Genome Shock in a Synthetic Allotetraploid Wheat Invokes Subgenome-Partitioned Gene Regulation, Meiotic Instability and Karyotype Variation.

Abstract

It becomes increasingly evident that interspecific hybridization at homoploid level or coupled with whole genome duplication (i.e., allopolyploidization) has played a major role in biological evolution. Yet, the direct impact 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 to address this issue. Here, we resynthesized a pair of reciprocal F1 hybrids and corresponding reciprocal allotetraploids using the two diploid progenitor species, Triticum urartu (AA) and Aegilops tauschii (DD), of bread wheat (Triticum aestivum L., BBAADD). By comparing phenotypes related to growth, development and fitness, andanalyzing genome expression in both hybrids and allotetraploids in relation to parents, we find the types and trends of karyotype variation in the immediately formed allotetraploids, are correlated with both meiosis instability and chromosome- and subgenome-biased expression. We document clear advantages of allotetraploids over diploid F1 hybrids in several morphological traits including fitness, which mirror the tissue- and developmental stage-dependent subgenome-partitioning of the allotetraploids. The allotetraploids are meiotically unstable primarily due to homoeologous pairing that varies dramatically among the chromosomes. Nonetheless, the manifestation of organismal karyotype variation and occurrence of meiotic irregularity are 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, which are relevant to evolution and likely informative to crop improvement by synthetic polyploid approaches.