Chromosome Translocation Affects Multiple Phenotypes,causes Genome-wide Dysregulation Of Gene Expression,and Remodels Metabolome In Hexaploid Wheat

Polyploidy,or whole-genome duplication(WGD),is increasingly recognized as an important driving force for speciation and evolution,especially,almost all angiosperms have undergone one or more polyploidy events during their evolutionary histories.Polyploidization by doubling the number of chromosomes generates new genotypes,increases genetic diversity,and alters phenotypic space,and hance,provides more raw genetic materials for natural selection and evolution.Therefore,polyploidization is generally considered an important evolutionary mechanism and has significant implications for the formation and maintenance of biodiversity.However,polyploidy also faces the challenge of meiotic and/or mitotic abnormalities in the abruptly doubled genomic environment,leading to possible genome instability and t chromosomal rearrangements(CRs).CRs include various types such as loss,duplication,inversion,and translocation of chromosomal segments.These mutations can affect the stability and function of genome and may have significant phenotypic consequences.Ample studies have confirmed that chromosomal translocations(one of main type of CR)are a major type of genetic variation in eukaryotes,which is relevant to adaptative evolution.Especially,due to the buffering effect of duplicated genomes,chromosomal translocations can be more readily tolerated in polyploids allowing their longer-term retention and hence potential spreading/fixation within a lineage.However,the direct functional consequences of chromosomal translocations in plant polyploids remain unexplored.Further research is needed to uncover the relationship between polyploidy and chromosomal translocations,as well as how chromosomal translocations influence the fitness and evolution of polyploidy by regulating genome structure and expression.Common wheat(Triticum aestivum,2n = 6x = 42,genome BBAADD)originated in the Fertile Crescent of the Middle East,and then rapidly spreaded to Europe became the third largest food crop in the world.Common wheat is also a textbook example of speciation of allopolyploidization.The process of common wheat formation encompasses two allopolyploidization events,i.e.,allotetraploidization and allohexaploidization.Several translocations are associated with the two allopolyploidization events.Moreover,there are frequent translocation in cultivated hexaploid wheat cultivars,suggesting this type of genetic variants is probably related to adaptation to different geographical environments and contributes to intraspecific diversity.Nonetheless,the direct effects of translocation on gene expression and further downstream has not been thoroughly explored.In this study,a synthetic allohexaploid wheat(named AT5)mimic natural hexaploid common wheat(Triticum aestivum)was produced and used as the study material.AT5 was formed by hybridization and subsequently colchicine-induced whole genome doubling(WGD)between Triticum turgidum ssp.durum(2n = 28,genome BBAA,accession TTR04,♀)and Aegilops tauschii(2n = 14,genome DD,accession TQ27,♂).During our analysis of transgenerational chromosomal stability in selfed progenies of AT5 by FISH and GISH karyotyping,we identified a heterozygous individual in which the terminal parts of the longarms of chromosomes 2D(ca.193 Mb)and 4A(ca.167 Mb)were reciprocally translocated.According to Mendelian segregation,the selfed progenies of this heterozygous translocation plant would generate nine possible genotypes,including reverted euploidy,unbalanced translocation(involking copy number change of the translocated chromosome segments),and balanced translocation(translocation with no copy number change in the translocated chromosome segments).After further propogation of these translocation plants via selfing,we selected five representative translocation lines(including unbalanced translocation lines and balanced translocation lines)that had sufficient seeds,and used their sibling reverted euploidy as a control to investigate the impacts of chromosomal translocation on phenotype,genome-wide gene expression and metabolome.We found(1)chromosomal translocations had a significant effect on gamete fitness,in particular,the long arm terminal of chromosome 4A is critical for early postzygotic development in the synthetic hexaploid wheat;(2)the chromosomal translocation showed obvious phenotypic consequences,in particular,lines with balanced translocation and stable inheritance(homozygous)showed positive phenotypic changes relative to the reverted euploid;(3)compared with the sibling reverted euploid control,both unbalanced and balanced translocations induced substantial changes in gene expression mainly through trans-regulation in the newly synthesized allohexaploid whea;and(4)the chromosomal translocation showed obvious metabolic consequences,leading to purtabation of many primary and secondary metabolites,especially the flavonoid metabolism pathway and the phenylpropanoid pathway.To sum up,this study has elucidated the immediate phenotype,gene expression,and metabolome responses of CRs in the form of chromosomal translocations in a synthetic allohexaploid wheat.Our results underscore the profound impact of CRs on gene expression in nascent allopolyploids with phenotypic and metabolic consequences that are likely relevant to polyploid evolution and crop breeding.