Mitogenomic variation across cultivated and wild beet (Beta vulgaris L.) accessions reveals patterns associated with cytoplasmic male sterility

Background Beet hybrid production depends on cytoplasmic male sterility (CMS), which is determined by the mitochondrial genome. Systematically comparing mitochondrial genome structure, evolutionary dynamics, and inter-organellar DNA transfer across cultivated beet types and their wild progenitor, is key to understanding the evolutionary basis of CMS-associated features. Results We assembled complete mitochondrial genomes for 19 beet accessions, including four cultivated types (sugar, table, fodder, leaf) and one wild beet. Genome sizes ranged from 344 to 381 kb, with wild beet having the largest genome size and highest repeat content. All accessions shared 53 conserved core genes. The CMS‑specific sequence preSatp6 was present only in sterile lines and absent in wild beet. CMS lines exhibited accelerated evolutionary rates (both synonymous and non‑synonymous substitutions), whereas wild beet showed the lowest rates. We identified 809 plastid‑to‑mitochondrion transfers (PTMTs) and abundant nuclear organellar insertions (NUMTs/NUPTs); both wild beet and CMS lines accumulated more NUMTs compared to other cultivated types. Phylogenetic analysis placed wild beet at the basal position, supporting its ancestral position, and eight accessions (including four CMS lines and four non‑CMS sugar beet accessions) formed a tight, highly supported clade, with preSatp6 present exclusively in the CMS lines. Conclusions Beet mitochondrial genomes combine functional conservation with structural dynamism. Wild beet represents an ancestral state with a larger, repeat-rich genome and slow evolution, while CMS lines show distinctive structural configurations, accelerated evolution, and active cytonuclear interaction. This study provides a genomic framework for understanding CMS evolution and guiding for future breeding.