Heritable Knock-on Consequences of Transient Heterozygous Chromosomal Translocation on Phenotype, Transcriptome, and Metabolome in a Synthetic Hexaploid Wheat

Newly formed polyploidy is intrinsically associated with compromised meiosis stability, resulting in structural chromosomal variations (SCVs). However, not all SCVs that occurred in nascent polyploidy are retained in evolved polyploid species. Here, we investigated whether the otherwise ‘ephemeral SCVs’ may have transgenerational impacts by using a complete cohort of plant samples of a synthetic hexaploid wheat, which contains de novo occurred unidirectional and reciprocal heterozygous translocations, three successive generations of revertant euploidy progenies descended from the translocations, and bona fide wild-type euploidy. Our nuanced comparative phenotyping and transcriptome and metabolome profiling indicate that both types of translocations have protracted and heritable impacts on progenies, losing the initial SCVs. Intriguingly, the revertant progenies have undergone further heritable alterations, rendering some of the progenies manifesting a higher reproductive fitness than that of their initial translocation-containing progenitors. Together, our results suggest that SCVs may have knock-on consequences beyond the variant-bearing individuals and also impact the derived variant-free progenies. This previously unrecognized mutational property of SCVs may have implications for both evolution and crop improvement.