Abstract
Congruence among analyses of plant genomic data partitions (nuclear, chloroplast and mitochondrial) is a strong indicator of accuracy in plant molecular phylogenetics. Recent analyses of both nuclear and chloroplast genome data of land plants (embryophytes) have, controversially, been shown to support monophyly of both bryophytes (mosses, liverworts, and hornworts) and tracheophytes (lycopods, ferns, and seed plants), with mosses and liverworts forming the clade Setaphyta. However, relationships inferred from mitochondria are incongruent with these results, and typically indicate paraphyly of bryophytes with liverworts alone resolved as the earliest-branching land plant group. Here, we reconstruct the mitochondrial land plant phylogeny from a newly compiled data set. When among-lineage composition heterogeneity is accounted for in analyses of codon-degenerate nucleotide and amino acid data, the clade Setaphyta is recovered with high support, and hornworts are supported as the earliest-branching lineage of land plants. These new mitochondrial analyses demonstrate partial congruence with current hypotheses based on nuclear and chloroplast genome data, and provide further incentive for revision of how plants arose on land.
Highlights
The embryophytes, or land plants, share a green algal ancestor (McCourt, Delwiche & Karol, 2004) that colonized terrestrial environments between 515.1–470.0 Ma (Morris et al, 2018) and comprise gametophyte-dominant lineages, collectively known as bryophytes, and a sporophyte-dominant lineage, the tracheophytes
The tree-heterogeneous composition analysis (NDCH2) of the concatenated nucleotide data resulted in mosses supported as the earliest-diverging land plant lineage (PP = 0.98; Fig. 1B; Fig. S3), but placed liverworts as the sister-group to tracheophytes (PP = 0.94)
Whereas using a homogeneous model for the analysis of the codon-degenerate data shows liverworts well supported as the sister-group to other embryophytes, the tree-heterogeneous analysis (NDCH2) model places liverworts as the sister-group to the mosses, with maximum support, and hornworts as the sister-group to all other embryophytes, with maximum branch support. These results demonstrate that the phylogenetic signal contained in non-synonymous sites is subject to composition biases and that tree-heterogeneous composition models are required to model the data effectively
Summary
The embryophytes, or land plants, share a green algal ancestor (McCourt, Delwiche & Karol, 2004) that colonized terrestrial environments between 515.1–470.0 Ma (Morris et al, 2018) and comprise gametophyte-dominant lineages, collectively known as bryophytes, and a sporophyte-dominant lineage, the tracheophytes. 2014; Ruhfel et al, 2014; Zhong et al, 2013; Bell et al, 2020), and mitochondrial (Turmel, Otis & Lemieux, 2013; Liu et al, 2014; Bell et al, 2020) genomes have long remained conflicting These incongruences are likely due to molecular evolutionary processes that are especially apparent at deep timescales, such as multiple substitutions on the same site, that lead to loss of phylogenetic signal, and heterogeneity in substitution process patterns among sites and among lineages (Cox, 2018). Several recent phylogenomic analyses based on large nuclear data sets and extensive taxon sampling (e.g., Wickett et al, 2014; Leebens-Mack et al, 2019) have been equivocal These studies presented monophyletic-bryophyte phylogenies based on multi-species coalescent supertrees, but concatenated analyses of the same data resulted in trees in which the bryophytes were paraphyletic. These tree-heterogeneous composition models are demonstrably better-fitting and are likely more accurate and reliable than the analyses of larger data sets that used simpler and poorer-fitting models (Cox, 2018)
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