Transcriptome Shock Invokes Disruption of Parental Expression-Conserved Genes in Tetraploid Wheat

Allopolyploidy, entailing whole genome duplication (WGD) of merged divergent genomes of different species, often instigates transcriptome shock, whereby both total gene expression level and homeolog expression partitioning can be disrupted and remodeled. Little is known about the extent to which the parental expression-conserved genes will be disrupted/remodeled by allopolyploidization, nor the evolutionary relevancy of shock-induced expression repatterning. Here, by microarray-based gene expression profiling and gene-specific cDNA-pyrosequencing, we assessed transgenerational transcriptome shock in a synthetic allotetraploid wheat (AT2) with karyotype and basic morphology mimicking those of natural tetraploid wheat, Triticum turgidum. We show that the transcriptome shock in AT2 is exceptionally strong that it disrupted intrinsically conserved parental gene expression, and resulted in extensive expression nonadditivity in the newly formed allotetraploid plants. At total expression level, a substantial proportion of shock-induced novel expression, especially over-transgressive expression, was rapidly stabilized already in early generations of AT2. Extensive remodeling of homeolog expression occurred in AT2, including those genes that showed additive total expression, and which generated subgenome expression dominance, a pattern that mirrors T. turgidum. Thus, the shock-induced new patterns of gene expression at both the total expression level and subgenome homeolog partitioning showed evidence of evolutionary persistence. Complex relationships between homeolog expression remodeling and nonadditive total expression were observed in a tissue-specific manner.

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