Subgenome Interplay Shapes Genomic Variations and Transcriptomic Changes during Wheat Hexaploidization Events

Genomic variations and transcriptomic changes extensively occur in newly formed polyploids to reconcile immediate challenges caused by divergent subgenomes in one nucleus. To comprehensively investigate sequence elimination and expression alteration in wheat hexaploidization, here we performed whole exome capture experiments coupled with high throughput sequencing analysis by exploiting three sets of newly synthesized wheat species. We observed that the whole wheat chromosomes were subjected to extensive genomic elimination partially regulated by sequence homology in response to hexaploidization. But homeologous subgenomes exhibited distinct features that DNA sequences were preferentially eliminated on DD genome compared with AA and BB genome. In addition, a higher proportion of eliminated sequences occurred in exonic regions than in intergenic regions on DD genome, whereas a significant enrichment was observed in the repeat-rich intergenic regions for AA and BB genome, exhibiting a contrast distribution pattern compared to the gene density. Furthermore, we detected 488 overlapped genes with sequence elimination on DD genome but few on the other two genomes across three nascent hexaploid wheats. Interestingly, GO enrichment analysis showed genes with sequence elimination were enriched in distinct functional pathways between subgenomes. Transcriptome analysis indicates polyploidization enhanced gene expression differentiation between root and leaf and led to rapid and extensive gene expression changes in synthetic hexaploid wheat. AA and BB genome exhibited synergistic expression profiling which was distinct from DD genome, and interestingly, expression bias was observed for a proportion of homeologs in synthetic hexaploid wheat. Strikingly, only 3.3-23.6% genes with sequence elimination exhibited expression changes in synthetic hexaploid wheat compared with their respective progenitors, indicating genomic variation is not the major cause resulting in the transcirptomic changes during wheat polyploidization events, whereas epigenetic modifications might play an important role in regulating expression profiling alterations.