Complex and reticulate origin of edible roses (Rosa, Rosaceae) in China

Abstract

While roses are today among the most popular ornamental plants, the petals and fruits of some cultivars have flavored foods for millennia. The genetic origins of these edible cultivars remain poorly investigated. We collected the major varieties of edible roses available in China, assembled their plastome sequences, and phased the haplotypes for internal transcribed spacers (ITS1/ITS2) of the 18S-5.8S-26S nuclear ribosomal cistron. Our phylogenetic reconstruction using 88 plastid genomes, of primarily maternal origin, uncovered well-supported genetic relationships within Rosa, including all sections and all subgenera. We phased the ITS sequences to identify potential donor species ancestral to the development of known edible cultivars. The tri-parental Middle-Eastern origin of R. × damascena, the species most widely used in perfume products and food additives, was confirmed as a descendent of past hybridizations among R. moschata, R. gallica, and R. majalis/R. fedtschenkoana/R. davurica. In contrast, R. chinensis, R. rugosa, and R. gallica, in association with six other wild species, were the main donors for fifteen varieties of edible roses. The domesticated R. rugosa 'Plena' was shown to be a hybrid between R. rugosa and R. davurica, sharing a common origin with R. 'Fenghua'. Only R. 'Jinbian' and R. 'Crimson Glory' featured continuous flowering. All remaining cultivars of edible roses bloomed only once a year. Our study provides important resources for clarifying the origin of edible roses and suggests a future for breeding new cultivars with unique traits, such as continuous flowering.

Figure 1

A well-supported plastome phylogeny for roses. A maximum-likelihood (ML) tree was constructed to show the phylogenetic relationships of Rosa species and cultivars. The upper left panel shows the overall phylogenetic frame with branches for outgroups marked by gray lines. Edible roses were marked in blue, while branches with thickened lines showed bootstrap support at 100%. Numbers on branches represent supports between 50% – 99%. Clades, subclades, and lineages were marked as C1 to C4, C4–1 to C4–5, and C4–5a/b, respectively. Ploidy levels, taxonomic sections and subgenera information for species [1–3, 33] are included.

Figure 2

Phasing strategy for ITS haplotypes in R. × damascena L1. a. Variations in ITS1 with numbers in brackets indicating the clean read numbers per variable site. The frequency of each base per site is shown as a percentage. b. A schematic strategy for assembling the ITS haplotypes using Illumina reads. The variable sites corresponded to the positions in a. Gray lines represent raw reads mapped to the reference. Sequence variation at each variable site was given as A/T/C/G, while a “-” represented a deletion. c. The assembled ITS1 haplotypes with the proportion of coverage given as a percentage.

Figure 3

Phylogenetic clustering of ITS1 haplotypes. Bootstrap supports >50% are marked with numbers along each branch. Edible rose cultivars are labeled in blue. Alleles with identical sequences for edible roses in the same clades are marked with dashed rectangles. Their group numbers are given here as Roman numerals. a and b show the topologies for parts a and b in the left-hand panel, respectively.

Figure 4

Phylogenetic clustering for ITS2 haplotypes. Rectangle numbers are ordered according to cooccurrence with ITS1 haplotypes (Fig. 3).

Figure 5

Hypothetical origins of edible roses. Potential maternal or paternal progenitors are marked here with blue ♀ or orange ♂, respectively. Ploidy levels (2x to 4x), flowering patterns (OF, once flowering; CF, continuous flowering; OR, occasional reblooming; NF marks the four lines that did not flower at the KIB.), and leaf and flower morphology are on the right (the black bar on each leaf photo represents 2 cm).