Comparative Analyses of the Organellar Genomes of Quercus Reveal Contrasting Evolutionary Dynamics

Background: Mitochondrial and chloroplast genomes in plants have experienced distinct evolutionary trajectories due to differences in genomic organization, functional constraints, and genome maintenance mechanisms. However, comparative studies of their evolutionary dynamics in oaks remain limited. Methods: The complete mitochondrial and chloroplast genomes of Quercus arbutifolia were assembled and annotated using PacBio HiFi reads. Genome structure, repetitive sequences, codon usage, and mitochondrial plastid DNA transfers (MTPTs) were characterized. Evolutionary genomic and phylogenetic analyses were conducted across selected Quercus species to assess structural variation, sequence divergence, and phylogenetic relationships. Results: The mitochondrial genome of Q. arbutifolia was assembled as a 493,735 bp linear molecule, whereas the chloroplast genome was assembled as a 160,682 bp circular molecule. The mitochondrial genome exhibited lower coding density and a higher abundance of repetitive sequences than the chloroplast genome. Both organellar genomes preferentially used A/U-ending codons, with codon usage variation associated with mutation bias and selective constraints. Thirty-two MTPT regions were identified, predominantly representing plastid-to-mitochondrial transfers. Chloroplast genomes showed conserved inverted repeat boundaries among Quercus species, whereas mitochondrial genomes displayed extensive structural rearrangements, indicating contrasting evolutionary dynamics between the two organellar genomes. Nucleotide diversity analyses further revealed different sequence variation between organellar genomes, with chloroplast protein-coding genes (PCGs) generally exhibiting higher sequence divergence than mitochondrial PCGs. Phylogenetic analyses recovered largely consistent relationships among major Quercus lineages, with several lineage-specific conflicts. Conclusions: Overall, the mitochondrial and chloroplast genomes of Q. arbutifolia exhibit contrasting patterns of genome structure and sequence evolution. Their largely congruent but partially conflicting phylogenetic signals provide complementary information for investigating organellar genome evolution and diversification in Quercus.