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.新形成的多倍体（polyploidy）本质上与减数分裂稳定性受损密切相关，进而引发染色体结构变异（structural chromosomal variations，SCVs）。然而，并非所有在新生多倍体中出现的SCVs都会在演化后的多倍体物种中得以保留。本研究利用一套完整的合成六倍体小麦植株样本队列，探究原本“短暂存在的SCVs”是否具有跨代影响；该样本队列包含从头发生（de novo）的单向杂合易位与相互杂合易位、源自这些易位的连续三代回复整倍体（euploidy）后代，以及真实野生型整倍体材料。我们通过细致的比较表型分析、转录组（transcriptome）与代谢组（metabolome）图谱分析发现，两种易位均对后代产生了持久且可遗传的影响，且后代丢失了初始的SCVs。有趣的是，回复后代还发生了进一步的可遗传变异，使得部分后代的繁殖适合度（reproductive fitness）高于其携带易位的初始亲本。综上，本研究结果表明，SCVs可能会对携带变异的个体之外的群体产生连锁效应，同时也会影响后续获得的无变异后代。SCVs的这一此前未被认知的突变特性，可能对物种演化与作物遗传改良均具有重要启示。