9 Algal Evolution and the Early Radiation of Green Plants

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Charles F. Delwiche

Robert A. Andersen

Debashish Bhattacharya

Brent D. Mishler

Richard M. McCourt

121

Eukaryotes perform photosynthesis thanks to a specialized

organelle that is derived from once free-living cyanobacteria

(i.e., blue-green algae). In land plants and green algae this

organelle is called the “chloroplast” in reference to its green

pigmentation, and by analogy the photosynthetic organelles

of groups with other pigmentation patterns have been called

“rhodoplasts” (red algae), “chromoplasts” (brown algae), and

so forth. This terminology is confused by the fact that the

chloroplasts of land plants exist in a number of developmental

forms that have sometimes been given names redundant

with those of the different algal lineages (e.g., “chromoplast”

for the carotenoid-rich form that gives color to some ripe

fruit). For simplicity, and because these organelles seem to

share a common ancestry (Delwiche et al. 1995), we use the

term “plastid” to refer to all such organelles. The hallmark of

the plastid is its reduced genome and concomitant complete

dependence upon the nuclear genome of the host cell. Like

mitochondria, the other clearly endosymbiotic organelle,

plastids have genomes that are greatly reduced in size and

complexity from those of their free-living cyanobacterial relatives

(Glцckner et al. 2000). For example, the fully sequenced

genome of the free-living cyanobacterium Nostoc sp. PCC

7120 is 6.4 Mb (million bases) in size, and encodes about

6626 genes (i.e., protein- or RNA-coding regions), and that

of Synechocystis sp. PCC 6803 is 3.5 Mb and encodes about

4003 genes. By contrast, well-characterized plastid genomes

range from 136 Kb and 191 genes in the glaucocystophyte

Cyanophora paradoxa to 120 Kb and 108 genes in the land

plant Pinus thunbergii, with smaller and less complex genomes

in some species with nonphotosynthetic plastids. Some larger

plastid genomes are known, but these seem to be special

cases, and a typical plastid genome encodes ≤5% of the number

of genes found in a free-living cyanobacterium (Palmer

and Delwiche 1998). The number of proteins expressed in a

typical plastid is, however, much larger than the number

encoded in the plastid genome. This is accounted for by the

massive transfer of former plastid genes to the nucleus (Martin

et al. 2002). Because plastids still need the products of

these transferred genes, they are utterly dependent upon the

nuclear genome of their host cell. Thus, plastids are tightly

integrated into the host cell and show close genetic, physiological,

and developmental coordination with the host.

With the exception of land plants, all eukaryotes with

plastids are called “algae.” The land plants or “embryophytes,”

are a monophyletic group of green algae that are characterized

by a life cycle that involves multicellular haploid and

diploid phases (the “alternation of generations”) and a suite

of distinctive ultrastructural and biochemical features, notably,

phragmoplastic cell division and plasmodesmata (described

below). The term “alga” has fallen out of favor in

recent years, in large part because of the belief that it encompasses

a polyphyletic set of lineages. This is accurate with

reference to the nuclear phylogeny, but neglects the plastid

component of the cell. Because there is substantial (although

not conclusive) evidence that plastids are monophyletic, in

this chapter we use “algae” to refer to a diverse assemblage

122 The Relationships of Green Plants

of eukaryotic autotrophic organisms, usually aquatic, that

are polyphyletic with respect to their nuclear genomes but

monophyletic with respect to their plastids (described below).

In a strict sense, the land plants should be viewed as a

specific, largely terrestrial, lineage of green algae. With renewed

interest in algae that poison, kill, pollute, or aggressively

invade new habitats, the general public is regaining an

interest and appreciation of this diverse assemblage of organisms.

And that interest extends to the more benign and beautiful

algae, as well as those species used for food by a large

number of human societies, for example, nori (Porphyra),

kombu (Laminaria), and many others in Japan and throughout

Asia; chu rhu (Monostroma) in Bhutan; dulse (Palmaria)

in Canada and the United States, to name a few. The oceans

cover approximately 71% of Earth’s surface, and cyanobacteria

and algae account for nearly all of the primary production in

oceans, directly supporting nearly all marine animal life.

The plastids of three distinct algal lineages are directly

derived from free-living cyanobacteria. Characterized by the

presence of only two unit membranes, such primary plastids

are most familiar in the green algae (chlorophytes) and

their derived, terrestrial subgroup, the land plants (embryophytes),

but are also found in the red algae (rhodophytes)

and in the glaucocystophytes, a small and relatively obscure

group of organisms whose plastids retain the peptidoglycan

cell wall of the cyanobacterial endosymbiont. All other photosynthetic

eukaryotes rely on plastids that were acquired

when the host cell ingested another eukaryote that already

had plastids. Termed “secondary” plastids because their evolution

required (at least) two sequential endosymbiotic relationships

to be established, these organelles are always

surrounded by more than two unit membranes, and in some

cases are part of complex endomembrane systems that include

tiny residual eukaryotic nuclei (nucleomorphs). Table

9.1 lists the principal groups of photosynthetic eukaryotes

discussed here, along with the characteristics of their plastids.

A summary view of our current knowledge of plastid

and host ancestries is shown in figure 9.1, which can be compared

with Delwiche (1999), which does not incorporate

the chromalveolate hypothesis. For more information on

the evolution of plastids and algae, the reader is referred to

Delwiche (1999) and Palmer (2003).

Glaucocystophytes, Red Algae,

and the Relationships among Taxa

with Primary Plastids

Two groups of algae have plastids with pigmentation that resembles

that of typical cyanobacteria: the glaucocystophytes

and the red algae. The glaucocystophytes are an unfamiliar and

relatively rare group of mostly freshwater algae with plastids

that have often been confused with cyanobacteria. Unlike red

algae, they are flagellate, although in some cases the flagella

are reduced to vestigial appendages inside of a cell wall (Kies

and Kramer 1989, Bhattacharya et al. 1995). Glaucocystophytes

are pigmented with chlorophyll a and light-harvesting

protein structures termed “phycobilisomes” that are also found

in most cyanobacteria and in red algae. These light-harvesting

protein complexes form distinctive knobs studding the

surface of the thylakoid membranes, where photosynthesis

occurs. The phycobilisomes also prevent the thylakoid membranes

from forming stacks of the type seen in green plants

and other organisms without phycobilisomes. Because phycobilisomes

have a characteristic absorption spectrum and result

in a distinctive ultrastructure, the glaucocystophyte plastid

bears a striking superficial resemblance to cyanobacteria. This

similarity was reinforced by the retention of a thin peptidoglycan

cell wall on the plastid, and long after the endosymbiotic

origin of plastids was recognized, the plastids of glaucocytophytes

were a source of confusion. Even today many authors

fail to distinguish these organelles from their free-living relatives.

In fact, these structures are authentic plastids, with

genome size and complexity that are markedly smaller than

those of free-living cyanobacteria and comparable with those

of other plastids (Stirewalt et al. 1995), and molecular phylogenetic

analyses firmly place them with other plastids

(Bhattacharya and Schmidt 1997).

Glaucocystophytes are rare inhabitants of clean freshwater

lakes, streams, and ditches and are not usually found

in high population densities. Only a handful of genera are

known, with only rudimentary knowledge for several, and

only about 13 species in three genera have been described

with reasonable confidence. Although they are unlikely to

be of any great environmental or ecological significance, the

glaucocystophytes seem to occupy a key position in the evolution

of eukaryotes as one of the earliest-diverging lineages

of algae (Martin et al. 1998). The relationships among the

major algal groups remain unresolved, but the most likely

placement for the glaucocystophytes is either as the earliestdiverging

lineage of algae with primary plastids and the sister

group to red + green algae, or as the sister group to red

algae alone. In either case, these organisms display key ancestral

characters that have been lost in related lineages, most

notably, the peptidoglycan plastid wall, which is absent in

all other lineages, and flagella, which are absent in the red

algae.

By contrast with the glaucocystophytes, the red algae are

a diverse and widespread group that dominates many temperate

and tropical marine intertidal environments. Red algae

can also be found growing at depths where the incident

light is a tiny fraction of that at the surface, in freshwater

environments, and even occasionally in soil crusts. But red

algae are rare in the open ocean, presumably because they

lack flagella at any stage of the life history. They are environmentally

important primary producers and provide food and

industrial chemicals, including the polysaccharide agarose

that is a staple of bacteriology and molecular biology. There

are three fundamental lineages of red algae, the subclasses

Florideophycidae and Bangiophycidae and the order CyaniAlgal

Evolution and the Early Radiation of Green Plants 123

Colorless

(Colorless)

Colorless

Colorless

Colorless

Secondary

Endosymbioses

"Chromalveolata"

Cryptomonads

Heterokonts

Dinoflagellates

Tertiary

Endosymbiosis

Primary

Endosymbiosis

*

Plastid with 2 unit membranes

Plastid with 3 unit membranes

Plastid with 4 unit membranes

Nucleus

Nucleomorph

Mitochondrion

A

B

C

Green Algae

(including

land plants)

Red Algae

?

*

Haptophyes

Heterokont (Diatom)

*

Eukaryote Cyanobacterium

Apicomplexa

Glaucocystophyta

Euglenophytes

Chlorarachniophytes

Chl. a, b &

Carotene

Peridinium foliacium

Chl. a,c &

Peridinin

Chl. a,c &

Fucoxanthin

Green Lineage Red Lineage

Figure 9.1. Another hypothesis for endosymbiotic events in the evolution of plastids. This

hypothesis should be compared to that presented by Delwiche (1999). This scenario includes the

“chromalveolate hypothesis” presented by Cavalier-Smith (1999), which proposes that the

chlorophyll a/b taxa (cryptomonads, heterokonts, haptophytes, and dinoflagellates), as well as a

number of colorless taxa, are descendants of a single endosymbiotic event. Under this scenario,

there are relatively few primary endosymbiotic events but more losses of pigmentation and

plastids. Some nonphotosynthetic lineages, for example, members of Apicomplexa, retain

unpigmented plastids and plastid genomes, but such direct evidence of a photosynthetic past has

not been documented from all of the colorless lineages that would be implied by this hypothesis.

The “cabozoan hypothesis” is not shown here (Cavalier-Smith 1999).

124 The Relationships of Green Plants

diales, each of which is thought to be monophyletic (Oliveira

and Bhattacharya 2000). The florideophytes are primarily

found in marine environments and are known for complex

life histories that fascinate some life science students and

torment the remainder. The bangiophytes are found in both

marine and freshwater environments. Although they are typically

less structurally and developmentally complex than

the better studied florideophytes, bangiophytes do show

considerable phylogenetic diversity and seem to be key to

understanding the evolution of the group (Oliveira and Bhattacharya

2000, Mьller et al. 2001). The Cyanidiales are a small

group whose members occur primarily in acidic hot springs

and differ markedly from other red algae in a number of key

properties (Albertano et al. 2000), and may be an outgroup

to the remainder of the red algae. The plastids of red algae

are pigmented with chlorophyll a and phycobilisomes similar

to those of glaucocystophytes and cyanobacteria.

It is interesting to note that although the red algae are

generally viewed as a marine group, many of the earliestbranching

bangiophytes and members of Cyanidiales are not

marine inhabitants. Because the glaucocystophytes and many

green algae are freshwater forms, this raises the possibility

that the earliest photosynthetic eukaryotes were freshwater

organisms.

A key problem in algal evolution, and one that has been

the topic of much debate, is whether all primary plastids

constitute a monophyletic group, and if so, whether they are

the result of a single endosymbiotic event. Most molecular

phylogenetic analyses of plastid genes show red, green, and

glaucocystophyte plastids to be a monophyletic group

(Delwiche et al. 1995, Delwiche 1999, McFadden 2001), but

analyses of nuclear genes are more equivocal. Early analyses

of nuclear ribosomal RNA (rRNA) genes typically did not

place red and green algae together in a monophyletic group,

albeit with relatively little support for their relative positions,

and more recent analyses of RNA polymerase genes also show

these as two distinct groups (Stiller and Hall 1997). However,

analyses of nuclear-encoded protein-coding genes have

more consistently and strongly supported monophyly of the

three lineages with primary plastids (Baldauf et al. 2000,

Moreira and Philippe 2001). Thus, glaucocystophytes, red

algae, and green algae constitute a single monophyletic group

in many molecular phylogenetic analyses of both plastid and

nuclear genes. On the surface this would imply that all primary

plastids are derived from a single endosymbiotic event.

It is important to note, however, that even if both host

and endosymbiont lineages form a monophyletic group, this

does not guarantee that the plastids are the result of a single

endosymbiotic event. It is always possible that closely related

host lineages independently acquired closely related endosymbionts

(much as dinoflagellates inhabit lineages of related

animals in the modern world). Indeed, although there may

have been a single, and singularly momentous case of indigestion

leading to the development of endosymbiotic plastids,

it seems more likely that the acquisition of plastids was

the result of a gradual adaptation of the ingesting host lineage

to the retention of ingested cyanobacteria for increasing

lengths of time. This would eventually lead to retention

of the endosymbiont through the complete cell cycle. Once

the endosymbiont became heritable, then the door would

have been open to permanent and obligate symbiosis, but

there is a good chance that the host cell had significant adaptations

to the presence of an endosymbiont long before the

endosymbiont became permanent. Consequently, evidence

that can distinguish between single and multiple origins of

primary plastids would have to come from properties that

are distinctive to the phenomenon of endosymbiosis itself.

Among such properties would be the characteristics of the

Table 9.1

Major Lineages of Algae, along with the Characteristics of Their Plastids and Estimate of Their

Biological Diversity.

Lineage Membranes Pigmentation Diversitya

Primary plastids

Glaucocystophytes 2 a, PB 50

Rhodophytes 2 a, PB 5500–20,000

Chlorophytes 2 a, b 13,500–100,000

Charophytes (excluding land plants) 2 a, b 20,000

Charophytes (including land plants) 2 a, b 500,000–1,000,000

Secondary or tertiary plastids

Cryptomonads 4 w/ nucleomorph a, c, PB 1200

Heterokonts (= Stramenopiles) 4 a, c 107,500–10,000,000

Haptophytes (= Coccolithophorids) 4 a, c 2000

Dinoflagellates 3 (4 in some) Various 3500–11,000

Apicomplexa 4 None 4800–4,800b

Chlorarachniophytes 4 w/ nucleomorph a, b ~20

Euglenoids 3 a, b 800

aEstimated number of species, based on Norton et al. (1996) and Van den Hoek et al. (1995).

bPerkins et al., (2000).

Algal Evolution and the Early Radiation of Green Plants 125

transit peptides that target nuclear-encoded gene products

into the plastid, and the content of the plastid genome after

its reduction to that of an organelle (Lцffelhardt et al. 1997).

However, although gene content and arrangement are superficially

similar in all three lineages of primary plastids, the

importance of such similarity can be interpreted only with

knowledge of the degree of similarity that would be expected

from independent endosymbiotic events, and it is entirely

possible that the similar content of plastid genomes is the

product of convergent evolution (Stiller et al. 2003)

Recent study of plastid retention in sea slugs provides

support for the view that the endosymbiotic origin of plastids

is likely to have involved a long period of predation and

facultative retention of plastids before the permanent and

obligate symbiosis. These remarkable animals eat algae

and selectively retain the chloroplasts, which are ingested by

cells and retained in a highly branched digestive tract that extends

nearly to the surface of the mantle (Rumpho et al. 2000).

In some cases the plastids are thought to serve primarily as a

form of camouflage, but in others (e.g., Elosia chlorotica) the

sea slug is able to survive indefinitely with light as its sole energy

source. These “solar-powered” sea slugs very nearly qualify

as algae in the definition given above, except that the plastids

are not retained through the complete life cycle and

have to be obtained each generation by eating an alga. However,

the length of time that the plastids are retained and

their continued functionality despite the photodegradation

that takes place in a normal functioning plastid suggest that

the sea slugs have sophisticated adaptations for plastid

maintenance. Recent work indicates that there are genes

resident within the sea slug’s nuclear genome that serve the

specific purpose of maintaining the plastid (Green et al.

2000, Hanten and Pierce 2001), and it may well be that

these genes were derived from the prey genome via a process

of horizontal gene transfer. Apparently you really are

what you eat (Doolittle 1998).

Cryptomonads, Heterokonts,

and Haptophytes: Secondary Plastids

Derived from Red Algae

The phenomenon of secondary endosymbiosis—in which

eukaryotes have acquired plastids by establishing a symbiotic

relationship with other eukaryotes that already had

plastids—has created a great deal of confusion. Because

organisms with secondary plastids are chimeric (i.e., composed

of tissues of two distinct evolutionary ancestries),

they present a bewildering mixture of characters from seemingly

unrelated organisms. Ultrastructural observations by

Gibbs (1962, 1981) led her to propose that the plastids of

several groups were acquired by secondary endosymbiosis.

The most spectacular form of secondary plastids is exemplified

by the cryptomonads, which are thought to have acquired

a red algal endosymbiont (Gillott and Gibbs 1980).

In these organisms, a set of four membranes surrounds the

plastid stroma and thylakoids. The two innermost envelopes

correspond to the plastid envelope of the primary plastid,

and the two outer membranes presumably correspond to the

red algal plasma membrane and a food vacuole of the host

cell. Remarkably, in the space that would have been the cytoplasm

of the red algal endosymbiont, there are ribosomes

and a degenerate eukaryotic nucleus, or “nucleomorph.” The

nucleomorph is a greatly reduced red algal nucleus, with

three chromosomes (Douglas et al. 2001). In a striking example

of convergent evolution, a very similar overall genome

structure is seen in the green-pigmented secondary plastids

of chlorarachniophytes (described below).

The plastids of cryptomonads, like those of red algae,

contain phycobiliproteins, but these proteins are located in

the thylakoid lumen and are not organized into phycobilisomes.

However, unlike typical red algal plastids, two

chlorophylls, a and c, are present. Chlorophyll c has been

taken as a character linking a putative group of algae referred

to as “chromophytes” or, more recently, Chromalveolates

(Cavalier-Smith 2000), including cryptomonads, heterokonts,

haptophytes, and dinoflagellates, all of which share

chlorophyll c and many of which have light-harvesting carotenoids.

The chromophyte clade was originally proposed by

Chadefaud (1950) as an algal lineage to stand equal with the

blue-green algae (= cyanobacteria), red algae, and green algae.

The chromophytes included the cryptophytes, heterokont

algae (including haptophytes), dinoflagellates, and euglenoid

algae in Chadefaud’s definition, but the euglenoids were removed

when the division Chromophyta was formally described

(Christensen 1989). Molecular studies during the

1990s suggested that the host-cell lineages of these organisms

do not constitute a monophyletic group, and the concept of

chromophytes fell into disfavor, although it has retained fairly

widespread use because these organisms do share a number

of ecological and structural similarities. However, recent

analyses of plastid-encoded genes (Fast et al. 2001, Yoon

et al. 2002) provide support for the hypothesis that the

chromophytes, and in particular, the clade defined by the

cryptomonads, heterokonts, and haptophytes (Chromista;

Cavalier-Smith 1986) may in fact be a monophyletic group,

or at least the product of symbiotic events involving organisms

with closely related plastids (fig. 9.1). This is still very

much an area of active investigation, and a recent extensive

analysis of plastid genes and genomes did not find support

for the chromalveolate hypothesis (Martin et al. 2002).

The heterokonts, which are also known as “stramenopiles”

for the bristles on their anterior flagellum, constitute

one of the great lineages of eukaryotic diversity and include

many protists once classified as algae, protozoa, and aquatic

fungi. These organisms have not received the measure of

study given to other eukaryotic lineages with comparable

diversity and age (i.e., green plants, animals, and fungi). Space

limitations will not allow this group to be given full justice

here, but they are among the dominant primary producers

126 The Relationships of Green Plants

in most marine environments and, as such, lie near the base

of the food chain for two-thirds of the planet. As might be

expected for a group of such global significance, the heterokonts

show tremendous biological diversity in terms of number

of species, molecular sequence divergence, and structural

variation (Andersen 1992, 1998, Potter et al. 1997). The term

“heterokont” was first proposed by Luther (1899) for the

xanthophytes and freshwater raphidophytes, but today the

term refers to a larger phylogenetic lineage characterized (in

most cases) by organization of two flagella, the anteriorly

directed one being decorated with minute but elaborate

flagellar hairs (Van den Hoek et al. 1995). Such characteristic

flagella occur at some stage of the life cycle of many, but

by no means all, organisms in the lineage.

Interestingly, many early-branching heterokonts such as

the oomycetes, thraustochytrids, and bicosoecids are colorless

and apparently lack plastids. This may, on the surface,

suggest a nonphotosynthetic ancestry for this group, but a

recent analysis of the 6-phosphogluconate dehydrogenase

(gnd) gene from cyanobacteria and different protists suggests

otherwise. Phylogenetic analysis of gnd indicates that the

parasitic heterokont Phytophtora infestans was likely once

photosynthetic because it retains a gnd gene (of cyanobacterial

affinity) that is closely related to the homologue in photosynthetic

members of this lineage (Andersson and Roger

2002). Weaker evidence for a photosynthetic ancestry comes

from a phylogenetic analysis of plastid-targeted GAPDH (the

gene encoding glyceraldehyde phosphate dehydrogenase)

that groups heterokonts, dinoflagellates, and apicomplexans

in one clade, consistent with these groups having once shared

a common plastid, with losses occurring in ciliates and in

nonphotosynthetic heterokonts (Fast et al. 2001).

The photosynthetic heterokonts have a chromophyte

pigmentation and include such ecologically important groups

as the diatoms and brown algae. The chloroplast typically has

a girdle lamella, a saclike structure that encloses all remaining

lamellae. The chloroplast is almost without exception

connected to the nucleus; that is, the nuclear envelope is

continuous with the plastid endoplasmic reticulum. The storage

product is a b-1,3-linked glucan consisting of only about

25–35 residues, and because of the small molecular size, the

storage product is maintained in a cytoplasmic vacuole. A

large and diverse number of microscopic algal groups make

up the heterokont algae, along with the brown algae, which

are as large and structurally complex as are animals or plants.

The microalgae include the diatoms, which produce silica cell

walls of opaline glass, like that found in glass windows. The

diatoms (with as many as 10 million species!) are the “insects”

of the microbial world (Norton et al. 1996), and diatoms

are probably the major original carbon source of many

petroleum deposits (crude oil, natural gas). The heterokont

algae, with a few noteworthy exceptions (e.g., the diatom

Pseudo-nitzschia and the raphidophyte Chattonella), are rarely

toxic or harmful.

Haptophytes are predominately marine phytoplankters,

including the calcarious-scaled coccolithophores that are

famous for having formed the White Cliffs of Dover. Although

there are probably only a few thousand species of

haptophytes worldwide, these organisms are of great environmental

significance (see Tyrrell 2003). Some species (e.g.,

Emiliania huxleyi, Gephyrocapsa oceanica) can occur in vast

populations, particularly in temperate and polar seas, and are

responsible for substantial primary productivity. As a consequence,

they make a noticeable contribution to the global

carbon cycle and are thought, for example, to have given rise

to the North Sea oil fields. The pigmentation of haptophytes

is similar or identical to that of some heterokont algae, they

also store small b-1,3-linked glucans in cytoplasmic vacuoles,

and there is a membrane continuity between the nuclear

envelope and the plastid endoplasmic reticulum. However,

haptophytes lack flagellar hairs like those found in the

heterokonts. A few (e.g., Chrysochromulina) are harmful or

toxic, killing fish when they occur in bloom conditions.

Dinoflagellates and Apicomplexans:

A Confusion of Plastids

Dinoflagellates show the greatest diversity of plastids of any

eukaryotic group (Delwiche 1999). They are members of the

alveolates, another major eukaryotic lineage comparable with

the heterokonts, plants, animals, and fungi. Many dinoflagellates

(e.g., Alexandrium, Prorocentrum) produce deadly toxins

such as saxitoxin or okadaic acid, and they cause shellfish

poisoning and other types of death or illness to humans and

marine life.

Only about one-half of all dinoflagellates are photosynthetic,

and like the heterokonts, many of the basal branching

lineages are colorless and presently show no structural

sign of having had a plastid in the past. Curiously, members

of the closely related Apicomplexa, a nonphotosynthetic

group of obligate parasites, have a spherical structure composed

of four nested membranes that has been shown to be

a remnant, colorless plastid (Kцhler et al. 1997), which raises

the obvious possibility that the common ancestor of both

apicomplexans and dinoflagellates was equipped with a plastid.

There is at present only scanty evidence that the nonphotosynthetic

basal lineages of dinoflagellates were ever

equipped with a plastid, although tantalizing evidence from

GAPDH suggests dinoflagellates may share a common plastid

origin with heterokonts and haptophytes (Fast et al.

2001). These data should be viewed with caution, however,

both because GAPDH has been notoriously difficult to interpret

and because (as discussed above in the context of

primary plastids), it can be difficult to infer the number of

endosymbiotic events, particularly from limited information.

Most dinoflagellates that are photosynthetic rely on a

characteristic peridinin-pigmented plastid that is surrounded

Algal Evolution and the Early Radiation of Green Plants 127

by three unit membranes. There are, however, a number of

photosynthetic dinoflagellates that show other pigmentation

types (Delwiche and Palmer 1997) and seem to have acquired

their plastids via independent endosymbiotic events involving

green algae, diatoms, cryptophytes, haptophytes, and

other organisms (Delwiche 1999, Tengs et al. 2000, Yoon

et al. 2002). Curiously, some dinoflagellates with plastids

other than the typical peridinin-type plastid are phylogenetically

dispersed as subclades among the peridinin-containing

taxa. This may imply that dinoflagellates with peridinin-type

plastids are less tightly bound to their endosymbiont than are

most algae. There are at least two possible explanations for this

phenomenon. The first involves the peculiar type of rubisco

that performs photosynthesis in peridinin-containing dinoflagellates.

This form II rubisco is probably far more sensitive

to oxygen than is form I rubisco, which is used by all other

oxygenic phototrophs, and may mean that the quantum yield

of photosynthesis in dinoflagellates is lower than in other

organisms. In practice, dinoflagellates can be very difficult

to transport, because they can only survive a short time in

the dark, and this may reflect a relatively low ratio between

photosynthesis and respiration attributable in part to the type

of rubisco they use for photosynthesis. A second possible

explanation involves the unusual genomic structure of dinoflagellate

plastid genomes, which seem to be coded entirely

as single-gene minicircles (Zhang et al. 1999, 2001). This

genomic organization might be less stable than a more typical

chromosomal organization, and this could in turn lead

to more frequent loss of plastids than in other groups. These

and other hypotheses remain to be tested.

A recent study provides a surprising view of dinoflagellate

plastid evolution, suggesting that this lineage may have

undergone a tertiary plastid replacement (i.e., the uptake of

an alga containing a secondary endosymbiont) involving a

haptophyte (Yoon et al. 2002). These data suggest that the

dinoflagellates once likely contained a secondary plastid of

red algal origin (see GAPDH data in Fast et al. 2001) that may

have been shared by all chromalveolates and that was subsequently

replaced by a haptophyte plastid before the radiation

of the photosynthetic dinoflagellates. If this is correct,

and if the chromalveolate hypothesis is correct (Cavalier-

Smith 1999), then the implication would be that there was a

single ancient endosymbiotic event that gave rise to the plastids

of all chromophytes, but that the dinoflagellates lost this

red algal endosymbiont and later reacquired a haptophyte

endosymbiont. Under this scenario, the fucoxanthin-pigmented

dinoflagellates, which have pigmentation and chloroplast

morphology very similar to those of haptophytes

(Tengs et al. 2000), would represent the primitive condition

among plastid-containing dinoflagellates, whereas those with

peridinin-type plastids would represent a derived condition

(Yoon et al. 2002). Together, these data are potentially valuable

for resolving long-standing questions about plastid

evolution and the number of secondary and tertiary endosymbioses,

but they clearly need to be corroborated with

resolved host-cell trees using either or both nuclear and mitochondrial

genes. Several potentially serious analytical problems

exist with the data that have been examined to date, and

at present several competing hypotheses are plausible.

Chlorarachniophyes and Euglenoids:

Secondary Plastids Derived from Green Algae

Although the greatest diversity of organisms with secondary

plastids is found among the organisms that acquired secondary

plastids from red algae, there are also organisms with

secondary plastids derived from green algae (none have yet

been shown to be derived from glaucocystophytes). In a remarkable

display of parallel evolution, the amoeboid chlorarachniophytes

have a green algal plastid in a four-membrane

compartment similar to that of cryptomonads, complete even

to the presence of a nucleomorph (McFadden et al. 1994).

The euglenoids are common in eutrophic freshwater or

estuarine habitats. Like dinoflagellates, only about one-half

of all species are photosynthetic, and the dependence of the

host cell upon the plastid seems to be relatively weak. When

grown at high temperatures and with an external carbon

source, some euglenoids will undergo cell division more rapidly

than the plastid can divide, and the host cell will be

“cured” of its plastid, which will, of course, never regenerate

(Gibbs 1978). This observation was important in early discussions

of the endosymbiotic origin of plastids.

Green Algal Diversity

Green algae are not the most diverse of algal groups (table

9.1), but their presumed close relationship to higher plants

and frequent occurrence in freshwater habitats used by humans

make them one of the more familiar and well-studied

groups of algae. Their plastids are primary and contain

chlorophylls a and b and a variety of accessory pigments

such as carotenes and xanthophylls. Most green algae are microscopic,

but within this diminutive realm they manifest a

relatively broad variety of growth habits, from unicells (e.g.,

Chlamydomonas), to colonies (e.g., Volvox), to unbranched

(e.g., Ulothrix) and branched filaments (e.g., Cladophora), to

true parenchymatous forms (e.g., Coleohaete and Chara). This

variety of morphology was once considered to represent a

progression of forms from simple to complex (e.g., unicells

to large colonies of unicells; unbranched to branched filaments;

small branched clumps to large, plantlike forms;

Smith 1955, Fritsch 1965, Bold and Wynne 1985). It appears,

however, that complex forms have arisen numerous

times from simple ancestors, and numerous reversions to

simple forms further complicate matters (e.g., McCourt et al.

2000). Some green algae are macroscopic, particularly those

128 The Relationships of Green Plants

that occur in intertidal or subtidal marine benthic habitats.

In many cases, these larger forms are coenocytic; that is, their

thalli or plant bodies are composed of ramified networks of

tubes containing a cytoplasm with many nuclei and plastids

but not divided into discrete cells. These tubular modules

may be compressed into spongy large thalli (e.g., Codium)

or be elaborate structures more than a meter in length with

rootlike processes, leaflike assimilators, and spreading connectors

analogous to stolons (e.g., Caulerpa). That such structural

complexity is possible in a thallus that is, in effect, a

single cell challenges conventional thought on the role of

multicellularity in plant development.

Other green algae are microscopic and have cells of more

familiar form, but even these can show a fair measure of complexity

and tissue differentiation. To give one example, Volvox,

which is widely familiar to biology students, is organized

into a sphere of biflagellate cells linked by thin cytoplasmic

strands and often with new thalli developing on the inside

of the sphere. Although often described as a colony, most

species of Volvox show clear functional differentiation among

cells, and development of the thallus includes an elaborate

process of inversion reminiscent of gastrulation, although

these processes are certainly not homologous (Kelland 1977,

Kirk 1999, 2001). Highly complex algae are also found in

the lineage that includes land plants, the Charophyta (or

Streptophyta; described below).

Green algae are nearly ubiquitous, albeit not terribly

abundant in many habitats. Found most often in aquatic

environments from freshwater to marine and hypersaline,

green algae are common and sometimes abundant phytoplankton

in lakes and streams. Many grow attached to

rocks or other hard substrata, although large free-floating

mats of “pond scum” are widely distributed in quiet fresh

waters. Certain groups have colonized subaerial or truly terrestrial

habitats, such as soil interstices, within limestone

rocks, on the surface of desert soils, on bark and leaf surfaces

of some seed plants, or as photosynthetic symbionts

(not endosymbionts) in lichens. Green algae possess a mirror

image distribution compared with two other large groups

of algae, the red and brown algae: the latter two are the dominant

macrophytes in the oceans, with a relative few species

occupying freshwater habitats, whereas green algae are far

more abundant in freshwater. In all these groups there are

marked size differences between marine and freshwater species:

marine greens, like reds and browns, are generally large;

freshwater taxa of these three groups tend to be smaller and

most are microscopic. As is the case with many marine and

freshwater organisms capable of aestivation or dormancy,

freshwater green algae frequently form resistant spores or

bodies through sexual or vegetative means; these structures

are much less common in marine algae.

Large marine green algae include several abundant and

widespread taxa such as the sea lettuce (Ulva) and dead-man’s

fingers (Codium). Members of the Caulerpales can at times

be conspicuous members of reef communities and are raised

by aquarium enthusiasts. It should be noted that a semidomesticated

variety of Caulerpa, of recent infamy, has

wreaked havoc in the Mediterranean as an aggressive exotic

(Meinesz et al. 1993), and it now threatens North America

(Jousson et al. 2000). Although some planktonic green algal

unicells (e.g., Dunaliella) are known in the world’s seas, the

oceanic phytoplankton is primarily dominated by other

groups of algae, notably diatoms and haptophytes (Graham

and Wilcox 2000), along with cyanobacteria.

Instead of basing phylogeny on growth habit (Fritsch

1965), modern approaches have discovered ultrastructural

characters of flagellar structure, particularly the anchorage

of flagella in the cell (O’Kelly and Floyd 1983) and cell division

(Pickett-Heaps 1975) that are morphological synapomorphies

for groups composed of a variety of body forms.

This ultrastructural anatomical consistency contrasts with

a diversity of thallus types, from unicells to colonies to

branched and unbranched filaments. The ultrastructural

approach was pioneered by Pickett-Heaps and Marchant

(1972) and others but was codified by Mattox and Stewart

(1984) in a dramatic restructuring of the systematics of the

green algae. Mattox and Stewart’s hypothesis was that there

are four or five major lineages of green algae, each characterized

by a particular type of motile unicell, and all showing

some degree of morphological convergence of body types that

had previously been considered of overriding taxonomic

importance. This radical new classification that placed emphasis

on ultrastructural features led the way to other studies

of biochemistry (e.g., glycolate metabolism enzymes) and

cell division (e.g., mode of cell wall formation at cytokinesis)

that corroborated Mattox and Stewart’s hypothesis. Although

new data and analyses have led to substantial revision

of the system established by Mattox and Stewart, their treatment

marked a turning point in green algal systematics, and

most modern classifications rely heavily on it.

A new comprehensive treatment of green algal systematics

is badly needed. Although Mattox and Stewart’s (1984)

system established a baseline for modern classification, it is

now nearly 20 years old and was developed in the absence

of any molecular systematic data and without formal phylogenetic

analysis. Molecular data both have confirmed many

elements of their system and have helped reveal a series of

additional surprising arrangements (e.g., a monophyletic

class Trebouxiophyceae, containing many photobionts of

lichens along with other forms). Recent comprehensive treatments

have been presented in response to the need to organize

general textbooks (e.g., Van den Hoek et al. 1995, Graham

and Wilcox 2000). Although these systems include more recent

information, including some molecular phylogenetic data,

and are in some respects excellent, they are fundamentally an

afterthought in the context of broader texts and fail to make

full use of modern data and analytical methods.

In Mattox and Stewart’s (1984) system, there were five

classes of green algae: Charophyceae, Micromonadophyceae

(now known as Prasinophyceae), Ulvophyceae, PleurastroAlgal

Evolution and the Early Radiation of Green Plants 129

phyceae (now Trebouxiophyceae; Friedl 1995), and Chlorophyceae.

Although considerable uncertainty remains as to the

relationships among these groups, most of them seem to

more or less correspond to monophyletic groups, with the

exception of the Prasinophyceae, which are probably paraphyletic

(Fawley et al. 2000), and the Charophyceae, from

which Mattox and Stewart omitted the land plants. The status

of the Ulvophyceae is uncertain, with some data indicating

that there are two or more unrelated elements submerged

within this group (Van den Hoek et al. 1995).

Molecular phylogenetic data indicate that the chlorophytes

as a whole are divided into two primary lineages

(fig. 9.2A; Graham and Wilcox 2000). The first of these is a

clade composed of Mattox and Stewart’s Charophyceae plus

the land plants, a group termed “Streptophyta” by Bremer

(1985) and “Charophyta” by Karol et al. (2001). The latter

term will be used here. This group is characterized by asymmetric

placement of flagella (if present), along with several

other ultrastructural, biochemical, and molecular features.

A few (but not all) charophyte orders perform cell division

in a manner that is strikingly similar to the way it occurs in

land plants. The charophyte lineage will be considered in

more detail below. The second lineage seems to include all

of the other classes recognized by Mattox and Stewart and

thus includes the bulk of the green algae. We refer to that

lineage here as the “Chlorophyta sensu stricto.” The branching

order among these groups is still under investigation.

The Prasinophycae may be the least natural of the classes

recognized by Mattox and Stewart (1984). They are scaly,

unicellular flagellates, a cell morphology that probably represents

the ancestral condition in green algae (Van den Hoek

et al. 1995). In the absence of clear synapomorphic characters

that define the group, it is not surprising that at least

some organisms classified in the Prasinophyceae on the basis

of morphology would be best placed elsewhere. Nonetheless,

the majority of prasinophytes fall within the Chlorophyta

sensu stricto, where they form a paraphyletic grade at the base

of the group (fig. 9.2C; Fawley et al. 2000). It may well be

that there is a great deal of unrecognized biological diversity

among these organisms.

An organism of particular importance is Mesostigma viride,

a unicellular and scaly flagellate that was placed by Mattox

and Stewart (1984) and others among the prasinophytes but

that has some (possibly plesiomorphic) ultrastructural similarities

to charophytes (Rogers et al. 1981). Molecular phylogenetic

analyses support the distinctive nature of Mesostigma

but differ on whether it is sister to the charophytes (Karol

et al. 2001) or to all of known green algal diversity (i.e., to

the clade comprising charophytes and chlorophytes sensu

stricto; fig. 9.2A; Lemieux et al. 2000). Resolving this issue

will require phylogenetic analysis of a rather rich data set,

including genome-scale data from a substantial number of

organisms, but the potential rewards of such a study are great.

Whichever phylogenetic position is correct, Mesostigma is

clearly a pivotal organism in green plant evolution.

The Ulvophyceae have a cruciate flagellar root system

with basal bodies that are offset counterclockwise, and neither

a phycoplast nor a phragmoplast is formed during cell

division. These are likely to be plesiomorphic conditions, and

recent classifications have suggested that these organisms

should be divided into two or more separate groups (Van

den Hoek et al. 1995, Watanabe et al. 2001). The ulvophytes

include both marine and freshwater forms, are highly varied

in form, and include some ecologically and economically

important organisms. Familiar ulvophytes are the sheetlike

Ulva that covers riprap worldwide, and the filamentous

Ulothrix (another polyphyletic genus) that is common in

cold-water environments. Cladophora, a small coenocytic

branched filament, occurs in both freshwater and marine

environments. Cladophora and its close relatives are extremely

widespread, are both economically and culturally important,

and would benefit from additional systematic analysis

(Hanyuda et al. 2002). A close relative of Cladophora,

Figure 9.2. Phylogenetic relationships among the green plants.

(A). All green plants, including Charophyta, Chlorophyta, and

two possible placements of Mesostigma viride. (B) A Japanese

stamp commemorating Aegagropila linnaei (“marimo balls”).

(C) Primary lineages in Chlorophyta. (D) Primary lineages in

Charophyta. (E) The “liverworts basal” hypothesis for the

branching order among the four early-diverging lineages of land

plants. (F) The competing “hornworts basal” hypothesis (by

C. F. Delwiche).

Coleochaetales

Charales

Liverworts

Hornworts

Mosses

Vascular

Chlorokybales

Klebsormidiales

Zygnematales

Coleochaetales

Charales

Land Pl.

Coleochaetales

Charales

Liverworts

Hornworts

Mosses

Vascular

e f

c d

a

Charophyta

Chlorophyceae

Ulvophyceae

"Prasinophytes"

Charophyta

Trebouxiophyceae

Chlorophyta Charophyta

? ? Mesostigma

b

130 The Relationships of Green Plants

Aegagropila, grows into the famous marimo balls of Lake Akan

in Japan and is probably the only alga to have been designated

a national treasure and commemorated on a postage

stamp (fig. 9.2B). Also classified among the ulvophytes are

huge and elaborate coenocytes of Bryopsis, Caulerpa, and their

relatives, and the microscopic but highly complex and fully

terrestrial Trentepohliales (Chapman et al. 2001, Thompson

and Wujek 1997).

Members of Chlorophyceae are mostly freshwater, have

a cruciate microtubular root system with basal bodies that

are either directly opposed or offset clockwise, and at least

in most cases form a distinctive structure called a “phycoplast”

during cell division. The chlorophytes include such

familiar taxa as Chlamydomonas, an important model organism

(Harris 1989), and Volvox, also a model system and famous

for its beautiful spherical form. Also in this group are

Hydrodictyon, an elaborate net-shaped organism that was

mentioned in Chinese literature nearly 2000 years ago (Tilden

1937); Characiosiphon, a multinucleate coenocyte; and highly

differentiated filamentous algae such as Stigeoclonium,

Draparnaldia, and Fritschiella.

The Trebouxiophyceae are mostly small unicells that live

in freshwater or terrestrial environments, but some are filamentous

or even organized into bladelike sheets (e.g.,

Prasiola). A key model system in the study of the physiology

and biochemistry of photosynthesis was a trebouxiophycean

species of Chlorella, a genus that molecular phylogenetic studies

indicate is grossly polyphyletic and is currently undergoing

revision (Huss et al. 1999). Lichen phycobionts are often

trebouxiophytes, and they are rather common in terrestrial

habitats both in lichenized and unlichenized states (Friedl

1995, Lewis and Flechtner 2002).

Green Algae and the Colonization of the Land

Although a great diversity of algae, green and otherwise, inhabit

the terrestrial environment (Lewis and Flechtner 2002),

a single monophyletic group characterized by a life cycle that

involves an alternation of multicellular diploid and haploid

generations and a syndrome of ultrastructural and biochemical

features. This group dominates the land in terms of biomass,

primary production, ground coverage, and known

biological diversity among phototrophs. This lineage, referred

to here as “land plants” and known more formally as “embryophytes”

in reference to their life cycle, are from a phylogenetic

perspective green algae that have become adapted to

life in the terrestrial environment (Karol et al. 2001).

Green algae as a whole contain chlorophylls a and b, store

starch inside the chloroplast, have cellulosic cell walls, and

possess a unique star-shaped structure at the flagellar transition

zone (Graham 1993). These features are shared with

land plants, and consequently even before biochemical and

ultrastructural similarities were known in detail, the green

algae were considered ancestral to land plants (Bower 1908,

Fritsch 1965). However, thought on the identity of the closest

relatives of land plants has changed considerably as

knowledge of cell biology, ecology, and phylogeny of the

green algae has developed (Van den Hoek et al. 1995). In the

absence of phylogenetic information that is independent of

morphology, heterotrichous forms such as Fritschiella, with

prostrate rhizoids and upright, branched structures, were

thought to represent a stage in the evolutionary series from

unicells to land plants (Singh 1941). At the same time it was

recognized that there was ample opportunity for convergent

evolution, and all classifications were viewed as tentative, and

probably artificial (Tilden 1937, Fritsch 1965). The classical

sequence of increasing grades of developmental complexity

(Smith 1955, Bold and Wynne 1985), which runs from permanently

flagellate unicells, through coccoid forms with

motile stages, unbranched and branched filaments, to complex

thalli composed of layers of cells organized in three dimensions

has proven to have some truth to it, but various

forms of complexity have evolved independently in several

lineages. Consequently, study with the light microscope

could identify a number of candidate taxa that seemed to be

relevant to the origin of land plants, but was not effective at

choosing among these.

With the rapid accumulation of ultrastructural data in

the 1970s and molecular data in the 1980s and 1990s, the

picture that has emerged places land plants firmly within the

Charophyta (Mishler and Churchill 1985, Bremer et al. 1987,

Graham et al. 1991, McCourt 1995, Graham and Wilcox

2000, Karol et al. 2001). The charophytes are remarkably

diverse structurally and display the full range of classical

grades of complexity. Interestingly enough, the phylogeny

within this group seems to follow the classical developmental

sequence rather well, albeit with some reversals and parallelism

(McCourt et al. 2000, Karol et al. 2001, Delwiche

et al. 2002). Because of their structural diversity, although

several charophytes had been discussed with respect to the

origin of land plants (e.g., Zygnematales, Coleochaetales,

Charales), these taxa were rarely classified together before the

advent of ultrastructural and molecular phylogentic data, and

even today some authorities shy away from treating them as

an integrated whole (e.g., Wehr and Sheath 2003).

Graham (1993) termed these green algae “charophyceans,”

derived from Mattox and Stewart’s (1984) class

Charophyceae. Rather than substitute a class-based name

for a paraphyletic group of algae, however, we use the term

“charophytes” informally, or the division name “Charophyta”

to refer to the whole clade including land plants (Karol et al.

2001). These terms have their own limitations—historically

“charophytes” has referred to the Charales and related fossil

forms (Tappan 1980). Bremer and Wanntorp (1981) recognized

the importance of naming monophyletic groups and

used Jeffrey’s (1967) term “Streptophyta.” This term refers

to the twisted shape of the sperm and was originally used

to refer to the clade composed of embryophytes and the

Charales (Jeffrey 1967). More recently, the streptophytes

Algal Evolution and the Early Radiation of Green Plants 131

have been taken to include other algae on the plant lineage

as well, but we prefer the term in its original sense and use

“Charophyta” to refer to the more inclusive group. The

groups that make up the charophytes include several previously

recognized orders, each of which is monophyletic

(fig. 9.2D): Chlorokybales, Klebsormidiales, Zygnematales

(including Desmidiaceae), Coleochaetales, and Charales,

plus, of course, land plants.

As noted above, the unicellular flagellate Mesostigma (fig.

9.3F) is apparently a basal branch within the charophytes

(Karol et al. 2001), although other analyses question this

genus’s placement (Lemieux et al. 2000, Turmel et al. 2001).

To further complicate matters, analyses of rRNA weakly support

a topology that places Mesostigma in a clade with the

genus Chaetosphaeridium (Marin and Melkonian 1999). This

topology differs from that found in analyses of proteincoding

genes (Karol et al. 2001, Bhattacharya et al. 1998) but

does not seem to be a spurious result. The Chlorokybales

(fig. 9.3E) are a monotypic order consisting of the species

Chlorokybus atmosphyticus, a rare soil alga that forms small

packets of cells embedded in mucilage. The Klebsormidiales

(fig. 9.3D) include the genera Klebsormidium, Interfilum, and

Entransia; they are unbranched filaments and are common

in freshwater and terrestrial environments. Klebsormidium is

frequently a component of the green film that accumulates

on sheltered walls and structures in warm, moist climates and

of desert crusts (Lockhorst 1996, Lewis and Flechtner 2002).

Members of Zygnematales (fig. 9.3C) are common freshwater

algae including both filamentous (e.g., Spirogyra) and

unicellular (e.g., Micrasterias) forms. In this group the unicellular

form seems to be a derived condition, with some

species having independently reacquired a filamentous

growth form (e.g., Desmidium; McCourt et al. 2000). No

member of Zygnematales has any flagellate stage, and consequently

they indulge in a distinctive form of sexual reproduction

termed “conjugation” that does not require motile

cells. Although the filamentous Zygnematales are often considered

to be unbranched, some branching is associated with

holdfast formation, and the conjugation tube is developmentally

similar to a branch (Fritsch 1965).

Coleochaetales (fig. 9.3B) include the genera Coleochaete,

Chaetosphaeridium, and the exquisitely rare Awadhiella

(Delwiche et al. 2002, Nandan Prasad and Kumar Asthana

1979). They form complex branched thalli that are found

living on submerged rocks and vegetation worldwide. Reproduction

is oogamous, and in Coleochaete there are elaborate

developmental changes that occur in response to the fertilization

of the egg. Members of the genus Coleochaete show

many structural and biochemical features that resemble land

plants, including phragmoplastic cell division, plasmodesmata,

plantlike peroxysomes, and the production of more

than four meiotic products from the zygote (Graham 1993,

Delwiche et al. 2002). The thalli have a distinct three-dimensional

organization, and in some the laterally adjacent cell

files are so tightly adjoined that the tissue organization has

been viewed as a simple parenchyma (Graham 1993). Vegetative

growth occurs by cell division in very specific locations

in the thallus, depending upon the species (Delwiche

et al. 2002). Typically cell divisions that increase the length

of a filament occur in the apical cell of the filament, and

branching occurs either in the apical cell or in the second or

third cell from the apex. Because of these similarities to land

plants, Coleochaete has long been discussed in the context of

the origin of land plants (e.g., Bower 1908), but many of these

Figure 9.3. Representative species in Charophyta. (A) Chara

globularis (Charales) KGK0044, showing cortication of developing

oogonium and antheridium in the background. Freshwater. Scale

bar, 1 mm. (B) Coleochaete pulvinata (Coleochaetales) CFD 56a6,

showing early developmental stage of zygote cortication.

Freshwater. Scale bar, 30 mm. (C) Spirogyra maxima (Zygnematales)

UTEX 2495, showing conjugation tubes and partially

developed zygotes. Freshwater. Scale bar, 100 mm. (D) Klebsormidium

nitens (Klebsormidiales) SAG 335–2b, showing a single

parietal chloroplast per cell. Moist soils or freshwater. Scale bar,

30 mm. (E) Chlorokybus atmosphyticus (Chlorokybales) UTEX

2591 growing in characteristic sarcinoid packets of cells. Moist

soils. Scale bar, 10 mm. (F) Mesostigma viride (Mesostigmatales)

SAG 50-1. Note surface scales visible on upper portion of cell;

flagella are not visible, but would emerge from the medial groove

in direction of viewer. Freshwater. Scale bar, 10 mm.

a b

c d

e f

132 The Relationships of Green Plants

characters are also found in the Charales and not all are uniformly

present in Coleochaetales.

Charales (fig. 9.3A) are large and complex organisms with

a conspicuous node/internode organization reminiscent of

the more developmentally complex land plants. However, the

thallus structure is fundamentally different from that of land

plants, with the internodes formed from a single giant cell,

in some cases secondarily covered by corticating filaments

(Graham and Wilcox 2000). Reproduction is oogamous, and

the zygote, which may be a millimeter or more in diameter,

is surrounded by a thick sporopollenin wall, which, in addition

to heavy calcification in many forms, ensures that

oopores and associated structures often form well-preserved

fossils (Delwiche et al. 1989, Feist and Feist 1997). As a consequence,

the Charales have a rich fossil record extending

back well more than 400 million years (Grambast 1974,

Tappan 1980). The Charales have a distinctive and complex

form, with elaborate multicellular antheridia and oogonia

covered with sterile jacket cells, early development consisting

of protonemal filaments with subsequent formation of

nodes and internodes, well-differentiated rhizoids, stolonlike

growth, and a variety of other developmental responses to

the environment. Because of these striking apomorphies,

many authors have separated them into a division or class of

their own. Although many of these features are highly specialized

and clearly evolved independently of their analogs

in land plants (Fritsch 1965, Graham 1993), there are enough

features shared with land plants that, like Coleochaetales,

Charales has long featured in the search for the sister taxon

to land plants.

As noted above, members of Charales are now thought to

be the closest living relatives of land plants, with a recent

multigene analysis supporting a strong sister-group relationship

between these two groups (Karol et al. 2001). This analysis

is the first to provide robust support for a sister taxon to

land plants. If accurate, this arrangement suggests that the common

ancestor of Charales and land plants exhibited several

traits: branching thallus, oogamy, branched rhizoidal structures,

a complex sperm, and a freshwater habitat. The Charales have

clear developmental patterning in three dimensions, and the

organization of cells in the nodes is often considered to be

parenchyma, but it does not have the degree of complexity and

tissue differentiation found in land plants. Growth occurs by

division of an apical cell with a single cutting face.

A freshwater origin for land plants is perhaps not surprising,

given that terrestrial animals also likely originated there.

The availability of a robust phylogeny for the charophytes also

helps resolve a long-standing issue in botany, the origin of the

life history of land plants (e.g., Bower 1908, Tilden 1937,

Fritsch 1965, Mishler and Churchill 1985, Graham 1993). All

charophytes except for land plants have a life cycle in which

the vegetative cells are haploid and the only diploid stage is

the zygote (i.e., haplontic), so the life cycle of land plants

almost certainly arose by intercalation of a multicellular diploid

phase in a haplontic life cycle.

What other conclusions can be made about the origin of

land plants from an understanding of their placement within

Charophyta? Graham (1993) has discussed in detail the features

that unite Charales, Coleochaetales, and other charophyte

algae with land plants, as well as those features that

are distinctive to land plants. Among the characters that are

unique to land plants (and fairly universal among them) are

an alternation of generations in the life cycle; tissue composed

of cells organized in three dimensions (“parenchyma”) and

with fairly small cells; large size overall, which may be dependent

upon the preceding; extensive tissue differentiation

and specialization; a well-developed cuticle; distinctive and

complex multicellular antheridia and archegonia; numerous

spores with a thick sporopollenin coat; and a number of technical

biochemical and ultrastructural characters. Although

the gap between the “algal” charophytes and land plants is

smaller than some have suggested, there are clearly a number

of features that are unique to the land plants. These features,

and probably some combination of them, permitted

this clade to undergo dramatic diversification and to inhabit

a wide range of habitats. This is particularly interesting in

view of the fact that several other charophytes are partially

or wholly terrestrial (e.g., Chlorokybus, Klebsormidium), and

yet the embryophytes overwhelmingly dominate the land.

The embryophytes have a known fossil record that is only

slightly deeper than that of Charales and show a degree of

molecular divergence that is comparable with the other

charophycean orders. Perhaps it is primarily their ability to

grow large that has given them command of the terrestrial

environment.

The Land Plants: Terrestrial Green Algae

Land plants are the unchallenged masters of the terrestrial

environment. They are found in nearly every terrestrial environment

with the exception of the high alpine and polar

regions and severe deserts. Because of a high degree of tissue

differentiation and sophisticated adaptations to water

management, some land plants are able to survive even in

very dry environments by relying on water storage, tap roots

that can mine deep water, or life cycles that involve long

periods of dormancy. Algae that are not part of the land plant

clade can be found living in similarly dry environments (e.g.,

Klebsormidium; Lewis and Flechtner 2002), but these survive

by dormancy and remarkable desiccation tolerance (Oliver

et al. 2000) and do not achieve the biomass found in land

plants.

Although the most conspicuous members of the terrestrial

flora are large vascular plants, these are relatively derived

members of the clade, and their extreme adaptations to the

terrestrial environment obscure some of the fundamental

similarities of land plants to other charophytes. Early

branches in the land plant lineage include a number of small

and inconspicuous organisms without fully developed vasAlgal

Evolution and the Early Radiation of Green Plants 133

cular tissue and with reproductive mechanisms that require

the availability of liquid water. Although the early-diverging

land plants have a life cycle involving an alternation of multicellular

haploid and diploid generations that is characteristic

of land plants, there are three lineages, sometimes

artificially lumped together as “bryophytes,” in which the

conspicuous, long-lived, and vegetatively spreading generation

is haploid (the “gametophyte” after its ability to produce

gametes), and the diploid stage (the “sporophyte” after its

ability to produce spores) is simple, unbranched, generally

short-lived, and incapable of surviving independently of the

gametophyte.

The liverworts have relatively simple gametophytes,

which may be flattened thalli with dichotomous branching

and no leaves or dorsiventral stems with filmy leaves that are

only a single layer of cells thick. The cells have multiple, discoidal

chloroplasts without pyrenoids, similar to those of

Charales and all other land plants except the hornworts. In

the complex thalloid liverworts, internal air chambers communicate

with the atmosphere by means of a pore that is

surrounded by a ring of specialized cells but that does not

actively regulate the flow of gasses into the chamber. A cuticle

is present but is typically very thin and does not provide

robust protection against drying. The tissue is well

organized in three dimensions, and growth occurs by division

of an apical cell with three or more cutting faces. The

sporophyte is very simple, without pores or stomata, and it

follows a fixed developmental trajectory (i.e., determinate).

Liverworts are fairly common in wet environments around

the world but are rarely conspicuous. There are roughly 8000

species and 330 genera, and they show considerable diversity

of structure and ecology, but all are small plants that

require at least periodically wet conditions to thrive

(Schofield 1985).

The hornworts are superficially similar to the thalloid

liverworts and have often been confused with them. However,

the hornworts differ from liverworts in a number of key

characters and are almost certainly a monophyletic group.

Like thalloid liverworts, the gametophytes are flattened structures

without a distinct stem and leaves and radiate with irregular

branching from the point of germination to form a

more or less disk-shaped structure. The cells of most species

have a single large chloroplast with a pyrenoid, similar

to Coleochaetales and some other charophytes, but quite

unlike Charales or other land plants (Graham and Kaneko

1991). Many species have a permanent symbiotic relationship

with a nitrogen-fixing cyanobacterium, Anabaena. The

sporophytes are dramatically different from those of the liverworts,

with tracheophyte-like stomata capable of opening and

closing, tissue specialized for water conduction, and indeterminate

growth. In some cases the sporophyte seems to

become largely independent of the gametophyte, and it may

survive for a considerable period of time (a year or more).

Hornworts are moderately rare but can be found on bare soil

or rocks on stream margins as well as wet cliffs and road cuts.

There are probably fewer than 500 species in six or seven

genera (Schofield 1985).

The mosses are a large, widespread, and familiar group.

The gametophyte is organized into distinct stems and leaves

with an elaborate and precisely coordinated architecture.

Many species have a fairly well-developed vascular system.

Taken together, these features give the gametophyte of

mosses a structure that is strongly reminiscent of the architecture

of vascular plants, but it is important to remember

that the gametophytes of vascular plants do not have a similar

form. Consequently, this similarity is very likely the result

of convergent evolution or, possibly, a heterochronic

shift. The sporophyte of mosses is unbranched and determinate

but is structurally quite complex, with stomata, a

specialized aperture to release the spores, conducting tissue,

and, depending upon the species, a variety of teeth and other

specialized structures. Mosses are often inconspicuous but

are nearly ubiquitous, extending their range far into alpine,

arctic, and desert regions where few other land plants occur.

The species that occupy these extreme environments rely on

great desiccation tolerance and rapid recovery to take advantage

of brief periods of moisture availability and moderate

temperatures to complete their life cycles. There are about

10,000 species of moss in roughly 700 genera (Schofield

1985).

Although the liverworts, hornworts, and mosses each

almost certainly constitute a monophyletic group, the

branching order among these groups in relation to the fourth

land plant lineage, the tracheophytes (for discussion of this

major group of land plants, see Pryer et al., ch. 10 in this vol.),

remains a topic of active debate. Classical botanical thought

considered a wide range of possibilities and often declined

to speculate on the relationships among them (e.g., Bold

1967), or arbitrarily grouped them into a single heterogeneous

taxon. Cladistic analyses based on morphological data

suggested that the three lineages formed a ladderlike grade,

with liverworts most basal, hornworts next, and mosses

most closely related to a monophyletic tracheophyte clade

(fig. 9.2E), although a few analyses reversed the branching

order of liverworts and hornworts, placing hornworts most

basal (reviewed in Bremer et al. 1987). Early molecular phylogenetic

analyses were mostly based either on a single rRNA

gene or on the plastid gene rbcL, and although there was

strong support from many sources for monophyly of land

plants as a whole and of vascular plants, the branching order

among the three “bryophyte” lineages varied greatly from

analysis to analysis, with almost every possible branching

order represented (Chapman and Buchheim 1992, Mishler

et al. 1994, Kranz et al. 1995). For a time the matter appeared

settled, with most authorities accepting the liverwort/hornwort/

moss sequence (fig. 9.2E), but Nickrent et al. (2000)

presented an analysis based on four genes (rbcL, and SSU

rDNA from the chloroplast, mitochondrial, and nuclear genomes)

that reopened this question. In this analysis they

investigated the contributions of each of the individual genes

134 The Relationships of Green Plants

to the analysis, as well as differences in rate at different codon

positions, evidence for saturation, and the results of several

analytical methods. From this they concluded that rRNA

genes supported a “hornworts basal” topology (fig. 9.2F) and

suggested that prior analyses based on rbcL had favored a

“liverworts basal” topology (fig. 9.2E) because of analytical

artifacts traceable to saturation at third-codon positions. This

is, however, unlikely to be the last word on the matter. In

addition to several potential morphological synapomorphies

such as conducting tissue, mosses and tracheophytes alone

share isoprene emission (Hanson et al. 1999). Mosses, hornworts,

and tracheophytes share an apparently derived ability

to conjugate auxin (Sztein et al. 1995), as well as three

synapomorphic mitochondrial introns (Qiu et al. 1998).

Furthermore, a recent analysis based on 11,518 amino acid

sites from the 52 proteins encoded by all green plant chloroplast

genomes placed liverworts as the first diverging group

of land plants (Kugita et al. 2003). Although this latter analysis

is based solely on chloroplast genes and would benefit

greatly from availability of chloroplast genome sequences

from a larger number of organisms, it suggests that the topology

shown in figure 9.2E is not simply an artifact peculiar

to the gene rbcL. In the future, “total evidence” analyses

are needed to combine all relevant genomic, biochemical, and

morphological data, from a sufficient sample of taxa representing

all major lineages (Mishler 2000).

Fortunately, with the rapid collection of genome-scale

DNA sequence data from diverse organisms, it is likely that

it will be possible to directly address this question and many

others with large and well-curated molecular data sets in

the near future. High-throughput sequencing projects have

begun to take advantage of phylogenetic information to select

organisms for study, and it appears that substantial

quantities of sequence information will soon become available

from some of the groups that have been largely

neglected to date. It is important to recognize that some unfamiliar

organisms are of great importance and that there

is potentially a great deal to be gained by studying such

organisms.

Acknowledgments

This work was supported in part by National Science Foundation

grants DEB-9978117 and MCB-9984284 and Green AToL

grant DEB-0228729. Tsetso Bachvaroff, John Hall, Ken Karol,

Jeff Lewandowski, and other members of the Delwiche lab

provided useful commentary. Dan Nickrent participated in

useful discussions and provided access to unpublished data.

Tashi Wangchuk provided “chu rhu” for analysis and snacking.

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