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.

Organellar genomes of the four-toothed moss, Tetraphis pellucida

“…In liverworts, both Haplomitrium [38] and Treubia [27] retain a functional mitochondrial nad7 gene, while all other species investigated have pseudogenised copies, varying greatly in their degrees of degeneration but remarkable for having persisted throughout the long evolutionary history of the group [38]. This is consistent with current hypotheses of Haplomitrium and Treubia forming the sister clade (Haplomitriopsida) to the rest of the liverworts (Marchantiopsida and Jungermanniopsida, e.g.…”

Characterization and Phylogenetic Analysis of Chloroplast and Mitochondria Genomes from the Antarctic Polytrichaceae Species Polytrichum juniperinum and Polytrichum strictum

“…The plastid genomes of the closest Polytrichum species have a GC percentage of 28% to 33% [21,22] and those of seed plants range between 34% and 40% [50]. Cai et al, observed high G + C contents in the chloroplast coding regions, and certain regions had higher percentages than others, such as the IR region with its four genes with high levels of G and C [51]. Thus, the distribution of GC content in the chloroplast is unequal, and, perhaps, the higher content presented by the Polytrichaceae species refers to the significant number of coding regions scaffolded.…”

Plant Mitochondrial Genome Evolution and Cytoplasmic Male Sterility

“…Flowering plant mitogenomes exemplify the former, with substantial variation in genome size and structure even among close relatives (Francis and Fernand, 1977;Alverson et al, 2010;Tang et al, 2015;Chen et al, 2017). They have highly variable intergenetic regions containing diverse repeated sequences (Kitazaki and Kubo, 2010), frequent structural rearrangements (Galtier, 2011), massive genes loss, frequent endogenous and foreign DNA transfer (Bergthorsson et al, 2003;Kubo and Newton, 2008;Hao and Palmer, 2009;Bock, 2010;Liu et al, 2011), and a highly variable RNA editing process (Takenaka et al, 2008). Conversely, plant mitochondrial genes display exceptionally low rates of nucleotide substitution (Wolfe et al, 1987;Palmer et al, 2000;Mower et al, 2007;Galtier, 2011).…”