Meiotic pairing irregularity and homoeologous chromosome compensation cause rapid karyotype variation in synthetic allotetraploid wheat

Abstract

Summary Allopolyploidization may initiate rapid evolution due to heritable karyotypic changes. The types and extents of these changes, the underlying causes, and their effects on phenotype remain to be fully understood. Here, we designed experimental populations suitable to address these issues using a synthetic allotetraploid wheat. We show that extensive variation in both chromosome number (NCV) and structure (SCV) accumulated in a selfed population of a synthetic allotetraploid wheat (genome SbSbDD). The combination of NCVs and SCVs generated massive organismal karyotypic heterogeneity. NCVs and SCVs were intrinsically correlated and highly variable across the seven sets of homoeologous chromosomes. Both NCVs and SCVs stemmed from meiotic pairing irregularity (presumably homoeologous pairing) but were also constrained by homoeologous chromosome compensation. We further show that homoeologous meiotic pairing was positively correlated with sequence synteny at the subtelomeric regions of both chromosome arms, but not with genic nucleotide similarity per se. Both NCVs and SCVs impacted phenotypic traits but only NCVs caused significant reduction in reproductive fitness. Our results implicate factors influencing meiotic homoeologous chromosome pairing and reveal the type and extent of karyotypic variation and its immediate phenotypic manifestation in synthetic allotetraploid wheat. This has relevance for our understanding of allopolyploid evolution.

Effects of Allopolyploidization and Homoeologous Chromosomal Segment Exchange on Homoeolog Expression in a Synthetic Allotetraploid Wheat under Variable Environmental Conditions

“…It is also difficult to distinguish de novo altered expression patterns from those inherited from parents (parental legacy), as the exact parents may have gone extinct or, at least, are difficult to determine. Furthermore, even less is understood about the immediate impacts of genome shock-induced secondary structural chromosomal changes on gene expression, which are superimposed on the effects of allopolyploidization, although they are known to occur frequently in newly formed allopolyploids due to meiosis instability [34][35][36]. This again is difficult to study using naturally formed allopolyploid species, as structural variants are known to affect recombination and hence mutational trajectories [37,38].…”

Little Evidence for Homoeologous Gene Conversion and Homoeologous Exchange Events inGossypiumAllopolyploids

“…Ultimately, both HE and hGC can act to homogenize sequences across otherwise divergent subgenomes, thereby complicating allopolyploid genome assembly and analyses. In turn, this sequence homogenization can generate heterogeneous phenotypes (as demonstrated in Brassica (12,13), Tragopogon (14,15), Oryza (16)(17)(18)) by altering allele dosage and other (epi)genomic patterns (19), acting to reshuffle genetic variation and potentially resulting in novel genomic combinations for selection to act upon. Although multiple methods have been implemented to identify regions of allopolyploid genomes that have experienced homoeologous exchanges (e.g.…”