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.
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