Whole-genome sequencing of 1,060 Brettanomyces bruxellensis isolates reveals significant phenotypic impact of acquired subgenomes in allopolyploids

Genomic architecture changes can significantly influence genome evolution and phenotypic variation within a species. Polyploidization events are thought to be one of the important catalysts for adaptation, speciation and tumorigenesis. However, little is known about the overall impact of such events on the phenotypic landscape at a population level. Here, we completely sequenced and phenotyped a large population of 1060 Brettanomyces bruxellensis yeast isolates, punctuated by multiple independent polyploidization events, notably allopolyploidization, giving rise to a highly structured population related to various anthropized ecological niches. A subgenome-aware population analysis revealed differential genome evolution between the primary and acquired genomes, with the latter showing a higher degree of conservation between isolates. Distinct phenotypic signatures were identified across major populations, with allopolyploid isolates showing an enrichment of extreme phenotypes. Genome-wide association analysis consistently revealed the substantial influence of the acquired genome of allopolyploids, with associated variants exhibiting significantly larger effect sizes than those from the primary genome. Overall, our study illustrates the profound and species-wide impact of polyploidization events on genome evolution and phenotypic diversity. It also provides a useful resource to explore the impact of allopolyploidy on adaptation.