Zhang, F.; Gao, L.-Z.

Plant mitochondrial genomes are evolutionary paradoxes, structurally fluid yet functionally conserved. In hybridization-prone lineages like Camellia (Theaceae), where polyploidy and introgression blur species boundaries, mitochondrial dynamics remain unexplored. Here, we assemble mitochondrial genomes of eight Camellia species and Actinidia eriantha as outgroup, revealing three hallmarks of reticulate evolution: first, genome inflation (788,876 bp-1,000,198 bp) driven by short repeats (<100 bp; ~92.6-94.9% of total repeats, PGLS: R2=0.9729, P=6.293*10-6), overturning the long-repeat paradigm in plants; second, multichromosomal architectures in C. sinensis var. sinensis LJ43 and C. taliensis, with lineage-specific plastid DNA occupying up to 25.5% of mitochondrial content; and third, phylogenomic conflicts between mitochondrial, chloroplast, and nuclear gene trees, revealing genome-wide hybridization signatures. Mitochondrial genomes emerge as recorders of historical gene flow, capturing repeat explosions triggered by pervasive hybridization and cytonuclear co-evolution. By linking micro-repeat dominance to genomic shock, this work redefines mechanisms of plant mitochondrial evolution and provides a roadmap to resolve taxonomic complexities in rapidly radiating angiosperms.