Spatial and Temporal Transcriptomic Heredity and Asymmetry in an Artificially Constructed Allotetraploid Wheat (AADD)

Polyploidy, or whole-genome duplication (WGD), often induces dramatic changes in gene expression due to "transcriptome shock. " However, questions remain about how allopolyploidy (the merging of multiple nuclear genomes in the same nucleus) affects gene expression within and across multiple tissues and developmental stages during the initial foundation of allopolyploid plants. Here, we systematically investigated the immediate effect of allopolyploidy on gene expression variation in an artificial allopolyploidy system consisting of a constructed allotetraploid wheat (AADD genome, accession AT2) and its diploid progenitors Triticum urartu and Aegilops tauschii. We performed comprehensive RNA sequencing of 81 samples from different genotypes, tissues, and developmental stages. First, we found that intrinsic interspecific differences between the diploid parents played a major role in establishing the expression architecture of the allopolyploid. Nonetheless, allopolyploidy per se also induced dramatic and asymmetric patterns of differential gene expression between the subgenomes, and genes from the D subgenome exhibited a more drastic response. Second, analysis of homoeolog expression bias (HEB) revealed that the D subgenome exhibited significant expression bias and that de novo-generated HEB was attributed mainly to asymmetrical differential gene expression. Homoeolog-specific expression (HSE) analyses showed that the cis-only regulatory pattern was predominant in AT2, reflecting significant divergence between the parents. Co-expression network analysis revealed that homoeolog expression connectivity (HEC) was significantly correlated with sequence divergence in cis elements between subgenomes. Interestingly, allopolyploidy-induced reconstruction of network modules was also associated with different HSE patterns. Finally, a transcriptome atlas of spike development demonstrated that the phenotypic similarity of AT2 to T. urartu may be attributed to the combination of relatively stable expression of A-subgenome genes and drastic downregulation of their D-subgenome homoeologs. These findings provide a broad, multidimensional characterization of allopolyploidy-induced transcriptomic responses and suggest that allopolyploidy can have immediate and complex regulatory effects on the expression of nuclear genes.