Comparative analysis of the organelle genomes of seven Rosa species (Rosaceae): insights into structural variation and phylogenetic position

Rongxiang Zhang¹Shuwen Liu¹Ying Liu²Pei Wei²Xiang Niyan³Yuemei Zhao¹Xiaoman Gao⁴Yebing Yin⁴Lijun Qin⁵Tao Yuan^2*

• ¹Guizhou Education University, Guiyang, Guizhou Province, China
• ²Wuhan University, Wuhan, Hubei Province, China
• ³Hubei University, Wuhan, Hubei Province, China
• ⁴Tibet University, Lhasa, Tibet, China
• ⁵Guizhou University, Guiyang, Guizhou Province, China

In this study, we analysed the organelle genome assemblies of species within the genus Rosa, focusing on genome structure, gene transfer events, and phylogenetic relationships. Our findings indicate that the plastome structure in Rosa species is highly conserved with a lower Ka/Ks value, while the mitogenome displays a more complex structure with a higher Ka/Ks value. Inconsistencies between phylogenetic trees constructed from plastid and mitogenomic data may be due to frequent polynucleotide substitutions caused by microreversals misrepresenting phylogenetic trouble. Notably, the majority of PCGs in both organelles have a Ka/Ks ratio below 1, suggesting these genes in Rosa species underwent strong negative selection during evolution. Nucleotide polymorphism analysis identified four variable regions in the Rosa plastome: rps19, ndhF, ycf1, and psbM-trnD-GUC, which could serve as molecular markers for future species identification and studies on genetic diversity. The collinearity among mitogenomes across species reveals extensive structural rearrangements, disrupting the original gene order, although some gene sequences remain conserved in clusters. Through homology analysis between organelles, we discovered widespread gene transfer among Rosa species, including mitochondrial plastid (MTPT) DNAs such as rrn16 and rpl23. These two transfer events are a widespread phenomenon in Rosa spp. dating back to ca. 4.46 million years ago (Mya). Divergence time estimates suggest that the rapid differentiation of Rosa species occurred approximately 4.46 Mya, likely due to the uplift events in the Qinghai-Tibet Plateau during the late Miocene. Our study provides insights into the evolutionary processes of organelles in Rosa species and lays the groundwork for further research on the structural and functional genetic mechanisms of their plastomes and mitogenomes.