New mitochondrial genomes of leptosporangiate ferns allow modeling the mitogenomic inflation syndrome across all land plant lineages

Plants’ mitochondrial genomes (mitogenome) evolve in a hard-to-predict fashion. To reconstruct the evolutionary trajectories of land plant mitogenomes, we, here, filled the last major mitogenomic gap within land plants by assembling the mitogenomes of the leptosporangiate ferns Azolla filiculoides and Pteridium revolutum and, secondly, analyzed the mitogenomic evolutionary regime shifts across land plants. By testing various Ornstein-Uhlenbeck stabilizing selection models in an a priori-free analysis of five selected mitogenomic traits, we observed 71 evolutionary regime shifts across 218 land plant species. These shifts can lead to genomic convergence, in which certain traits such as size, GC content, and the proportion of non-coding DNA converge, or non-converging regimes, which are characterized by exceptional paths of genomic evolution such as extreme GC content or size. We also found that non-seed plants have a slightly, but significantly, higher rate of synonymous substitutions across all gene classes than seed plants, and that ferns differ significantly in the number of nonsynonymous and synonymous changes compared with other non-seed and seed plants. This pattern matches an outstandingly high rate of RNA editing in the small but repeat-rich mitogenomes of leptosporangiate ferns. In sum, our study highlights the considerable changes in mito-chromosomal architecture that occur during land plant evolution and suggests that these changes may be related to increases in error-prone repair mechanisms. Further study of underrepresented plant groups such as ferns and lycophytes is needed to understand the mechanisms and dominating forces behind the evolutionary dynamics and the mitogenomic inflation syndrome. Significance Statement Our study provides new insights into the complexity and diversity of land plant mitogenome evolution and reveals that they take many turns of molecular evolutionary directions across 218 land plant species. Our results have the potential to inform future research in this area and to advance our understanding of the mitogenomic inflation syndrome during plant evolution.