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

ABSTRACT: 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.

ORGANISM(S): Triticum turgidum Aegilops tauschii Triticum aestivum

PROVIDER: GSE56587 | GEO | 2014/10/20

SECONDARY ACCESSION(S): PRJNA244006

REPOSITORIES: GEO

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Project description:The three subgenomes (B, A and D) of common wheat (2n=6x=42) are largely intact, which makes extraction of the BBAA subgenomes as organismally independent genomes possible. Availability of such novel extracted tetraploid wheat (Extracted-tetra) provides a unique opportunity to study whether and to what extent the BBAA subgenomes of common wheat have been irreversibly modified, as well as its attendant biological consequences, during their evolutionary trajectory as allohexaploidy. We report here that the extracted-tetra is stable in karyotype but with severely deteriorated phenotypes. Microarray-based transcriptome analysis revealed a substantial portion of differentially expressed genes (down- or up-regulation) between extracted and natural tetraploid wheat, Triticum turgidum, which exceeded the transcriptome divergence at tetraploid level, implying reinforced effects of allopolyploidization and domestication at the allohexaploid level. Great majority of the differentially expressed genes showed additive expression in a resynthesized allohexaploid wheat (parented by Extracted-tetra), indicating transcriptome modifications to the BBAA subgenomes are largely irreversible. Analysis of a newly synthesized allohexaploid wheat (parented by T. turgidum) suggests that whereas most of the modified genes are accrued evolutionary changes, some showed immediate regulation post-allohexaploidization and evolutionary perseverance. Homeologue-specific pyrosequencing of 44 genes revealed either concordant or independent expression changes to the B and A homeologues. The Extracted-tetra vs.T. turgidum down-regulated genes showed enrichment for distinct GO categories. Structurally, the three constituent subgenomes of common wheat, BB, AA and DD, are largely intact with only a few inter-subgenomic translocations. Because of these unique attributes, it is feasible to extract the BBAA subgenomes from the common wheat BBAADD genome by hybridization to a durum line and repeated back-crossing to the hexaploid parent, restituting a novel type of extracted tetraploid wheat, namely Extracted-tetr, with a genome constitution BBAA, virtually identical to the subgenomes BBAA of its common wheat donor. Availability of the extracted-tetra, the resynthesized allohexaploid wheat parented by the extracted-tetra, and newly synthesized allohexaploid wheat parented by natural tetraploid wheat, T. turgidum, provides an excellent system to address the issues of whether and to what extent transcriptome modifications to the BBAA subgenomes of common wheat have occurred since its formation ca. 10,000 years ago, timing of the modifications, and their biological consequences. Here, we have addressed these issues by microarray-based transcriptome analysis.

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

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