Pan-mitogenome in Dipterocarpoideae: mitochondrial plastid DNAs and repeats shape the dynamic evolution of mitogenomes.

BACKGROUND: Plant mitochondrial genomes (mitogenomes), essential for cellular energy production and development, are characterized by rapid structural variations and highly diverse non-coding sequences. However, the underlying causes of these variations remain controversial. Dipterocarpaceae, a tropical tree family of ~ 16 genera and 500-700 species, includes many ecologically and economically important taxa. Its largest lineage, Dipterocarpoideae (13 genera, 470-650 species), with a well-resolved evolutionary history, serves as an ideal model for investigating mitogenome evolution. RESULTS: Here, we assembled 13 new mitogenomes from the five most species-rich Dipterocarpoideae genera and conducted comprehensive pan-mitogenome analyses. These mitogenomes ranged from 378.3 to 442.8 kb in size and shared 64 conserved core fragments encoding 30 protein-coding genes (PCGs), three unique rRNA genes, and nine unique tRNA genes. Phylogenetic analyses based on organellar and nuclear genomes consistently recovered three major clades: Vatica, Dipterocarpus, and a clade comprising Shorea, Hopea, and Parashorea. The Vatica mitogenomes contained fewer mitochondrial plastid DNAs (MTPTs) and repeats, resulting in a simpler mitogenome structure. In contrast, the other clades contain more MTPTs and repeats, leading to a more complex mitogenome. This pattern suggests that MTPTs and repeats may jointly contribute to increased mitogenome complexity. Moreover, the synonymous substitution rate in coding regions was comparable to that in non-coding regions, while the non-synonymous substitution rate was lower, indicating similar mutation inputs but different selective pressures. CONCLUSION: These findings provide new insights into the structural complexity and evolutionary dynamics of plant mitogenomes.