The mitochondrial genomes of the early land plants Treubia lacunosa and Anomodon rugelii: dynamic and conservative evolution

Abstract

Early land plant mitochondrial genomes captured important changes of mitochondrial genome evolution when plants colonized land. The chondromes of seed plants show several derived characteristics, e.g., large genome size variation, rapid intra-genomic rearrangement, abundant introns, and highly variable levels of RNA editing. On the other hand, the chondromes of charophytic algae are still largely ancestral in these aspects, resembling those of early eukaryotes. When the transition happened has been a long-standing question in studies of mitochondrial genome evolution. Here we report complete mitochondrial genome sequences from an early-diverging liverwort, Treubia lacunosa, and a late-evolving moss, Anomodon rugelii. The two genomes, 151,983 and 104,239 base pairs in size respectively, contain standard sets of protein coding genes for respiration and protein synthesis, as well as nearly full sets of rRNA and tRNA genes found in the chondromes of the liverworts Marchantia polymorpha and Pleurozia purpurea and the moss Physcomitrella patens. The gene orders of these two chondromes are identical to those of the other liverworts and moss. Their intron contents, with all cis-spliced group I or group II introns, are also similar to those in the previously sequenced liverwort and moss chondromes. These five chondromes plus the two from the hornworts Phaeoceros laevis and Megaceros aenigmaticus for the first time allowed comprehensive comparative analyses of structure and organization of mitochondrial genomes both within and across the three major lineages of bryophytes. These analyses led to the conclusion that the mitochondrial genome experienced dynamic evolution in genome size, gene content, intron acquisition, gene order, and RNA editing during the origins of land plants and their major clades. However, evolution of this organellar genome has remained rather conservative since the origin and initial radiation of early land plants, except within vascular plants.

Figure 1. The gene map of Treubia lacunosa mitochondrial genome.

Genes (exons indicated as closed boxes) shown on the outside of the circle are transcribed clockwise, whereas those on the inside are transcribed counter-clockwise. Genes with group I or II introns (open boxes) are labeled with asterisks. Pseudogenes are indicated with the prefix “ψ”.

Figure 2. The gene map of Anomodon rugelii mitochondrial genome.

Genes (exons indicated as closed boxes) shown on the outside of the circle are transcribed clockwise, whereas those on the inside are transcribed counter-clockwise. Genes with group I or II introns (open boxes) are labeled with asterisks. Pseudogenes are indicated with the prefix “ψ”.

Figure 3. Gene order comparison among mitochondrial genomes of Chara vulgaris, Treubia lacunosa, Marchantia polymorpha, Pleurozia purpurea, Physcomitrella patens, Anomodon rugelii, Phaeoceros laevis, and Megaceros aenigmaticus.

Species are arranged according to the organismal phylogeny , , , except that positions of the two hornworts are reversed as the Megaceros gene order more likely represents the ancestral condition according to a parsimony criterion (a supplementary figure (Fig. S1) is presented in which the two hornworts are placed in their correct organismal phylogeny positions). Solid lines connect orthologous genes between species with the same orientation, whereas dashed lines connect those with the reversed orientation. Repeat sequences are color-coded: in liverworts, RepA – black, RepB – green, RepB2 – purple, RepC – red, RepD – blue, and RepE – orange; in hornworts, RepA – red, RepB – blue (responsible for the inversion between Megaceros and Phaeoceros), RepC – green (this class of repeats was not annotated in either hornwort due to their length of <100 bp, inverted in Megaceros but direct in Phaeoceros), and RepD – purple.