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.