Mitochondrial genomes of the early land plant lineage liverworts (Marchantiophyta): conserved genome structure, and ongoing low frequency recombination

Abstract

Background: In contrast to the highly labile mitochondrial (mt) genomes of vascular plants, the architecture and composition of mt genomes within the main lineages of bryophytes appear stable and invariant. The available mt genomes of 18 liverwort accessions representing nine genera and five orders are syntenous except for Gymnomitrion concinnatum whose genome is characterized by two rearrangements. Here, we expanded the number of assembled liverwort mt genomes to 47, broadening the sampling to 31 genera and 10 orders spanning much of the phylogenetic breadth of liverworts to further test whether the evolution of the liverwort mitogenome is overall static.

Results: Liverwort mt genomes range in size from 147 Kb in Jungermanniales (clade B) to 185 Kb in Marchantiopsida, mainly due to the size variation of intergenic spacers and number of introns. All newly assembled liverwort mt genomes hold a conserved set of genes, but vary considerably in their intron content. The loss of introns in liverwort mt genomes might be explained by localized retroprocessing events. Liverwort mt genomes are strictly syntenous in genome structure with no structural variant detected in our newly assembled mt genomes. However, by screening the paired-end reads, we do find rare cases of recombination, which means multiple concurrent genome structures may exist in the vegetative tissues of liverworts. Our phylogenetic analyses of the nuclear encoded double stand break repair protein families revealed liverwort-specific subfamilies expansions.

Conclusions: The low repeat recombination level, selection, along with the intensified nuclear surveillance, might together shape the structural evolution of liverwort mt genomes.

Keywords: Bryophytes; introns; recombination; repeats; structural evolution.

Fig. 1

Comparison of mt genome size, intergenic, intronic, and exonic contents among (a) liverwort genera, and (b) land plant major lineages. The order of liverworts and land plants in (a) and (b) are sorted by the phylogeny in Fig. 3. Major liverwort clades, HAP (Haplomitriopsida), MAR (Marchantiopsida), PEL (Pelliidae), MET (Metzgeriidae), POR (Porellales), JUNA (Jungermanniales clade A), JUNB (Jungermanniales clade B), JUNC (Jungermanniales clade C), are indicated in (a). The number of taxa analyzed for each group is indicated in the bracket following each group’s name in (b)

Fig. 2

Intron content of liverwort mitochondrial genomes. The species are ordered as in the phylogeny in Fig. 3. The black circle indicates the presence of an intron; the white square the absence of an intron. Intron nomenclature follows Dombrovska and Qiu (2004) and Knoop (2004). The number of species analyzed for each genus is indicated in the bracket following each genus’s name. The numbers at the bottom of each column indicate the total intron number

Fig. 3

Heat map of mt genome rearrangements in pairwise comparisons of land plants along a phylogenetic tree based on mt nucleotide sequences (Additional file 3: Figure S1). All nodes are maximally supported (i.e., 100% bootstrap support) unless otherwise marked