Genome fractionation and loss of heterozygosity in hybrids and polyploids: mechanisms, consequences for selection, and link to gene function

Abstract

Hybridization and genome duplication may cause serious damages but may also open unique opportunities to invade new ecological niches or adapt to novel environments better than their parents. Following the initial merging or multiplications, the subgenomes of hybrids and polyploids undergo considerable changes, often eliminating segments of one parental genome, phenomena known as loss of heterozygosity (LOH) and genome fractionation. Mechanisms causing such changes are not well understood, and remain enigmatic particularly when hybridization is linked with asexual (clonal) reproduction that may enforce diverse array of genome evolutionary pathways ranging from long-term stasis to dynamic reformations. Analysis of genome evolution in diploid and polyploid clonal hybrids between fish Cobitis elongatoides and either C. taenia or C. tanaitica species revealed that clonal genomes remain generally static on chromosome-scale level but undergo small-scale restructurations resulting in genome fractionation and LOH events. These events have complex molecular background in two distinct processes, the hemizygous deletions and conversions between orthologous subgenomes. The impact of both processes on clonal evolution is ploidy-dependent; while deletions frequently accumulated in polyploids, they appeared to be selected against in diploid asexuals where gene conversions prevailed. The incidence of genomic restructuration was not random with respect to individual genes, but it preferentially affected loci with unusually high transcription levels, genes under relatively strong purifying selection and also genes with particular functions, such as those related to endoplasmatic reticulum. Likelihood that given orholog would be retained or lost correlated significantly with its parental origin, GC content (preferential loss of low-GC alleles) and expression (less expressed alleles tended to be replaced by more expressed ones). Contrary to expectations, however, we observed that the preferentially retained subgenome (the one derived from C. elongatoides) was not dominant at the transcription level as all hybrids were phenotypically more similar to the other parent whose genes were preferentially lost. Our data show that the fate of subgenomes in asexual hybrids and polyploids depends on complex interplay of molecular mechanisms and selection that are affected by sequence composition, expression as well as parental ancestry.

Brettanomyces bruxellensis: Overview of the genetic and phenotypic diversity of an anthropized yeast

“…LOH events are a source of genomic rearrangements and can contribute to the rapid onset of phenotypic diversity (Dutta, Dutreux, & Schacherer, 2021;Sampaio et al, 2020;Smukowski Heil et al, 2017). LOH has gained attention for its frequent association with fitness, adaptation, polyploid stabilization, or even pathogenesis in yeasts but also in other organisms such as the oomycete Phytophthora capsica, hybrids of the cultivated rice Oryza or the Cobitis fish species (Beekman & Ene, 2020;Forche et al, 2011;Janko et al, 2021;Lamour et al, 2012;Morales & Dujon, 2012;Todd, Wikoff, Forche, & Selmecki, 2019 Wang, Li, & Chatterton, 1999). Compared to S. cerevisiae where LOH represents 50% of the genome, B. bruxellensis presents a low level of LOH, which is variable across subpopulations (Gounot et al, 2020;Peter et al, 2018).…”

An atlas of fish genome evolution reveals delayed rediploidization following the teleost whole-genome duplication

“…As a striking counter-example to the classical allopolyploid rediploidization model, asexual allotetraploid loaches present a bias in genes retention that is surprisingly in the opposite direction to the expression bias, i.e. the most expressed subgenome accumulated more gene losses (Janko et al 2021). Taken together, these results suggest that underappreciated factors may govern genes retention following genome duplication in vertebrates.…”