Genome shock in a synthetic allotetraploid wheat invokes subgenome-partitioned gene regulation, meiotic instability, and karyotype variation.

It is becoming increasingly evident that interspecific hybridization at the homoploid level or coupled with whole-genome duplication (i.e. allopolyploidization) has played a major role in biological evolution. However, the direct impacts of hybridization and allopolyploidization on genome structure and function, phenotype, and fitness remains to be fully understood. Synthetic hybrids and allopolyploids are trackable experimental systems that can be used to address this issue. In this study, we resynthesized a pair of reciprocal F1 hybrids and corresponding reciprocal allotetraploids using the two diploid progenitor species of bread wheat (Triticum aestivum, BBAADD), namely T. urartu (AA) and Aegilops tauschii (DD). By comparing phenotypes related to growth, development, and fitness, and by analysing genome expression in both hybrids and allotetraploids in relation to the parents, we found that the types and trends of karyotype variation in the immediately formed allotetraploids were correlated with both instability of meiosis and chromosome- and subgenome-biased expression. We determined clear advantages of allotetraploids over diploid F1 hybrids in several morphological traits including fitness that mirrored the tissue- and developmental stage-dependent subgenome-partitioning of the allotetraploids. The allotetraploids were meiotically unstable primarily due to homoeologous pairing that varied dramatically among the chromosomes. Nonetheless, the manifestation of organismal karyotype variation and the occurrence of meiotic irregularity were not concordant, suggesting a role of functional constraints probably imposed by subgenome- and chromosome-biased gene expression. Our results provide new insights into the direct impacts and consequences of hybridization and allopolyploidization that are relevant to evolution and likely to be informative for future crop improvement approaches using synthetic polyploids.