Dark side of the honeymoon: reconstructing the Asian × European rose breeding history through the lens of genomics.

Roses hold significant symbolic value in Western cultural heritage, often serving as a symbol of love and romance. Despite their ancient cultivation, the appreciation for the phenotypic diversity of roses emerged relatively recently, notably during the 19th century. This period is characterized by a remarkable expansion in the number of varieties, from around 100 to over 8,000, representing a golden age for roses. To trace the history of rose breeding in Europe and unveil genetic changes during this period, we gathered phenotypic and genetic data from 204 accessions. These included botanical roses and varieties cultivated between 1,800 and 1,910. Whole-genome sequences from 32 accessions were also included. Our analysis revealed a temporal shift in the genetic makeup, transitioning from a historical European to a near-Asian genetic background within a few generations. This shift was accompanied by a notable reduction in genetic diversity, attributed to the backcrossing with the less diverse Asian genepool, plus some genomic signatures of selection. We have generated the largest GWAS catalog for rose to date, offering a valuable resource for future breeding initiatives. We emphasize the critical importance of preserving ancient rose collections to safeguard diversity and ensure a sustainable breeding for the long-term.