Chloroplast phylogenomics of liverworts: a reappraisal of the backbone phylogeny of liverworts with emphasis on Ptilidiales

Abstract

As one of the four main lineages diverging from the early diversification of land plants, the phylogeny of liverworts holds the information about nearly 500 Myr of independent adaptation to changing environments. Thus, resolving the phylogenetic history of liverworts will provide unique insights into the successful diversification of early land plants in terrestrial ecosystems. However, the deep diverging events of this group remain incompletely resolved, such as the definite position of Ptilidiales. Here, we aimed to reconstruct the backbone relationships of liverworts using 84 protein‐coding chloroplast genes, a dataset comprising 35 representatives from all major lineages of liverworts, and three phylogenetic analyses, namely maximum parsimony, maximum likelihood and Bayesian inference. To test the impact of composition biases, the phylogenetic analyses were carried out using three alignments representing the same dataset either as: (i) nucleotides, (ii) amino acids, or (iii) recoded nucleotides applying ambiguity base code. Chloroplast genome data consistently supported the monophyletic origin of three major lineages in liverworts, as well as the majority of backbone relationships. Ptilidiales were found to be sister to Jungermanniales. The rapid accumulation of G/C tracks as a consequence of increased GC content is an important cause for the long branches inferred in this group. Our study not only provides empirical evidence to support the significance of plastid genome sequencing to reconstruct the phylogeny of this important plant lineage, but also suggests that the GC content has played a critical role in the evolutionary dynamics of plastid genomes in land plants.

The Increase of Simple Sequence Repeats during Diversification of Marchantiidae, An Early Land Plant Lineage, Leads to the First Known Expansion of Inverted Repeats in the Evolutionarily-Stable Structure of Liverwort Plastomes

“…The analysed dataset that was based on CDS and ribosomal genes delivered results that were mostly congruent with previous phylogenetic studies [12,19,20,29] and divided liverworts into five main lineages: Haplomitriidae, represented here by Haplomitrium blumei, which served as an outgroup, early divergent complex thalloids, followed by two lineages of simple thalloid and leafy liverworts (Figure 3) Genes 2020, 11, x FOR PEER REVIEW 5 of 14 organellar genomes this correlation was only found in the plastomes of Geraniaceae [25]. The plastome of C. conicum possesses a typical structure, despite the presence of longer TA repeats.…”

Sequencing of Organellar Genomes of Nowellia curvifolia (Cephaloziaceae Jungermanniales) Revealed the Smallest Plastome with Complete Gene Set and High Intraspecific Variation Suggesting Cryptic Speciation

“…However in some cryptic species morphological characters are too blurry despite strong molecular, physiological and environmental differentiation, but this concerns mainly simple thalloids [37,41,42]. The phylogenetic position of Asian specimens reflects their divergence from European and North American specimens (Figure 4), but it does not impact a general tree layout as it is congruent with previously published one [24]. The comparative data for genus or species levels are very limited, since most sequenced genera consist of genome sequence of single species [4,10,29,30].…”

“…Both ycf genes are often considered as promising barcodes in many taxa of vascular plants [31][32][33][34]. The phylogenetic position of Asian specimens reflects their divergence from European and North American specimens (Figure 4), but it does not impact a general tree layout as it is congruent with previously published one [24].…”

“…As the backbone of phylogenetic analysis we used plastid CDS alignment from studies on Ptilidiales [24]. Existing dataset, which includes a set of plastid Nowellia curvifolia genes from Asian specimens, was expanded by adding CDS from three newly assembled plastomes (two from Europe and one form North America).…”

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

“…Branch support for each internode was evaluated with 300 bootstrap approximation (Additional file 3: Figure S1). The mitochondrial phylogeny of liverworts is mostly congruent with that of the plastid phylogeny [53].…”