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Recent advances in high-throughput sequencing have enabled detailed characterization of plant mitochondrial genomes. Here, we assembled and analyzed the mitochondrial genome of Quercus chenii Nakai, a key oak species in Fagaceae, using Illumina NovaSeq6000. The genome consists of a 364,958 bp linear and a 53,677 bp circular chromosome, totaling 418,635 bp with a GC content of 45.6%. Repeat-rich regions (210–250 and 300–340 kb) may facilitate structural rearrangements, while extensive RNA editing-particularly in nad4 and ccmF -likely enhances protein functionality and mitochondrial adaptability. Comparative collinearity analysis showed high structural conservation with Q. acutissima Carruth. (90.92%) but marked divergence from Fagus sylvatica L. (35.80%), suggesting lineage-specific rearrangements. Phylogenetic analysis based on the mitochondrial genome supports the same placement of Q. chenii within Fagaceae as that derived from the chloroplast genome. The Ka/Ks analysis across Fagaceae mitochondrial genomes revealed strong conservation of core genes, with adaptive variations in energy metabolism-related genes, suggesting functional divergence linked to metabolic optimization under environmental stress. These findings highlight the distinct evolutionary strategies of mitochondrial and chloroplast genomes: the former optimizing energy production, while the latter fine-tunes photosynthesis and stress responses. Comparison analysis with the chloroplast genome further revealed both conserved ( psbT and psbC ) and divergent ( ndhD and ndhF ) genes, implying potential historical gene transfer events. Together, these findings highlight the dynamic yet conserved nature of the Q . chenii mitochondrial genome and provide new insights into organellar genome evolution, structural plasticity, and adaptive mechanisms within the Fagaceae family.

Shared ancestral polymorphism and introgression are two main causes of chloroplast DNA (cpDNA) haplotype sharing among closely related angiosperms. In this study, we explored the roles of these two processes in shaping the phylogeographic patterns of East Asian Cerris oaks by examining the geographic distributions of randomly and locally distributed shared haplotypes, which coincide with the expectations of shared ancestry and introgression, respectively. We sequenced 1340 bp of non‐coding cpDNA from Quercus acutissima (n = 418) and Q. chenii (n = 183) and compiled previously published sequence data of Q. variabilis (n = 439). The phylogenetic relationships among haplotypes were examined using a median‐joining network. The geographic patterns of interspecifically shared haplotypes were assessed to test whether nearby populations have a higher degree of interspecific cpDNA sharing than distant ones. We identified a total of 27 haplotypes that were grouped into three non‐species‐specific lineages with overlapping distributions. Ancestral haplotypes were extensively shared and randomly distributed across populations of the three species. Some young haplotypes were locally shared in mountainous areas that may have been shared refugia. The local exchange of cpDNA resulted in an excess of similar haplotypes between nearby populations. Our study demonstrated that the haplotype sharing pattern among East Asian Cerris oaks reflected the imprints of both shared ancestral polymorphism and introgression. This pattern was also associated with the relatively stable climates and complex landscapes in East Asia, which not only allowed the long‐term persistence of ancestral lineages but also connected the survived populations across refugia. We demonstrated that the haplotype sharing pattern among East Asian Cerris oaks reflected the imprints of both shared ancestral polymorphism and introgression. This pattern was also associated with the relatively stable climates and complex landscapes in East Asia, which not only allowed the long‐term persistence of ancestral lineages but also connected the survived populations across refugia.

Major topographic features facilitate intraspecific divergence through geographic isolation. This process may be enhanced by environmental isolation along climatic gradients, but also may be reduced by range shifts under rapid climatic changes. In this study, we examined how topography and climate have interacted over time and space to influence the genetic structure and evolutionary history of Quercus chenii , a deciduous oak species representative of the East China flora. Based on the nuclear microsatellite variation at 14 loci, we identified multiple genetic boundaries that were well associated with persistent landscape barriers of East China. Redundancy analysis indicated that both geography and climate explained similar amounts of intraspecific variation. Ecological differences along altitudinal gradients may have driven the divergence between highlands and lowlands. However, range expansions during the Last Interglacial as inferred from approximate Bayesian computation (ABC) may have increased the genetic diversity and eliminated the differentiation of lowland populations via admixture. Chloroplast (cp) DNA analysis of four intergenic spacers (2,866 bp in length) identified a total of 18 haplotypes, 15 of which were private to a single population, probably a result of long-term isolation among multiple montane habitats. A time-calibrated phylogeny suggested that palaeoclimatic changes of the Miocene underlay the lineage divergence of three major clades. In combination with ecological niche modeling (ENM), we concluded that mountainous areas with higher climatic stability are more likely to be glacial refugia that preserved higher phylogenetic diversity, while plains and basins may have acted as dispersal corridors for the post-glacial south-to-north migration. Our findings provide compelling evidence that both topography and climate have shaped the pattern of genetic variation of Q. chenii . Mountains as barriers facilitated differentiation through both geographic and environmental isolation, whereas lowlands as corridors increased the population connectivity especially when the species experienced range expansions.