynamism within polyploid genomes (Scannell et al 2006;Flagel and Wendel 2009;Parisod et al 2009;Chester et al 2012;Wang et al 2015;Wang et al 2018) and the presence of an ancestral polyploidy event at the base of the major land plant radiation (Jiao et al 2011).…”

“…Indeed, this phrase aptly captures the essence of this potentially catastrophic array of structural and biochemical changes that can occur, near-instantaneously, from ploidy elevation and hybridisation within the nascent allopolyploid genome. The suite of potential biological responses, both rapid and longer term, employed by the allopolyploid in response to genome shock have many potential manifestations, including genomic restructuring (Lim et al 2008;Wu et al 2015;Qin et al 2016;Wang et al 2018) and gene loss (Scannell et al 2006;Gordon et al 2009;Vallejo-Marín et al 2015). Although the impact of allopolyploidy is most often viewed through the lens of nuclear genomic studies, organellar genomes (Sloan et al 2018), small RNAs (Ha et al 2009;Jiao et al 2018) and the gene expression profiles of allopolyploid species (Yoo et al 2014;Jung et al 2015) are also affected.…”