Haplotype-resolved genome assembly of Rosa laevigata reveals molecular mechanisms of secondary metabolite synthesis and adaptation evolution

Abstract

Rosa laevigata is a valuable edible plant and traditional herbal medicine in China, renowned for its potent antioxidant and anti-inflammatory properties, as well as its therapeutic efficacy in treating urinary system disorders. Its remarkable adaptability to karst environments and high resistance to aphids further position it as an exceptional rose germplasm resource and a promising candidate for rocky desertification management in karst regions. However, the absence of a high-quality genome has limited a comprehensive understanding of its medicinal compound biosynthesis and environmental adaptation mechanisms. In this study, we successfully assembled two haplotype genomes of R. laevigata, the size of the two haplotype genomes were 493 Mb and 479 Mb, and the N50 was 49.5 Mb and 64.9 Mb, respectively. 43480 and 41251 protein-coding genes were annotated, respectively, with BUSCO assessments of 98.6 and 98.7. Comparative genomic analyses revealed recent proximal and tandem duplication events, which contributed to the expansion of gene families associated with terpenoid biosynthesis, anthocyanin biosynthesis, and glutathione metabolism. These expansions may have led to the population expansion of golden cherry since the Pleistocene as well as the adaptation to high radiation karst environments. We identified 249 positively selected genes, primarily enriched in metabolic pathways such as vitamin B6 metabolism, glutathione metabolism, and ascorbate and aldarate metabolism. Meanwhile, the gene families associated ascorbate and aldolate metabolism were significantly amplified. Additionally, we identified four calcium regulation-related genes (MHX, NCL, CBL8, and PAO) positively selected in early karst-distributed species. Protein-protein interaction analysis revealed direct and indirect interactions between MHX and proteins such as NCL, CCX, CAX, and MRS, The CBL8 proteins of R. laevigata have a higher calyx Ca^2 + binding capacity compared to those of Arabidopsis thaliana. This suggesting their potential roles in the adaptation of karst-distributed species to high-calcium environments. In summary, this study provides profound insights into the genomic evolution, metabolite biosynthesis, and environmental adaptation mechanisms of R. laevigata. It also establishes a robust foundation for future functional genomic research, including germplasm conservation and breeding studies.