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

Abstract

Roses have a specific symbolic charge in Western cultural heritage, often used as a metaphor for love and romance. Despite its ancient cultivation, the passion for the phenotypic diversity of roses is relatively recent, dating back to the early 19th century. During that century, the number of rose varieties has increased exponentially from roughly 100 to 8,000, in such a way that this period can be considered as the golden age for rose breeding. To retrace the history of rose breeding in Europe and shed new light on genetic changes during this period, we collected large phenotypic and genetic data from 204 accessions, including botanical roses and varieties bred between 1800 and 1910. We also used whole-genome sequences from 32 accessions as an extra resource. The genetic makeup of roses is remarkably consistent with a temporal shift from a historical European to a near-Asian genetic background within a few generations. Our analyses are consistent with a substantial erosion of the genetic diversity during this period, both because of the greater contribution of the Asian genepool - a less genetically diverse group - and of specific genomic footprints of selection, in particular regarding the extension of the blooming period. Thanks to this study, we have generated the largest GWAS catalog for roses to date, which can be used as a tool for future rose breeding programs. We particularly discuss the crucial importance of preserving ancient rose collections to safeguard genetic diversity and ensure a sustainable breeding for the long-term.