Abstract
The colonization of land by descendants of charophyte green algae marked a turning point in Earth history that enabled the development of the diverse terrestrial ecosystems we see today. Early land plants diversified into three gametophyte-dominant lineages, namely the hornworts, liverworts, and mosses, collectively known as bryophytes, and a sporophyte-dominant lineage, the vascular plants, or tracheophytes. In recent decades, the prevailing view of evolutionary relationships among these four lineages has been that the tracheophytes were derived from a bryophyte ancestor. However, recent phylogenetic evidence has suggested that bryophytes are monophyletic, and thus that the first split among land plants gave rise to the lineages that today we recognize as the bryophytes and tracheophytes. We present a phylogenetic analysis of chloroplast protein-coding data that also supports the monophyly of bryophytes. This newly compiled data set consists of 83 chloroplast genes sampled across 30 taxa that include chlorophytes and charophytes, including four members of the Zygnematophyceae, and land plants, that were sampled following a balanced representation of the main bryophyte and tracheophyte lineages. Analyses of non-synonymous site nucleotide data and amino acid translation data result in congruent phylogenetic trees showing the monophyly of bryophytes, with the Zygnematophyceae as the charophyte group most closely related to land plants. Analyses showing that bryophytes and tracheophytes evolved separately from a common terrestrial ancestor have profound implications for the way we understand the evolution of plant life cycles on land and how we interpret the early land plant fossil record.
Highlights
It is widely accepted that land plants, or embryophytes, descend from an aquatic green algal ancestor (Karol, 2001; McCourt et al, 2004) that colonized land over 450 Mya (Magallón et al, 2013; Morris et al, 2018), reconstructing the relationships among the bryophytes and tracheophytes, and identifying the algal lineage that is most closely related to the embryophytes, has been challenging and controversial (Cox, 2018)
All ML bootstrap analyses of the protein-coding nucleotide data (GTR+G4 +Fest) strongly support the placement of the moss lineage as sister-group to all other plants (BS>90%), with the hornworts fully supported as the sister-group to the tracheophytes
ML bootstrap analyses with optimal numbers of gene partitions (11 partitions with separate models; Figure S1) did not result in topological differences compared to the nonpartitioned ML bootstrap analysis (Figure 2A), and the use of an alternative starting tree for estimating the optimal gene partitioning scheme resulted in a slightly altered partitioning scheme but had no substantial effect on the statistical support regarding the placement of bryophyte lineages (Figure S2)
Summary
It is widely accepted that land plants, or embryophytes, descend from an aquatic green algal ancestor (Karol, 2001; McCourt et al, 2004) that colonized land over 450 Mya (Magallón et al, 2013; Morris et al, 2018), reconstructing the relationships among the bryophytes (liverworts, hornworts, and mosses) and tracheophytes (lycopods, ferns, and seed plants), and identifying the algal lineage that is most closely related to the embryophytes, has been challenging and controversial (Cox, 2018). In recent years, several studies have supported a hypothesis whereby the first divergence of land plants was between bryophytes and tracheophytes, ruling out a direct descendance of the tracheophytes from bryophytes, and having profound implications for how we view the evolution of plants on land. These newer studies have used better-fitting models that more accurately account for heterogeneity in the data, and suggest that previous hypotheses were based on overly simplistic analyses (Cox et al, 2014; Puttick et al, 2018; Sousa et al, 2019)
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