mRNA and sRNA Transcriptomes Reveal Insights into Dynamic Homoeolog Regulation for Allopolyploid Heterosis in Nascent Hexaploid Wheat

Nascent allohexaploid wheat may represent the initial genetic state for the evolution and domestication of common wheat, which arose by combining the AB genomes of tetraploid Triticum turgidum with the D genome from Aegilops tauschii and out-competed its parents in growth vigor and adaptability. To better understand the molecular basis for this success, we performed mRNA and small RNA expression analyses in three tissues of nascent allohexaploid wheat and its following generations, their progenitors, and Chinese Spring, with the assistance of newly released A and D genome sequences. We found that nonadditive expression was rare among protein-coding genes which exhibited profound parental expression level dominance, with genes of total homoeolog expression level in nascent allohexaploid progeny similar to their expression levels in T. turgidum functionally enriched for development and those to Ae. tauschii distinctively for adaptation. In contrast, miRNAs appeared to be sensitive to polyploidization, with nonadditively expressed miRNAs potentially involved in growth vigor and adaptation. Meanwhile, siRNAs may contribute to biased repression of D homoeolog, possibly due to increased siRNA density on transposable element (TE)-associated D homoeologs. Together, our data provide new insights into homoeolog regulatory mechanisms that may be essential to heterosis in nascent hexaploid wheat. Overall design: We performed mRNA and small RNA analyses in three tissues of nascent allohexaploid wheat and its following generations, their progenitors, and Chinese Spring.Among these samples, Samples 1-6 and 26-31, tetraploid progenitors; Samples 7-12 and 32-37, diploid progenitors; Samples 13-22 and 38-47, following generations; Samples 23-25 and 48-50, Chinese Spring.