Liverworts on the Green Tree of Life
Bryophytes as a natural group
Liverworts, along with mosses and hornworts, are often referred to as “Bryophytes.” There is strong evidence, however, that bryophytes, broadly defined in this way, are an artifical (i.e., non-monophyletic) group. Instead, the three bryophytes groups appear to form an evolutionary grade leading to the tracheophytes or true vascular plants. The three bryophyte groups (mosses, liverworts, hornworts) share a haploid-dominant life and unbranched sporophytes, traits that appear to be plesiotypic within the land plants (embryophytes). As early diverging lineages of green plants, the bryophyte groups comprise the oldest extant lineages of land plants. However, which group of bryophytes was the first to diverge, taking hold of terrestrial habitats for the first time? And which group is most closely related to that most successful group of plants, the vascular plants?
Phylogenetic relationships among bryophyte groups
Identifying the earliest branch in the land plant tree of life has been an elusive goal over the past two decades. Nearly every possible hypothesis of the relationships among bryophytes (hornworts, liverworts, and mosses) and tracheophytes (vascular plants) has been advanced. Early phylogenetic studies of this problem converged on liverworts as the sister group to the rest of the embryophytes (Mishler and Churchill, 1984 [morphology], Mishler et al., 1994 [nuclear DNA and morphology], Lewis et al., 1997 [chloroplast DNA]). Fossil evidence (Edwards et al., 1995), analyses of the entire chloroplast genome (Kugita et al., 2003), analyses of group II mitochondrial introns (Qiu et al., 1998; Pruchner et al., 2001; Groth-Malonek et al., 2005), and mitochondrial DNA editing (Steinhauser et al. 1999) also support this hypothesis. Nevertheless, some studies support the hornworts as the earliest-diverging taxon, with mosses and liverworts forming a clade that is sister to the tracheophytes (Hedderson et al. 1996, 1998 (nrDNA); Garbary and Renzaglia, 1998 (morphology); Nishiyama and Kato (cpDNA) 1999; Renzaglia et al. 2000 (morphology); Nickrent et al. 2000 (nrDNA, mtDNA, cpDNA). A few recent studies have suggested that bryophytes are monophyletic and sister to the tracheophytes (Nishiyama et al., 2004; Goremykin and Hellwig, 2005).
Currently, the National Science Foundation funds an ATOL project focused upon resolving the earliest evolutionary splits in the land plant tree: The Green Tree of Life. Preliminary results from this project suggest that the liverworts are the earliest lineage – that is, are sister to all other groups of land plants -- followed by the mosses, and finally, the hornworts as sister to the tracheophytes. This conclusion is supported by mitochondrial data (Groth-Malonek and Knoop, 2005; Groth-Malonek et al., 2005) as well as combined data from the chloroplast and nuclear genomes (Davis, 2005).
The importance of determining phylogenetic relationships
among early land plants
The placement of bryophytes in the embryophyte phylogeny is important for interpreting the evolution of many important and fundamental plant characteristics including stomata, IAA (auxin) conjugation, chloroplast morphology, and sperm morphology. For example, stomata are absent on liverwort sporophytes, but they are present in mosses and hornworts. In addition, liverworts do not conjugate IAA, while the rest of embryophytes do (Sztein et al., 1995). If liverworts are the earliest lineage, it is most parsimonious to infer the origin of stomata and IAA conjugation after the liverworts split from the rest of the embryophytes. A similar scenario is presented with the consideration of chloroplast pyrenoids and sperm cells. Pyrenoids are present in the chloroplasts of green algae and hornworts, but are absent from other embryophytes (Renzaglia and Vaughn, 2000). If liverworts diverged first, then there have been multiple losses of pyrenoids, or else pyrenoids independently evolved in the hornwort lineage. Likewise, green algae and hornworts have sperm cells with asymmetrically attached flagella, but swimming sperm in all other embryophytes have symmetrically attached flagella (Renzaglia et al., 2000). In the context of current ideas about early land plant phylogeny, asymmetrical attachment of sperm flagellae is best interpreted as an independent gain in the hornworts, or multiple independent gains of symmetrically attached flagella in the other embryophyte groups.