A de novo-originated gene drives rose scent diversification.

Abstract

How evolution builds genes, how these genes attain enhanced expression, and how they integrate into existing regulatory networks to drive phenotypic diversification are all fascinating questions. Here, we generated chromosome-level genome assemblies for two Rosa banksiae subspecies and re-sequenced an additional 40 rose accessions. Genomic analysis of more than 100 Rosa accessions revealed multiple evolutionary steps leading to the de novo origination of a taxon-restricted gene, SCREP, specific to the rose lineage. Extensive transcriptomic, metabolomic, and functional analyses demonstrated that the recruitment of a Miniature Inverted-repeat Transposable Element (MITE) transposon into the gene promoter led to elevated expression, that the gene SCREP orchestrates eugenol biosynthesis, and that the evolutionary dynamics of SCREP account for variation in rose scent among different species and cultivars. Our results provide insights into the mechanism of de novo gene origination, the role of transposable elements in gene expression, and the evolutionary consequences of taxon-restricted genes in phenotypic diversification.