Origin of land plants: do conjugating green algae hold the key?

Abstract

Background: The terrestrial habitat was colonized by the ancestors of modern land plants about 500 to 470 million years ago. Today it is widely accepted that land plants (embryophytes) evolved from streptophyte algae, also referred to as charophycean algae. The streptophyte algae are a paraphyletic group of green algae, ranging from unicellular flagellates to morphologically complex forms such as the stoneworts (Charales). For a better understanding of the evolution of land plants, it is of prime importance to identify the streptophyte algae that are the sister-group to the embryophytes. The Charales, the Coleochaetales or more recently the Zygnematales have been considered to be the sister group of the embryophytes However, despite many years of phylogenetic studies, this question has not been resolved and remains controversial.

Results: Here, we use a large data set of nuclear-encoded genes (129 proteins) from 40 green plant taxa (Viridiplantae) including 21 embryophytes and six streptophyte algae, representing all major streptophyte algal lineages, to investigate the phylogenetic relationships of streptophyte algae and embryophytes. Our phylogenetic analyses indicate that either the Zygnematales or a clade consisting of the Zygnematales and the Coleochaetales are the sister group to embryophytes.

Conclusions: Our analyses support the notion that the Charales are not the closest living relatives of embryophytes. Instead, the Zygnematales or a clade consisting of Zygnematales and Coleochaetales are most likely the sister group of embryophytes. Although this result is in agreement with a previously published phylogenetic study of chloroplast genomes, additional data are needed to confirm this conclusion. A Zygnematales/embryophyte sister group relationship has important implications for early land plant evolution. If substantiated, it should allow us to address important questions regarding the primary adaptations of viridiplants during the conquest of land. Clearly, the biology of the Zygnematales will receive renewed interest in the future.

Figure 1

Consensus Tree inferred by PhyloBayes under the CAT+ Γ4 using the viridiplant data set of 40 taxa and 30,270 amino acid positions (129 concatenated nuclear encoded proteins). An identical topology was obtained with two different methods (ML, BI) and four different models applied (site homogeneous ML, LG+F+Γ4 and GTR+Γ4; site heterogeneous BI, CAT+Γ4 and CATGTR+Γ4). Numbers represent (in order from top to bottom) the bootstrap support values for the PhyloBayes CAT+Γ4 and the RAxML GTR+Γ4 analyses. Black dots indicate that the branch was supported by a BP of 100% using both models. All except three nodes, which are indicated by a star, were supported by posterior probabilities (PP) of 1. The scale bar denotes the estimated number of amino acid substitutions per site.

Figure 2

Consensus Tree inferred by PhyloBayes using reduced data sets of 25 taxa (A. Spermatophytes and Selaginella eliminated) or 26 taxa (B. Chlorophytes and Mesostigma eliminated). The same methods and models were used as in Figure 1, with the only exception that no bootstrap analyses were performed for the PhyloBayes analyses, for which only the posterior probabilities are given. The alternative taxon samplings were aimed at either eliminating the fast evolving embryophytes (all spermatophytes and Selaginella) (A) or the distantly-related outgroup sequences eliminating chlorophytes and Mesostigma (B).

Figure 3

Principal component analysis of the complete 46 taxa data set. The two first axes of the multidimensional space are shown, they account together for 48% of the data. The principal component analysis demonstrates that the majority of the sequences have a homogeneous amino acid composition. Nevertheless, there are also several outliers most of them expectedly associated with distant outgroup species; more precisely there are two red algae, several chlorophytes, but also three streptophyte algae (Mesostigma, Klebsormidium and Closterium) and the embryophyte Huperzia.