The Rosa genome provides new insights into the domestication of modern roses

Abstract

Roses have high cultural and economic importance as ornamental plants and in the perfume industry. We report the rose whole-genome sequencing and assembly and resequencing of major genotypes that contributed to rose domestication. We generated a homozygous genotype from a heterozygous diploid modern rose progenitor, Rosa chinensis 'Old Blush'. Using single-molecule real-time sequencing and a meta-assembly approach, we obtained one of the most comprehensive plant genomes to date. Diversity analyses highlighted the mosaic origin of 'La France', one of the first hybrids combining the growth vigor of European species and the recurrent blooming of Chinese species. Genomic segments of Chinese ancestry identified new candidate genes for recurrent blooming. Reconstructing regulatory and secondary metabolism pathways allowed us to propose a model of interconnected regulation of scent and flower color. This genome provides a foundation for understanding the mechanisms governing rose traits and should accelerate improvement in roses, Rosaceae and ornamentals.

Figure 1. Chromosome level assembly correlation with genetic map and Hi-C data.

a, Rosa chinensis ‘Old Blush’ mature flowers. b, Representation of chromosome connections between the physical positions on the reconstructed chromosome and genetic map positions (left panel). Scatter plot with dots representing the physical position on the chromosome (x-axis) versus the map position (y-axis). Rho (ρ) is the Pearson correlation coefficient (middle panel). Hi-C intra-chromosomal contact map for each chromosome (right panel). The intensity of pixels represents the count of Hi-C links between 400kb windows on chromosomes on a logarithmic scale. Darker red color indicates higher contact probability

Figure 2. Structure of diversity in resequenced genotypes highlights the origin of modern rose cultivars.

a, Genealogy of resequenced genotypes. Sections : CIN = Cinnamoneae ; SYN = Synstylae ; CHI = Chinenses. Genotypes : PEN, R. pendulina ; RUG, R. rugosa ; MAJ, R. majalis ; ARV, R. arvensis ; MOS, R. moschata ; WIC, R. wichurana ; SPO, R. chinensis ‘Spontanea’ ; GIG, R. gigantea ; MUT, R. chinensis ‘Mutabilis’ ; SAN, R. chinensis ‘Sanguinea’ ; GAL, R. gallica ; DAM, R. damascena ; OB, Rosa chinensis ‘Old Blush’ ; HUM, R. chinensis ‘Hume’s Blush’ ; FRA, R. x hybrida ‘La France’ (flower photo). b, Genetic structure and variant density. 1, circular representation of pseudomolecules. 2, schematic representation of the contribution of Cinnamonea, Synstylae and Chinenses sections to ‘La France’ in 35 chromosomal segments: light red = CHI, light green = SYN, light blue = CIN, multiple bands: mixed origin in the fragment. 3-8, density in heterozygote and homozygote variants (light and dark shades respectively) in 1 Mb sliding windows in ‘La France’, R. gigantea, ‘Hume’s Blush’, ‘Mutabilis’, ‘Sanguinea’, and ‘Old Blush’ heterozygote genotype respectively. c, Principal component analyses of genetic variation in three illustrative genomic segments. ‘La France’, orange dot; CIN, SYN and CHI in blue, green and red respectively; other cultivars in black. y-axis, 1^st component. x-axis, 2^nd component. The number indicated in each plot refers to the genomic fragments analyzed (e.g. 4.3 is the third segment of chromosome 4, Supplementary Fig. 6).

Figure 3. Inter-regulatory connections between color biosynthesis and some scent pathways.

a, Schematic representation of the rose chromosomes together with the position of candidate genes for anthocyanin pigments and volatile molecules biosynthesis and for flowering. Chromosome segments 2.4, 3.2-3.6 and 5.1 originating only from R. chinensis are indicated in light red. Anthocyanin synthesis genes are indicated in red; terpene biosynthesis genes in blue; flowering time genes in black; and development genes in green. b, Schematic representation of interconnections between color (pink background) and scent (blue background) pathways. Gene expression data show the anti-correlation between miR156 and SPL9 genes during petal development. RT-qPCR was performed on petals harvested at three successive stages: Non-colored petals early during development (St1); Petals at onset of anthocyanin synthesis (St2); Fully colored petals (St3). Black arrows: biosynthetic steps reported in the rose. Red arrows: biosynthetic steps reported in other species, but not in the rose. Green arrows: putative steps with unknown enzymes. Dashed black arrow: Several enzymatic steps. Maroon arrows: Gene regulation reported in A. thaliana, but not in the rose. Dashed maroon arrow: putative gene regulations. IPP: isopentenyl diphosphate, DMAPP: dimethylallyl diphosphate, DFR: dihydroflavonol-4-reductase, ANS: anthocyanidin synthase, 3GT: anthocyanidin 3-O-glucosyltransferase, GT1: anthocyanidin 3,5-diglucosyltransferase, GPPS: geranyl diphosphate synthase, FPPS: farnesyl diphosphate synthase, GGPPS: geranylgeranyl diphosphate synthase, GDS: germacrene D synthase, TPS: terpene synthase, NES: linalool/nerolidol synthase, CCD1/4 : carotenoid cleavage dioxygenases 1/4, NUDX1: nudix hydrolase1.