Reduced chromatin accessibility underlies gene expression differences in homologous chromosome arms of diploid Aegilops tauschii and hexaploid wheat.

Fu-Hao Lu,Ming-Cheng Luo,Michael W Bevan,Laura-Jayne Gardiner,Neil Mckenzie,Anthony Hall

doi:10.1093/gigascience/giaa070

Abstract

BackgroundPolyploidy is centrally important in the evolution and domestication of plants because it leads to major genomic changes, such as altered patterns of gene expression, which are thought to underlie the emergence of new traits. Despite the common occurrence of these globally altered patterns of gene expression in polyploids, the mechanisms involved are not well understood.ResultsUsing a precisely defined framework of highly conserved syntenic genes on hexaploid wheat chromosome 3DL and its progenitor 3 L chromosome arm of diploid Aegilops tauschii, we show that 70% of these gene pairs exhibited proportionately reduced gene expression, in which expression in the hexaploid context of the 3DL genes was ∼40% of the levels observed in diploid Ae tauschii. Several genes showed elevated expression during the later stages of grain development in wheat compared with Ae tauschii. Gene sequence and methylation differences probably accounted for only a few cases of differences in gene expression. In contrast, chromosome-wide patterns of reduced chromatin accessibility of genes in the hexaploid chromosome arm compared with its diploid progenitor were correlated with both reduced gene expression and the imposition of new patterns of gene expression.ConclusionsOur pilot-scale analyses show that chromatin compaction may orchestrate reduced gene expression levels in the hexaploid chromosome arm of wheat compared to its diploid progenitor chromosome arm.

Highlights

Polyploidy arises from the duplication of genomes or the fusion of genomes from different species and has occurred frequently in the lineages of many organisms, from fish to flowering plants (Otto 2007)
70% of the gene pairs were expressed in the five analysed tissues (Additional File 2: Figure S1), and of these, 70% showed a proportionate reduction in gene expression in wheat, in which expression of the DD gene complement in the AABBDD genome fell to 40% of that measured in the DD genome of Ae. tauschii, and the overall expression of 1:1:1 AABBDD homoeologs was 1.2 times higher than in the DD genome
Similar overall reductions in expression have been observed in newly formed wheat hybrids (Akhunova et al 2010; Jiao et al 2018; Chelaifa et al 2013), suggesting a dynamic re-alignment of gene expression to near-diploid levels is an early consequence of allopolyploidy for the majority of wheat genes

Summary

Introduction

Polyploidy arises from the duplication of genomes or the fusion of genomes from different species and has occurred frequently in the lineages of many organisms, from fish to flowering plants (Otto 2007). Maize is an ancient tetraploid that has been re-diploidized by recombination of homoeologous chromosomes, leading to traces of two sub-genomes called maize and maize, which differentially retain duplicated genes (Gaut and Doebley 1997; Schnable et al 2011) These preferentially retained genes were more highly expressed (Renny-Byfield et al 2017), and had different patterns of DNA methylation that were correlated with expression differences, but it was not possible to establish causal relationships between methylation differences and gene expression. RNAseq analyses of newly formed allotriploid ABD and stable allohexaploid AABBDD lines generated from T. turgidum AABB with Ae. tauschii DD showed rapid and extensive changes in gene expression in triploid tissues that were partly restored upon genome duplication (Hao et al 2017). Dramatically reduced chromatin accessibility in genes in the hexaploid context indicated a novel role for chromatin dynamics in altered gene expression

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Conclusion