Differential chromatin accessibility landscape reveals structural and functional features of the allopolyploid wheat chromosomes

Authors: Jordan, Katherine; HE, FEI - Kansas State University; FERNANDEZ DE SOTO, MONICA - Kansas State University; AKHUNOVA, ALINA - Kansas State University; AKHUNOV, EDUARD - Kansas State University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/6/2020
Publication Date: 7/19/2020
Citation: Jordan, K., He, F., Fernandez De Soto, M., Akhunova, A., Akhunov, E. 2020. Differential chromatin accessibility landscape reveals structural and functional features of the allopolyploid wheat chromosomes. Genome Biology. 21. Article 176. https://doi.org/10.1186/s13059-020-02093-1.
DOI: https://doi.org/10.1186/s13059-020-02093-1

Interpretive Summary: The wheat genome is very large and complex, representing over 16 billion bases of DNA sequence. The gene-coding portion, which represents approximately 10% of the genome, is not all equally available for gene and phenotype expression. Some segments of chromatin are tightly bound to histone proteins to form nucleosomes and are therefore inaccessible (closed) for transcription factors and RNA polymerase to bind to DNA and regulate gene expression, while other segments of chromatin are not bound to nucleosomes and are therefore accessible (open) for DNA binding. This study used a differential nuclease sensitivity assay to score the degree of openness across the entire wheat genome. We found that chromatin accessibility scores are highest near the tips of the chromosomes and lowest at the centromeres. Accessibility positively correlates with recombination rate, gene expression levels, and proximity to genes, however, we find a substantial proportion of potential regulatory regions quite a distance from genes within the repetitive, noncoding 90% of the genome. This study provides new tools to prioritize genetic variation that affects both gene and trait expression in wheat.

Technical Abstract: Background: We have a limited understanding of how the complexity of the wheat genome influences the distribution of chromatin states along the homoeologous chromosomes. Using a differential nuclease sensitivity (DNS) assay, we investigated the chromatin states in the coding and transposon element (TE)-rich repetitive regions of the allopolyploid wheat genome. Results: We observed a negative chromatin accessibility gradient along the telomere-centromere axis with mostly open and closed chromatin located in the distal and pericentromeric regions of chromosomes, respectively. This trend was mirrored by the TE-rich intergenic regions, but not by the genic regions, which showed similar averages of chromatin accessibility levels along the chromosomes. The genes’ proximity to TEs was negatively associated with chromatin accessibility. The chromatin states of TEs was dependent on their type, proximity to genes, and chromosomal position. Both the distance between genes and TE composition appear to play a more important role in the chromatin accessibility along the chromosomes than chromosomal position. The majority of MNase hypersensitive regions were located within the TEs. The DNS assay accurately predicted previously detected centromere locations. SNPs located within more accessible chromatin explain a higher proportion of genetic variance for a number of agronomic traits than SNPs located within closed chromatin. Conclusions: The chromatin states in the wheat genome are shaped by the interplay of repetitive and gene-encoding regions that are predictive of the functional and structural organization of chromosomes, providing a powerful framework for detecting genomic features involved in gene regulation and prioritizing genomic variation to explain phenotypes.