Asymmetrical changes of gene expression, small RNAs and chromatin in two resynthesized wheat allotetraploids

Abstract

Polyploidy occurs in some animals and all flowering plants, including important crops such as wheat. The consequences of polyploidy in crops remain elusive, partly because their progenitors are unknown. Using two resynthesized wheat allotetraploids S S AA and AADD with known diploid progenitors, we analyzed mRNA and small RNA transcriptomes in the endosperm, compared transcriptomes between endosperm and root in AADD, and examined chromatin changes in the allotetraploids. In the endosperm, there were more non-additively expressed genes in S S AA than in AADD. In AADD, non-additively expressed genes were developmentally regulated, and the majority (62-70%) were repressed. The repressed genes in AADD included a group of histone methyltransferase gene homologs, which correlated with reduced histone H3K9me2 levels and activation of various transposable elements in AADD. In S S AA, there was a tendency for expression dominance of S over A homoeologs, but the histone methyltransferase gene homologs were additively expressed, correlating with insignificant changes in histone H3K9me2 levels. Moreover, more 24-nucleotide small inferring RNAs (siRNAs) in the A subgenome were disrupted in AADD than in S S AA, which were associated with expression changes of siRNA-associated genes. Our results indicate that asymmetrical changes in siRNAs, chromatin modifications, transposons and gene expression coincide with unstable AADD genomes and stable S S AA genomes, which could help explain the evolutionary trajectories of wheat allotetraploids formed by different progenitors.

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

“…This pattern of reduced expression may reflect balancing gene expression in which approximately 70% of 1:1:1 AABBDD homoeologs are expressed at an approximate mid-point level (Ramírez-González et al 2018) . Similar overall reductions in expression have also 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.…”

“…Changes in small RNA and chromatin, as measured by chromosome immunofluorescence (Jiao et al 2018) , accompany the formation of new allotetraploid wheat lines, suggesting some forms of chromatin modification may contribute to altered gene expression in wheat allopolyploids.…”

“…In newly synthesised allohexaploid wheat (Chagué et al 2010) and tetraploid AADD and S'S'AA (where S'S' is Ae. longissima ) (Jiao et al 2018) wheat lines between 60-80% of genes were additively expressed, suggesting a dynamic re-adjustment of gene expression patterns as a consequence of allopolyploidy . Rapid asymmetric changes in short RNA, histone methylation and gene expression in the two allotetraploids were also observed and were thought to contribute to genome-biased gene expression and the activation of TE transcription (Jiao et al 2018) .…”

The allotetraploid origin and asymmetrical genome evolution of common carp Cyprinus carpio

“…The faster methylation change rate suggested that, rather than vast gene loss and sequence substitution, epigenomic evolution provided quick and efficient regulation to deal with the massive changes of "genome shock" after the genome merger and ensured the survival of the tetraploidized C. carpio. Many evolutionary studies on allotetraploid genomes suggested that dominantly expressed subgenomes tend to have less methylation sites in genic regions [45][46][47][48] . Therefore, we compared the global DNA methylation level of two subgenomes and looked for epigenetic evidence of subgenome dominance in C. carpio based on all annotated genes.…”

Evolutionary and ecological functional genomics, from lab to the wild

“…This study analyzed various mutants, and studied the distribution, context and periodicity of genome methylation including at rDNA genes and telomeres, which were inaccessible to previous methods. Although single‐base‐pair resolution epigenomes have been obtained for plant species as diverse as melon (Martin et al ., ), rice (Li et al ., ), tomato (Zhong et al ., ), wheat (Jiao et al ., ), spruce (Ausin et al ., ) and apple (Daccord et al ., ), most work on dissecting epigenomic mechanisms has been done in the model plant A. thaliana (Liu, ; Seymour and Becker, ; Springer and Schmitz, ).…”