Wheat chromatin architecture is organized in genome territories and transcription factories
Lorenzo Concia, Alaguraj Veluchamy, Juan S. Ramirez-Prado, Azahara C. Martín, Ying Huang, Magali Perez, Séverine Domenichini, Natalia Yaneth Rodriguez‐Granados, Soon-Kap Kim, Thomas Blein, Susan Duncan, Clement Pichot, Deborah Manza-Mianza, Caroline Juéry, Etienne Paux, Graham Moore, Heribert Hirt, Catherine Bergounioux, Martín Crespi, Magdy M. Mahfouz, Abdelhafid Bendahmane, Chang Liu, Anthony Hall, Cécile Raynaud, David Latrasse, Moussa Benhamed
Abstract
BACKGROUND: Polyploidy is ubiquitous in eukaryotic plant and fungal lineages, and it leads to the co-existence 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.