Unveiling the Patterns of Reticulated Evolutionary Processes with Phylogenomics: Hybridization and Polyploidy in the Genus Rosa

Abstract

Reticulation, caused by hybridization and allopolyploidization, is considered an important and frequent phenomenon in the evolution of numerous plant lineages. Although both processes represent important driving forces of evolution, they are mostly ignored in phylogenetic studies involving a large number of species. Indeed only a scattering of methods exists to recover a comprehensive reticulated evolutionary history for a broad taxon sampling. Among these methods, comparisons of topologies obtained from plastid markers with those from a few nuclear sequences are favored, even though they restrict in-depth studies of hybridization and polyploidization. The genus Rosa encompasses c. 150 species widely distributed throughout the northern hemisphere and represents a challenging taxonomic group in which hybridization and polyploidization are prominent. Our main objective was to develop a general framework that would take patterns of reticulation into account in the study of the phylogenetic relationships among Rosa species. Using amplicon sequencing we targeted allele variation in the nuclear genome as well as haploid sequences in the chloroplast genome. We successfully recovered robust plastid and nuclear phylogenies and performed in-depth tests for several scenarios of hybridization using a maximum pseudo-likelihood approach on taxon subsets. Our diploid-first approach followed by hybrid and polyploid grafting resolved most of the evolutionary relationships among Rosa subgenera, sections, and selected species. Based on these results, we provide new directions for a future revision of the infrageneric classification in Rosa. The stepwise strategy proposed here can be used to reconstruct the phylogenetic relationships of other challenging taxonomic groups with large numbers of hybrid and polyploid taxa.

Comparative analysis of the chloroplast genomes of Rosa species and RNA editing analysis

“…In this study, a phylogenetic tree based on chloroplast genome sequences was constructed to explore the evolutionary relationship in the genus Rosa and was found to be generally consistent with previously reported results [13,26,33]. There were several inconsistencies between the nuclear and chloroplast phylogenetic topology, particularly the position of section Rosa, which may be due to incomplete lineage, differences in the evolutionary rates of chloroplast and nuclear genes, or introgressive hybridization [33]. The earliest divergence in the chloroplast phylogeny roughly distinguished species of sections Pimpinellifoliae and Rosa and subgenera Hulthemia, Platyrhodon, and Hesperhodos from species of sections Synstyale, Laevigatae, Banksianae, Caninae, and Chinenses, which is consistent with previous studies [33,34] RNA editing of the Rosa chloroplast genome is one of the focal points of this study.…”

“…In this study, a phylogenetic tree based on chloroplast genome sequences was constructed to explore the evolutionary relationship in the genus Rosa and was found to be generally consistent with previously reported results [13,26,33]. There were several inconsistencies between the nuclear and chloroplast phylogenetic topology, particularly the position of section Rosa, which may be due to incomplete lineage, differences in the evolutionary rates of chloroplast and nuclear genes, or introgressive hybridization [33].…”

Power and Weakness of Repetition – Evaluating the Phylogenetic Signal From Repeatomes in the Family Rosaceae With Two Case Studies From Genera Prone to Polyploidy and Hybridization (Rosa and Fragaria)

“…Neither entire repeatome data nor 45S or 5S rDNA clusters reflected phylogenetic relationships within the genus Rosa. Plastid phylogenies supported the split of Rosa into two major clades: the Rosa and allies clade and the Synstylae and allies clade (Fougère-Danezan et al, 2015;Debray et al, 2019Debray et al, , 2021 with R. persica (subg. Hulthemia) as the most basal taxon, which was only separated from the remaining species in the PCoA and the neighbor net based on all clusters (Figures 7A,B).…”

“…Hulthemia : R. persica and subg. Hesperhodos : R. minutifolia ( Figure 1C ; Fougère-Danezan et al, 2015 ; Debray et al, 2021 ). Nested within the Synstylae and allies clade that appear to be members of sect.…”

Characteristics and phylogenetic analysis of the complete chloroplast genome of Rosa glomerata (Rosaceae)

“… 2015 ; Debray et al. 2022 ). Here, we characterized the complete chloroplast (cp) genome sequence of R .…”