Plant Physiol.

(1998) 116: 9–15

Update on Evolution

Algal Phylogeny and the Origin of Land Plants1

Debashish Bhattacharya* and Linda Medlin

Department of Biological Sciences, Biology Building, University of Iowa, Iowa City, Iowa 52242–1324 (D.B.);
and the Alfred Wegener Institute for Polar and Marine Research, Am Handelshaven 12,
27570 Bremerhaven, Germany (L.M.)

The green algae and land plants form a monophyletic a bewildering array of cell morphologies and life cycles
lineage (the chlorophytes) that contains both protistan and and live in a multitude of habitats. The major lineages of
higher taxa (Graham, 1996). An important issue regarding the algae are the Chlorophyta (green algae), Rhodophyta
the evolution of this green lineage that still remains in (red algae), Glaucocystophyta, Euglenophyta, Chlorarach-
question is the identity of the green algal (i.e. flagellate) niophyta, Heterokonta, Haptophyta, Cryptophyta, and the
ancestor of land plants. Modern molecular phylogenetic dinoflagellates (within the Alveolata). The latter four
data provide the framework for reconstructing this evolu- groups have been loosely termed the chromophyte algae
tionary history and for asking deeper questions about the because they contain chlorophyll a and c and various xan-
origin of the genetic inventions that have played a role in thophylls that make them appear yellow or brown. The
the radiation of the green lineage, a group that contains algae include not only the world’s largest protists, the kelps
nearly all levels of vegetative morphology, from single cells (Macrocystis spp. in the Heterokonta, which may be up to
to filaments to well-organized colonies to complex terres- 30 m in length), but also many bacteria-sized (1–5 mm)
trial plants. coccoid taxa (e.g. Chlorella spp. and Micromonas spp. in the
The green lineage is, however, only one example of Chlorophyta and Pelagomonas spp. in the Heterokonta).
photosynthetic taxa that have successfully colonized our Many tiny, single-celled algae live within a complex
planet. A much greater diversity of plastid-containing or- exoskeleton made of CaCO3 or silica, which accumulates
ganisms is defined by the various other forms of algae. The over time in deep sea deposits in the world’s oceans (coc-
algae include the green algal relatives of land plants and a colithophorids, diatoms). The fossil remains of these algae
diverse collection of single-celled and multicellular taxa are routinely used for paleoclimatic reconstructions and to
such as the heterokonts, rhodophytes (red algae), crypto- predict climate change. Algae have played critical roles in
phytes, chlorarachniophytes, dinoflagellates, and hapto- ecological studies of aquatic (e.g. kelp forests in northern
phytes. Understanding the interrelationships and origins of California) and terrestrial ecosystems and have been used
these lineages is an interesting problem in evolutionary as model protists in physiological and biochemical studies
biology, not only because the algae contain the dominant (e.g. Chlamydomonas reinhardtii in the Chlorophyta) and
primary producers on this planet, but also because uncov- have been the cause of many fundamental questions in
ering the ancestry of their plastids offers the possibility to biology because of their diverse and complex life histories.
gain insights into the many facets of endosymbiosis, such In addition, algae have had a long history in the food (e.g.
as endosymbiont genome reduction and gene transfer to nori, wakame) and drug (e.g. agar-agar, carrageenan, alg-
the host nucleus (Gilson and McFadden, 1996). Present inic acid) industries. The motile stage of most algae have
knowledge argues overwhelmingly for a cyanobacterial two (or more) flagellae, but some lineages lost this charac-
origin of all algal plastids, with stable incorporation of ter once during their early evolution (e.g. Rhodophyta) or
many of the endosymbiont’s genes in the host genome multiple times in different members relatively late in evo-
(Bhattacharya and Medlin, 1995). These and other recent lution (Trebouxiophyceae, Chlorophyta). Readers are re-
data concerning the origins of algae and their plastids form ferred to descriptive/systematic treatments such as in Van
a starting point from which the origin of the green lineage den Hoek et al. (1995) for detailed information regarding
can be better understood. the different algal groups.
When phycologists were first faced with the daunting
problem of understanding the interrelationships of the dif-
THE ALGAE ARE A DIVERSE GROUP OF EUKARYOTES
ferent algal groups, they realized that it would be difficult
The algae, which can be loosely defined as photosyn- to find a set of reliable characters that could form the basis
thetic eukaryotes/protists excluding the land plants, have of this classification. The distinct morphology of many
lineages such as the red algae (e.g. the complete lack of
1
This research was financed in part by a grant from the Deut- flagellated stages) allowed their separation from other al-
sche Forschungsgemeinschaft (Bh 4/1-2). gae and recognition as an independent natural lineage, but
* Corresponding author; e-mail [email protected]. the interrelationship of this group (as with many other
edu; fax 1–319 –335–1069. algal groups) with other eukaryotes remained unclear.
9
10 Bhattacharya and Medlin Plant Physiol. Vol. 116, 1998

Many advances were made possible with the advent of the case of plastids with four membranes, the third mem-
electron microscopy, which allowed the detailed study of brane is presumably the plasmalemma of the engulfed
algal cell ultrastructure and led to hypotheses about the eukaryote, whereas the fourth is the phagosomal mem-
phylogeny of these taxa (Mattox and Stewart, 1984). One of brane of the host cell. Three-membraned complex plastids
the most important concepts that came out of these studies such as those in the euglenophytes and in most dinoflagel-
was the recognition that vegetative cell morphology forms lates appear to have resulted from the loss of one of the
a poor basis for a natural classification. The plasticity of outer membranes. The number of plastid membranes has
forms has led to the misclassification of species and over- turned out to be a good marker for primary and secondary
classification of ecotypes and has contributed to confusion endosymbiotic events and in combination with sequence-
in algal taxonomy. It is now widely recognized that aspects based phylogenies has clarified the origin of most algal
of the motile/reproductive cell ultrastructure, such as the plastids (Delwiche and Palmer, 1997).
morphology of the flagellae, flagellar roots, and basal bod-
ies, form a far more reliable basis for taxonomic classifica-
tion because these characters are stable over evolutionary
PLASTID ORIGIN DEFINES ALGAL ORIGIN
time (Friedl, 1997). One problem with using morphological
characters for creating phylogenies arises from the difficul- The molecular phylogenetic studies have superceded
ties in assigning phylogenetic values to certain key charac- the ultrastructure-based classification schemes and have
ters (e.g. ultrastructure of flagellar hairs) in distantly re- shown that the morphological diversity of the algae results
lated groups that either vary substantially in morphology in fact from their polyphyletic origins within the eukary-
or are of questionable homology (character state shared otic tree of life (Bhattacharya and Medlin, 1995; Stiller and
through common ancestry). Hall, 1997). The algae are an artificial group that includes
Further attempts to classify the algae during the 1960s some taxa that are more closely related to other nonphoto-
and 1970s were based on ultrastructural features of plastids synthetic protists (e.g. chlorarachniophytes to filose amoe-
of the major groups. These data led to the recognition of bae, euglenophytes to kinetoplastids, heterokont algae to
two fundamentally different types of plastids: the simple labyrinthulomycetes) than to other algae. A schematic view
plastids in the chlorophytes, rhodophytes, and glaucocys- of the tree of life based on rDNA sequence comparisons is
tophytes, which have two bounding membranes, and the shown in Figure 2. The important features of this tree are
complex plastids (Sitte, 1993) in virtually all other algae (a) the three domains of life (Archaea, Bacteria, Eukarya),
(Fig. 1), which have three or more bounding membranes. (b) the divergence of a number of protist groups (Micros-
The simple plastids are thought to retain the two mem- poridia, Trichomonads) relatively deep within the eukary-
branes of the engulfed cyanobacterium resulting from a otic domain, (c) the occurrence of a near-simultaneous
primary endosymbiotic event. origin of many eukaryotic groups within the so-called
Algae with plastids bounded by three or four mem- crown-group radiation, and (d) the enigmatic position of
branes have gained this organelle from the engulfment of the photosynthetic euglenophytes as the earliest algal
an existing alga (secondary endosymbiosis; Gibbs, 1993). In divergence.

Figure 1. Origins of simple and complex plastids via primary and secondary endosymbioses. Algae containing simple and
complex plastids are listed alongside the cells. The chloroplast ER (continuity of the outer plastid membrane and the outer
membrane of the nuclear envelope) found in some complex plastid-containing algae is not shown. N, Nucleus; CB,
cyanobacterium.
 Algal Phylogeny and the Origin of Land Plants 11

Furthermore, immunological studies have shown that the

light-harvesting antenna complex proteins of PSI are re-
lated in green and red algae but not in the cyanobacteria.
Finally, the ability of plastid transit peptides from the
glaucocystophyte alga Cyanophora paradoxa to direct effi-
ciently the targeting of nuclear-encoded plastid proteins
into land-plant plastids (and vice versa) suggests that these
organelles share a common import pathway (for review,
see Delwiche and Palmer, 1997). In spite of this evidence,
the search for the cyanobacterial ancestor(s) for the differ-
ent simple-plastid types, if such taxa exist, remains one
of the most important areas of future research in algal
evolution.
In this regard, the discovery of the Prochlorophyta
(Lewin, 1976) deserves mention in any discussion of plastid
endosymbiosis. These cyanobacteria contain chlorophyll a
and b and closely spaced thylakoids similar to those of the
green algae. They provided the first opportunity to test the
hypothesis of a separate primary endosymbiotic origin of
the green algal plastid. Other known cyanobacteria were
Figure 2. Small subunit rDNA phylogeny showing the three domains presumably the source of the red algal and glaucocysto-
of life with emphasis on the phylogeny of the eukaryotes. This tree phyte simple plastids, since these all contain only chloro-
has been adapted from Sogin et al. (1996). The branch lengths are phyll a and phycobilins. The expectation of a missing link
approximate evolutionary distances and show only the relative po- within the prochlorophytes was unfulfilled because phylo-
sitions of the taxa. Photosynthetic taxa are shown in gray or stippled genetic analyses have shown that the prochlorophytes are
fields. a paraphyletic group within the cyanobacteria and that
none of its members shares a direct common ancestry with
A more detailed phylogenetic analysis of the crown the monophyletic green algal plastid lineage (Palenik and
group radiation is shown in Figure 3A. Here we present a Haselkorn, 1992; Urbach et al., 1992). The paraphyletic
phylogeny of the host cells (Fig. 3A) and of the plastids that origin of the prochlorophytes also suggests that chloro-
are found in these host cells (Fig. 3B). These analyses allow phyll b has had multiple origins within the cyanobacteria.
us to deal separately with the origins of the hosts and the In light of the above data, do we then find a monophy-
endosymbionts and then, by comparison of the tree topol- letic origin of the host cells of the simple-plastid-containing
ogies, to reach conclusions about the number of primary algae in Figure 3A? Until now, no rDNA phylogeny has
and secondary endosymbiotic events that explain the ori- been able to show conclusively that chlorophytes, rhodo-
gin of the algae. The plastid tree, for example, shows that phytes, and glaucocystophytes form a monophyletic
there are three closely related major lineages of plastids: i.e. grouping in the host cell trees. However, there are prelim-
the simple plastids of the chlorophytes, rhodophytes, and inary data from actin sequence comparisons that support
glaucocystophytes (the latter are termed cyanelles), which this scenario (Bhattacharya and Weber, 1997) and limited
diverge nearly simultaneously from each other and are a RNA polymerase II (RPB1) data that do not (Stiller and
monophyletic sister group of the cyanobacteria. This result Hall, 1997). Comparison of the cox3 gene in red and green
is consistent with a primary endosymbiotic origin of these algal mitochondria support the monophyly of these
plastids from a cyanobacterial ancestor. Phylogenetic anal- groups, although glaucocystophyte sequences have not yet
yses of additional plastid genes such as tufA (Köhler et al., been included in these analyses (Boyen et al., 1994).
1997), atpB (Douglas and Murphy, 1994), rpoC1 (Palenik Clearly, additional taxa must be included in these protein-
and Swift, 1996), and psbA (Hess et al., 1995) also provide sequence phylogenies to test the monophyly of all simple-
moderate to strong support for plastid monophyly. The plastid-containing algae. The most parsimonious scenario
phylogenetic data do not, however, allow us to distin- of a single origin of all simple-plastid-containing algae
guish between the endosymbiosis of a single cyanobacte- from an ancestral protoalga remains open to question.
rium or of several closely related cyanobacteria in the What, then, about the origin of complex plastids?
common ancestor(s) of the chlorophytes, rhodophytes, and Here the molecular sequences provide clear and compel-
glaucocystophytes. ling results about secondary endosymbiosis. First, it is
The hypothesis that all simple plastids trace their ances- important to see in the host cell tree that some algal groups
try to a single origin is supported by great similarities in (e.g. heterokonts, cryptophytes, chlorarachniophytes) form
plastid genome content and organization (e.g. psbB/N/H secondarily photosynthetic groups that trace their ances-
and atp/rps/rpo gene clusters, Douglas, 1992). Because tries to nonphotosynthetic ancestors (Fig. 3A). The apicom-
gene order is variable among the cyanobacteria, this sug- plexan relatives of ciliates and dinoflagellates (Prorocen-
gests that if these organelles are of separate origins then trum micans within the alveolate lineage) contain a 35-kb,
massive convergence must have occurred independently in circular, extrachromosomal DNA that has also been iden-
each plastid lineage to result in the present gene maps. tified as a reduced plastid genome. However, unlike most
12 Bhattacharya and Medlin Plant Physiol. Vol. 116, 1998

Figure 3. Small subunit rDNA phylogenies. A, Host cell (nuclear) phylogeny constructed with the maximum likelihood
method. Results of a bootstrap neighbor-joining distance analysis with a Kimura matrix as input (100 replications) are shown
as branch nodes of differing thicknesses (see box to the right in A). NM, Gene from the nucleomorph or vestigial nucleus
within the plastid; NU, gene from the nucleus of the same organism. Photosynthetic taxa are shown in the gray field. This
tree is rooted within the branch leading to Dictyostelium discoideum. Bootstrap values greater than 70% are normally
interpreted as providing support for the groupings to the right of these values. B, Plastid phylogeny constructed with the
neighbor-joining method with a LogDet matrix as input. The three simple plastid lineages (plus the complex plastids derived
from these algae) have been boxed and are shown in the gray fields. The complex plastids are shown in large typeface. This
tree is rooted within the branch leading to Agrobacterium tumefaciens. For further details about these trees, see Bhattacharya
and Medlin (1995).

dinoflagellates, this plastid has four membranes and has protist group, rather than by a close phylogenetic relation-
likely resulted from the secondary endosymbiosis of a ship between euglenophytes and the green algae. Although
green alga (Köhler et al., 1997). The apicomplexans, includ- bootstrap values are not shown in the LogDet tree in Figure
ing the malaria parasite Plasmodium falciparum can there- 3B, another method, transversion analysis, provides cor-
fore be thought of as the most peculiar algae. In addition, roborative evidence for this topology (Van de Peer et al.,
as shown in Figure 3B, all known complex plastid rDNA 1996). The use of methods that correct for nucleotide bias,
sequences form sister groups to or are embedded within such as LogDet transformation, are necessary for the re-
the different simple-plastid lineages. These data argue con- construction of plastid rDNA phylogenies due to the vary-
vincingly for the origin of complex plastids from secondary ing nucleotide contents of this gene in different plastid
endosymbioses involving existing red and green algae. genomes (Bhattacharya and Medlin, 1995; Van de Peer et
The four-membraned plastids of the cryptophytes, het-
al., 1996).
erokonts, and haptophytes have all arisen from separate
More convincing evidence for secondary endosymbiosis
secondary endosymbioses involving red algae. Likewise,
comes from the finding of remnants of the nuclear genome
the three- and four-membraned plastids of the eugleno-
phytes and chlorarachniophytes, respectively, trace their of the algal symbionts in the periplastidial compartment
origins within the green algal lineage. These results are between the second and third membranes of the complex
supported by a number of ultrastructural and biochemical plastids of the cryptophyte and chlorarachniophyte algae.
characters (e.g. all chloroplasts and secondary endosymbi- This nucleomorph DNA has been analyzed and supports
onts from this lineage contain chlorophyll a and b). The further the algal origin of these plastids. See, for example,
presence of photosynthetic euglenoids can therefore be the grouping of the chlorarachniophyte nucleomorph
most easily explained by the secondary endosymbiosis of rDNA sequences with those of the green algae (Fig. 2A;
an existing green alga into this relatively early diverging Van de Peer et al., 1996).
 Algal Phylogeny and the Origin of Land Plants 13

Complete genome sequencing of the small, linear nucleo- to a primary endosymbiosis and has as a possible sister
morph chromosomes identified in the cryptophytes and group other simple, plastid-containing algae such as the
chlorarachniophytes promises to provide many new in- rhodophytes and glaucocystophytes. Characters that to-
sights into the process of genome reduction (e.g. the exis- gether distinguish the green lineage from all other eu-
tence of mini-spliceosomal introns of 19–20 nucleotides karyotes are a two-membraned plastid containing chloro-
and an average spacer length of 65 nucleotides) that must phyll a and b and stacked thylakoids with intraplastidial
occur following secondary endosymbiosis of an alga (Gil- starch storage and a stellate structure in the flagellar tran-
son and McFadden, 1996). The chlorarachniophyte nucleo- sition region. In the next section the phylogeny of the green
morph genome consists of three linear chromosomes with lineage will be presented in more detail.
a total size of 380 kb. The lack of nucleomorph DNA in the
heterokont, haptophyte, and euglenophyte plastids is most
FROM GREEN ALGAE TO LAND PLANTS
easily interpreted as the complete reduction of these ge-
nomes by the host cell. However, among the dinoflagel- The results of approximately 25 years of electron-
lates are binucleate species, in which the intact endosym- microscopic analyses of members of the green lineage have
biont nucleus remains within the host dinoflagellate. resulted in a number of hypotheses regarding the origin
Rubisco sequence comparisons have identified, for exam- and diversification of these taxa. The most important of
ple, the origin of the nondinokaryon nucleus in Peridinium these is based on the observation that two fundamentally
foliaceum as an advanced diatom genus (Chesnick et al., different types of microtubule organization are found
1996). within the green lineage during cytokinesis. The first,
Taken together, the phylogenetic analyses of algal hosts termed a phycoplast, is characterized by the collapse of the
and plastids shows that there is good support for a mono- spindle apparatus after mitosis, with the microtubules ori-
phyletic origin of the simple plastids from a cyanobacterial ented in the same direction as the plane of cell division. The
endosymbiont, although the host cell trees have not yet second, termed a phragmoplast, is characterized by the
been able to prove conclusively this scenario. Secondary development of a persistent telophase spindle and a cleav-
endosymbiosis has played a dominant role in the origin(s) age furrow, with the microtubules oriented at right angles
of algae, since many previously nonphotosynthetic taxa to the plane of cell division. That charophytes and land
have become algae after the uptake of an existing photo- plants have a phragmoplast type of cell division, whereas
synthetic eukaryote (Bhattacharya, 1997). The dinoflagel- chlorophytes, trebouxiophytes, and some members of the
lates contain a large variety of yet unexplored complex ulvophytes have a phycoplast type of cell division led to
plastids that will likely provide many further examples of the division of the green algae and land plants into two
independent secondary endosymbioses in algal evolution. distinct groups based on this cytokinetic character (Mattox
Future research on secondary endosymbiosis should focus and Stewart, 1984; Fig. 4).
on uncovering the origins of the complex plastids in Features of the motile cells were also found to be largely
dinoflagellate taxa such as Lepidodinium viride, Dinophysis in accordance with this scheme and have played a central
spp., and Gyrodinium aureolum, which appear to contain role in the resolution of evolutionary relationships of mem-
plastids of chlorophyte, cryptophyte, and haptophyte ori- bers of the green lineage. Of particular importance for the
gins, respectively (Bhattacharya and Medlin, 1995). distinction of the charophytes from other members of the
However, secondary endosymbiosis is not always the green lineage are the usual presence of square-shaped
result of a previously nonphotosynthetic protist engulfing scales on the surface of biflagellate, asymmetric cells with a
an alga since the cryptophytes share a common ancestry lateral/subapical flagellar insertion, and the presence of
with the simple plastid (cyanelle)-containing glaucocysto- multilayered structures associated with the flagellar roots.
phytes (Fig. 3A). In this lineage, the common ancestor of The molecular sequence data from nuclear- (Bhattacharya
the cryptophytes was likely photosynthetic (i.e. contained a and Ehlting, 1995; Kranz and Huss, 1996; Friedl, 1997),
cyanelle). This alga lost its plastid (e.g. Goniomonas trun- plastid- (Manhart, 1994), and mitochondria-encoded (Malek
cata) and later replaced it with that from a red alga. It is et al., 1996) genes also support a sister-group relationship
hypothesized that the uptake of a secondary endosymbiont between charophytes and land plants. In addition, several
may be simplified if the nuclear-encoded plastid proteins structural markers such as the presence of group II introns in
with existing transit sequences already exist in the host cell two different tRNA genes of all land plants, Coleochaete spp.,
nucleus and that these genes can be reutilized after the and Nitella spp. (Charales), which are found in only one of
uptake of a new symbiont that is phylogenetically closely these genes in Spirogyra spp. (Zygnematales) and in no
related to the original endosymbiont (Häuber et al., 1994). chlorophytes, suggests that the charophytes are directly re-
The host cell would then require only the invention of a lated to the land plants, with Chara/Nitella spp. being more
modified transit sequence to allow entrance into the now closely related than Spirogyra spp. (Manhart and Palmer,
four-membraned plastid. This hypothesis would be sup- 1990). In light of these data the monophyly of charophyte
ported by the finding of remnant genes encoding plastid green algae and land plants may be considered to be estab-
proteins in the nuclear genome of G. truncata. lished within the literature.
The results and hypotheses described above show that An intriguing question that still remains to be verified
the green algae are only one of many photosynthetic pertains to the ancestry of the charophytes/land plants,
groups that have evolved multiple times on our planet. The because the monophyly of the green lineage is consistent
green lineage contains a simple plastid that traces its origin with a flagellate ancestry of this group. The discovery of a
14 Bhattacharya and Medlin Plant Physiol. Vol. 116, 1998

Figure 4. Small subunit rDNA phylogeny of the green lineage. This tree has been constructed with a weighted maximum
parsimony method, and the results of bootstap analyses (200 replications) are shown as branch nodes of differing thicknesses
(see box on the right). The likely position of divergence of the prasinophyte M. viride is shown with a broken line. The
phylogeny is rooted within the branch leading to the rDNA sequence of the glaucocystophyte C. paradoxa.

group of unicellular taxa (the Prasinophyceae) that have with some members (Charales) reaching a size of 2 to 30
both their body and flagella covered with square-shaped, cm, to the bryophytes and then to the other land plants. To
nonmineralized scales and have parallel basal bodies and a gain insights into the genetic developments that have led
depression or groove from which the flagella arise offered stepwise to the origin of land plants we are analyzing
a likely source for this missing link. The typical scales of actin-coding regions to see whether duplications of this
the prasinophytes are also found in the flagellate stages of important cytoskeletal gene family may have accompanied
the Charophyceae and the Ulvophyceae but not in other the origin of multicellularity in the green lineage (Bhatta-
eukaryotes (Melkonian and Surek, 1995). charya and Ehlting, 1995).
Analyses of small subunit rDNA sequences have dem- Actin exists as a constitutively expressed single-copy
onstrated that the prasinophytes are a paraphyletic group gene in all green algae except the ulvophytes, which appear
that arise as multiple independent lineages at the base of to have undergone independent gene duplications. The
the radiation of the chlorophytes, ulvophytes, and treboux- charophytes also contain single-copy actin genes. The
iophytes (Fig. 4). One member of the Prasinophyceae, Me- present data show actin gene duplications to appear first
sostigma viride, has been positioned with low bootstrap within the ferns, which are positioned as the sister group to
support at the base of the charophytes/land plants in a the complex flowering plant actin gene families. Future
rDNA analysis (Melkonian and Surek, 1995). This relation- research will also focus on resolving the origin of coding
ship was predicted earlier from the unique cell ultrastruc- regions within the green algae and charophytes involved in
ture of M. viride. It is the only prasinophyte to lack flagellar morphogenesis, such as the MADS box genes, to gain
hair scales, and its cell body is extremely compressed along further insights into the evolution of the green lineage. It is
the anterior-posterior axis. Until now, no clear positioning likely that the evolution of multicellularity within plants
within the green algae was possible because of the equiv- has followed another plan than that in animals (for review,
ocal nature of the morphological data. Both M. viride and see Meyerowitz, 1997) and that phylogeny reconstruction
the charophytes share the feature of two multilayered can play an important role in creating a logical framework
structures located in the identical orientation to the flagel- for understanding the basis for plant organismal evolution.
lar roots.
In summary, there is now some evidence for a prasino-
phyte ancestry for the charophytes, which themselves are
the ancestors of the bryophytes, ferns, gymnosperms, and ACKNOWLEDGMENTS
angiosperms (Fig. 4). Fossil evidence shows that the land We thank V.A.R. Huss (Erlangen) for providing the green algal/
plants have existed for approximately 450 to 470 million plant rDNA alignment.
years (Gray et al., 1982). This assemblage has therefore seen
its members evolve from a single-celled alga similar to M. Received July 23, 1997; accepted October 6, 1997.
viride to the charophytes, the most complex green algae, Copyright Clearance Center: 0032–0889/98/116/0009/07.
 Algal Phylogeny and the Origin of Land Plants 15

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