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 SlSlAA 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 SlSlAA 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 SlSlAA, there was a tendency for expression dominance of Sl 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 SlSlAA, 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 SlSlAA genomes, which could help explain the evolutionary trajectories of wheat allotetraploids formed by different progenitors.