The mitochondrial genome of Phoebe Bournei highlighted the structure variation driven evolution in magnoliids

Plant mitochondrial genomes exist and function in a special way, this third-kind genetic material is essential for plant growth and development. However, its complex and highly variable genome structure leads to a poor understanding compared with chloroplasts. Especially Phoebe bournei (Magnoliaceae), an indigenous species of China, showcases a profusion of metabolites and excellent wood properties with long growth cycle to maturity.

With the help of HiFi sequencing, we obtained new insights of their structure and variations. We initially curated the complete reference mitochondrial genome for P. bournei, a 775 Kb two-circle merged main physical map. These unequal circles exhibited a simplification trend through one long lateral repeat region, with a whole GC content of 47.09%. Conserved 43 protein coding genes were annotated and evenly distributed in the two genome rings. COX-3-ATP8-CYTB gene synteny events were found in P. bournei and M. biondii, others in Lauraceae were randomly shuffled by recombinant fragment due to rapid reorganization. Aberrant selective pressure occurred for ccmB, Ka/Ks more than 1 in Magnoliids and around 2.5 in representative angiosperms. Mitogenome genes bore a greater burden of pressure compared to genes in those of chloroplasts. Comparisons of consistent sequences revealed significant large-scale and inclined rearrangements within both cytoplasmic and nuclear genomes. Furthermore, the identification of lateral transfers from chloroplast to mitochondrial genome highlighted the consistent capture of functional genes such as petN. Besides, transferred sequences displayed chromosomal preference in nuclear genome.

Based on the first report of a simple multi-circular conformation of the P. bournei mitogenome, our results may provide a primary foundation for the evolution of Magnoliids and further application in the tree breeding.