Wheat chromatin architecture is organized in genome territories and transcription factories

Lorenzo Concia
,
Alaguraj Veluchamy
,
Juan S. Ramirez-Prado
,
Azahara Martin-Ramirez
,
Ying Huang
,
Magali Perez
,
Severine Domenichini
,
Natalia Y. Rodriguez Granados
,
Soonkap Kim
Thomas Blein
Thomas Blein
,
Susan Duncan
,
Clement Pichot
,
Deborah Manza-Mianza
,
Caroline Juery
,
Etienne Paux
,
Graham Moore
,
Heribert Hirt
,
Catherine Bergounioux
,
Martin Crespi
,
Magdy M. Mahfouz
,
Abdelhafid Bendahmane
,
Chang Liu
,
Anthony Hall
,
Cécile Raynaud
,
David Latrasse
,
Moussa Benhamed
Genome biology, Volume 21, Issue 1, April 2020, 104
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.

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