Streptophyte algae and the origin of embryophytes

Annals of Botany 103: 999 –1004, 2009
doi:10.1093/aob/mcp044, available online at www.aob.oxfordjournals.org
BOTANICAL BRIEFING
Streptophyte algae and the origin of embryophytes
Burkhard Becker* and Birger Marin*
Botanisches Institut, Universität zu Köln, Gyrhofstr. 16, 50931 Köln, Germany
Received: 11 November 2008 Returned for revision: 15 December 2008 Accepted: 6 February 2009 Published electronically: 8 March 2009
Key words: Chlorophyta, Streptophyta, Embryophyta, Charales, Coleochaetales, Zygnematales, viridiplant
phylogeny, land plants, genome evolution, freshwater adaptation, sporophyte origin, diversification, extinction.
IN T RO DU C T IO N
The Viridiplantae (Latin for ‘green plants’) include all green
algae (Chlorophyta and streptophyte algae) and embryophyte
plants. They represent a monophyletic group of organisms,
which display a surprising diversity with respect to their morphology, cell architecture, life histories and reproduction, and
biochemistry. The colonization of terrestrial habitats by descendents of streptophyte algae started approx. 470 – 450 MY
ago (Ordovician period; reviewed in Sanderson et al., 2004),
and was undoubtedly one of the most important steps in the
evolution of life on earth (Graham, 1993; Kenrick and
Crane, 1997; Bateman et al., 1998). The evolution of the
various groups of land plants (embryophytes ¼ bryophytes,
pteridophytes and spermatophytes) resulted in our current terrestrial ecosystems (Waters, 2003) and significantly changed
the atmospheric oxygen concentration (Berner, 1999; Scott
and Glasspool, 2006). In this Briefing we will first describe
recent progress in our understanding of the phylogenetic
relationships within the Viridiplantae with a focus on streptophyte algae. We will then present new results and ideas in
* Both authors contibuted equally to this work. For correspondence,
e-mail [email protected] or [email protected]
molecular physiology and genome evolution as well as
primary adaptations and evolutionary trends, which were
important for the origin of true land plants.
P H Y LOG E NY OF T HE S T R E P TO P H YTA
The phylogenetic relationships within the Viridiplantae were
summarized by Lewis and McCourt (2004). Most phylogenetic relationships proposed at that time appear to be still
valid. The Viridiplantae split early into two evolutionary
lineages: Chlorophyta and Streptophyta (Fig. 1A). This split
occurred about 725– 1200 MY ago, according to different estimates by molecular clock methods (Hedges et al., 2004; Yoon
et al., 2004; Zimmer et al., 2007). Within the streptophyte
algae six morphologically distinct groups were recognized:
the flagellate Mesostigmatales, sarcinoid Chlorokybales, filamentous (unbranched) Klebsormidiales, the Zygnematales
(characterized by conjugation as the method of sexual reproduction and total absence of flagellated cells), and the two
morphologically most complex groups, the Charales (stoneworts) and Coleochaetales, both of which are characterized
by true multicellular organization (with plasmodesmata) of
parenchyma-like thalli or branched filaments with apical
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† Background Land plants (embryophytes) evolved from streptophyte green algae, a small group of freshwater
algae ranging from scaly, unicellular flagellates (Mesostigma) to complex, filamentous thalli with branching,
cell differentiation and apical growth (Charales). Streptophyte algae and embryophytes form the division
Streptophyta, whereas the remaining green algae are classified as Chlorophyta. The Charales (stoneworts) are
often considered to be sister to land plants, suggesting progressive evolution towards cellular complexity
within streptophyte green algae. Many cellular (e.g. phragmoplast, plasmodesmata, hexameric cellulose synthase,
structure of flagellated cells, oogamous sexual reproduction with zygote retention) and physiological characters
(e.g. type of photorespiration, phytochrome system) originated within streptophyte algae.
† Recent Progress Phylogenetic studies have demonstrated that Mesostigma (flagellate) and Chlorokybus (sarcinoid) form the earliest divergence within streptophytes, as sister to all other Streptophyta including embryophytes. The question whether Charales, Coleochaetales or Zygnematales are the sister to embryophytes is still
(or, again) hotly debated. Projects to study genome evolution within streptophytes including protein families
and polyadenylation signals have been initiated. In agreement with morphological and physiological features,
many molecular traits believed to be specific for embryophytes have been shown to predate the Chlorophyta/
Streptophyta split, or to have originated within streptophyte algae. Molecular phylogenies and the fossil
record allow a detailed reconstruction of the early evolutionary events that led to the origin of true land
plants, and shaped the current diversity and ecology of streptophyte green algae and their embryophyte
descendants.
† Conclusions The Streptophyta/Chlorophyta divergence correlates with a remarkably conservative preference for
freshwater/marine habitats, and the early freshwater adaptation of streptophyte algae was a major advantage for
the earliest land plants, even before the origin of the embryo and the sporophyte generation. The complete
genomes of a few key streptophyte algae taxa will be required for a better understanding of the colonization
of terrestrial habitats by streptophytes.
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Becker & Marin — Streptophyte algae and the origin of embryophytes
A
Chlorophyta
Streptophyta
B
Chlorophyta
Chlorophyceae
Trebouxiophyceae
Ulvophyceae
Chlorodendrales
Pseudoscourfieldiales
Coccoid prasinophytes
Mamiellales
Pyramimonadales
Mesostigmatophyceae
Chlorokybophyceae
Klebsormidiophyceae
Zygnemophyceae
Coleochaetophyceae
Charophyceae
Embryophytes
Mesostigmatales
Chlorokybales
Klebsormidiales
Zygnematales
Coleochaetales
Streptophyta
Charales
Embryophytes
Prasinophytes
Streptophyte algae
F I G . 1. Phylogenetic relationships among the major lineages of the
Viridiplantae. Branches indicated by dotted lines are not well supported. (A)
According to Lewis and McCourt (2004), and (B) based on unpublished,
ongoing work by the authors. Some of the class names used by Lewis and
McCourt (2004) have never been validly described, and for this reason we
use order designations in (B) and throughout the text. The informal term ‘prasinophytes’ is commonly used for scaly green flagellates (Mesostigmatales and
basal Chlorophyta).
growth and oogamous sexual reproduction. The genus
Spirotaenia, usually classified as member of the
Zygnematales, probably represents an independent lineage
separate from the Zygnematales (Gontcharov and Melkonian,
2004). The branching order among streptophyte algae was
not resolved in 2004 and has subsequently been addressed
by several publications, using rRNA and/or rbcL genes
(e.g. Hall et al., 2008), complete plastid genomes (e.g.
Turmel et al., 2005, 2006), or phylogenomic approaches
(Rodriguez-Ezpeleta et al., 2007). However, in phylogenetic
trees obtained to date the divergence of streptophyte algae is
still poorly resolved. The only major exception refers to the
phylogenetic position of Mesostigma. Called an enigma in
2004 (Lewis and McCourt, 2004), recent work has now
firmly established that Mesostigma forms a clade with
Chlorokybus (Fig. 1B), both representing the earliest divergence of streptophyte algae (Lemieux et al., 2007;
Rodriguez-Ezpeleta et al., 2007). In contrast, the question as
to which group represents the sister to the embryophytes is
far from being settled. In many illustrations depicting the
G E NO M E E VOL U T I ON W I T H IN
S T R E P TO P HY T E S A ND T HE U NI QU E NE S S
O F E M B RYO P H Y T E S
Public literature databases (e.g. Web of Science) contain many
references to proteins/genes that are considered to be plantspecific. Unfortunately, the term ‘plant-specific’ is often misleading, and merely indicates that a protein is only known
from land plants (embryophytes) or spermatophytes, and therefore the term spermatophyte- or embryophyte-specific would
be much better. Horizontal gene transfer into embryophytes
is extremely rare (Richardson and Palmer, 2006; Huang and
Gogarten, 2008; Keeling and Palmer, 2008), with the exception of mitochondrial genes transferred from one plant to
another (Richardson and Palmer, 2006; Keeling and Palmer,
2008), and an ancient horizontal or endocytic gene transfer
from a chlamydial-type bacterium (Huang and Gogarten,
2007; Becker et al., 2008) to the ancestor of Plantae
(Glaucoplantae, Rhodoplantae and Viridiplantae). Therefore,
nearly all the genes present in extant embryophytes were inherited from the eukaryotic host or the cyanobacterial endosymbiont of the common ancestor of all Plantae (Martin et al.,
2002). Thus, we should be very careful with terms such as
‘plant-specific gene’ (in the sense of embryophyte- or
spermatophyte-specific) until at least a single genome of a
streptophyte alga is completely sequenced.
We are convinced that many plant ‘innovations’ will actually turn out to be innovations of the streptophyte algae (or
the viridiplants), once complete streptophyte genomes
become available and/or comparisons include chlorophyte
genomes (Ostreococcus, Chlamydomonas). Recent examples
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Ulvophyceae
Chlorophyceae
Trebouxiophyceae
Chlorodendrales
Coccoid prasinophytes
Nephroselmidophyceae
Pycnococcaceae
Coccoid prasinophytes
Mamiellales
Pyramimonadales
evolution of streptophyte algae and land plants in textbooks
(e.g. Raven et al., 2005) or review articles (Lewis and
McCourt, 2004; McCourt et al., 2004; Qiu, 2008), the
Charales (stoneworts) are shown as sister to the embryophytes.
This is supported by an analysis of four genes encoded by
three cellular compartments (Karol et al., 2001). However, in
recent phylogenetic analyses, either the Charales or alternatively the Coleochaetales or Zygnematales are found as
sisters to the land plants, depending on the gene(s) analysed
and the taxon sampling, but none of these topologies has convincing statistical support. Analyses of chloroplast genomes
tend to support the Zygnematales or a clade consisting of the
Zygnematales and the Coleochaetales as sister to the embryophytes (Turmel et al., 2007). In contrast, in both our ongoing
work using a phylogenomic approach [similar to the one used
for Mesostigma (Rodriguez-Ezpeleta et al., 2007) using five
streptophyte algae including Chara and Coleochaete;
S. Wodniok, M. Melkonian, H. Philippe and B. Becker,
University of Cologne, Germany, unpubl. res.], or using complete rRNA operons of the nuclear and plastidic genomes
(using ten streptophyte algae; B. Marin and M. Melkonian,
University of Cologne, unpubl. res.) we observed the
Charales as sister to embryophytes, albeit with low statistical
support. We are currently trying to test these results by
improved taxon sampling (rRNA trees) and the inclusion of a
larger number of genes ( phylogenomics). The phylogenetic
relationships between the streptophyte algae we both currently
agree on are depicted in Fig. 1B.
Becker & Marin — Streptophyte algae and the origin of embryophytes
TA B L E 1. Examples of ‘plant-specific’ proteins recently found in
streptophyte and/or chlorophyte algae
Protein*
Arabinogalactan-proteins
BIP 2
Class II homeodomain-leucin zipper
Embryophyte type of cellulose synthase Ces A
Endotransglucosylase (XET; MXE)
GAPDHB
MIKc-type MADS-box
Reference
Eder et al. (2008)
Nedelcu et al. (2006)
Floyd et al. (2006)
Roberts and Roberts (2004)
Van Sandt et al. (2007),
Fry et al. (2008)
Petersen et al. (2006),
Simon et al. (2006)
Tanabe et al. (2005)
* BIP, binding protein; GAPDHB, glyceraldehyde 3-phosphate
dehydrogenase isoform B; MXE, mixed-linkage-glucan: xyloglucan
endotransglucosylase; XET, xyloglucan endotransglucosylase.
N E W HY POT H E S E S A B O UT T H E OR IG IN OF
E M B RYOP H Y T E S A N D T H E E VO L U T I O N
O F S T R E P TOP H Y T E AL G AE
Why were terrestrial environments conquered by only a single
lineage of ‘true land plants’, which evolved from streptophyte
green algae?
Given the diversity in morphology, cell architecture, life histories and reproduction, and biochemistry among photoautotrophic eukaryotes, it is surprising that ‘true land plants’
evolved uniquely within the streptophytes. Terrestrial (micro)
algae are present in several other algal groups (e.g. Cyanobacteria, diatoms, Chlorophyceae and Trebouxiophyceae);
however, none of these algae ever rose above their substrate.
Macroalgae (Ulvophyceae, red and brown seaweeds) became
dominant players in marine habitats but never invaded terrestrial ecosystems. Why were streptophytes so successful in the
colonization of terrestrial habitats? We suggest that streptophyte algae were physiologically pre-adapted to terrestrial
existence by their primary freshwater life style, in contrast to
their marine sister lineage, i.e. Chlorophyta (Fig. 2A).
Freshwater adaptation allowed a slow and gradual move
towards moist habitats in the proximity of water, and ultimately the colonization of dry land, dependent on rainwater.
In contrast, the ecological gradient between marine and terrestrial habitats is very sharp (mainly salinity; but also extremes
of temperature, exposure to high irradiance, dehydration, ultraviolet radiation; Smith and Smith, 2006), and apparently did
not enable the successful colonization of terrestrial regions by
marine algae. Interestingly, the animal groups with major
players in terrestrial habitats (insects and vertebrates) originated
in freshwater environments and are still completely (amphibians and insects) or largely (reptiles, birds and mammals)
absent from the oceans (Vermeij and Dudley, 2000; Glenner
et al., 2006). The same holds for streptophyte algae (strict freshwater preference, with only a few Charales that tolerate brackish
habitats), and for the Embryophyta with primary terrestrial
origin and adaptation, many secondary freshwater plants (bryophytes, ferns and angiosperms), and only very few derived
angiosperms adapted to marine, fully saline environments
(the monocot sea-grasses, e.g. Zostera).
Streptophytes adapted to deal with freshwater conditions
very early during their evolution, and probably were the first
eukaryotic freshwater algae (Fig. 2A). For the foundation of
the first terrestrial ecosystems, streptophytes were exploiting
an entirely new environment, almost free of competing organisms, probably with the exception of cyanobacteria and fungi
(Labandeira, 2005). This situation allowed the explosive radiation of early land plants, beginning in the Silurian period,
possibly earlier in the Ordovician or even Cambrian
(Labandeira, 2005; Taylor and Strother, 2008), adapting their
morphology, physiology, life history and reproduction to
land life (Fig. 2B). Any algal group that later developed a tendency towards terrestrial and macrophytic life styles was confronted with the opposite situation: competition with already
adapted land plants. It is therefore not surprising that no
second lineage of land plants evolved successfully besides
streptophytes.
What can be speculated about the origin and advantage of the
sporophyte generation?
The major difference between streptophyte algae and
embryophytes is the heteromorphic life history of the latter,
i.e. development of the zygote towards an embryo and a
diploid sporophyte generation. All streptophyte algae are haplonts with the zygote being the only diploid cell, which
immediately undergoes meiosis (resulting in four meiospores).
In contrast to gametes (eggs, sperms), spores are enclosed by a
pigmented cell wall composed of sporopollenin, an extremely
resistant biopolymer, and are thus well protected from predators, mechanical and chemical damage, degradation and mutagenic UV light. Interestingly again, sporopollenin evolved
within the streptophyte algae (Delwiche et al., 1989). Spores
are not protected from desiccation, but tolerate dehydration,
which might even offer an advantage for spore dispersal.
Therefore, the optimal reproduction and dispersal strategy for
early terrestrial plants was the production of spores rather
than gametes, ideally in very large numbers, to ensure survival
and germination of at least some of them. We regard the presence of a multicellular sporophyte, resulting from a delay of
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of proteins/genes now also found in streptophyte and/or chlorophyte algae are given in Table 1.
A nice example is the ‘plant-specific’ vacuolar sorting
receptor (formerly known as BP80). One of us has recently
shown that this protein originated in the last common viridiplant ancestor and is present in the Chlorophyta and the
Streptophyta (Becker and Hoef-Emden, 2009). The overall
structure of the receptor has not changed in green algae and
land plants and the overall rate in sequence evolution
appears to be slower in streptophytes than in chlorophytes.
This seems to be a general pattern. Similar slow evolution
rates have been observed for many proteins in phylogenetic
trees published in recent years. Embryophyte evolution
appears mainly to involve expansion of protein families followed by differential expression rather than sequence variations. This seems also to be the case for the chloroplast
genome. Turmel et al. (2007) concluded that ‘most of the features typical of land plant chloroplast genomes were inherited
from their green algal ancestors’.
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Becker & Marin — Streptophyte algae and the origin of embryophytes
C. Paleozoic to Mesozoic Era:
Carboniferous–Cretaceous Period
(approx. 360–65 MY ago)
Freshwater
i Chloro- and Trebouxiophyceae
(Chlorophyceae dominated freshwater
phytoplankton communities after the
Permian/Triassic mass extinction
250 MY ago)
i Streptophyte algae (mainly Charales
and Zygnematales)
i Embryophyte water plants (first aquatic
angiosperms: early Cretaceous Period)
Ocean
i Ulvophyceae (e.g. Ulvales
Dasycladales, Bryopsidales,
Cladophorales)
i ‘Prasinophytes’ (e.g.
Mamiellales,
Pyramimonadales)
Ordovician–early
Devonian Period
(approx. 490–400 MY ago)
Zygnematales (conjugating green algae;
unicells or unbranched filaments)
Ul
Ancient Chlorophyta:
several clades of marine
‘prasinophyte’ flagellates
and/or coccoids
Charales (stoneworts - branched filaments organized as
a main axis and whorls, resembling Equisetum)
Coleochaetales (parenchymateous branched filaments)
vo
(m ph
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Ch rine ea
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(fr ro
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Tr
hw yc
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at ea
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,
(fr xi
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hw h
Ch
at yce
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e
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(m de
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ar nd
in ra
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s
Four clades
of derived
Chlorophyta:
e
ea
yc
h
o
op t
or ae
hl ce
C y
of ph ts
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fr
EMBRYOPHYTA (bryophytes, lycophytes, ferns, spermatophytes)
Phycoplast
Phragmoplast
CHLOROPHYTA
Klebsormidiales and Entransia
(unbranched filaments)
Mesostigma
and Chlorokybus
(flagellate, sarcinoid)
STREPTOPHYTA
A. Neoproterozoic Era:
Cryogenian–Ediacaran Period
(approx. 850–540 MY ago)
Freshwater
Ocean
Ancient Chlorophyta:
marine and brackish
leiosphaerids and tasmanitids –
ancestors of extant ‘prasinophytes’
(scaly green flagellates and coccoids)
CHLOROPHYTA
Ancient Streptophyta:
unknown ancestors of extant streptophyte lineages –
freshwater flagellates, coccoids,
sarcinoids and filaments
ancestors of Mesostigma
and Chlorokybus (scaly
freshwater flagellates)
STREPTOPHYTA
F I G . 2. Diversification of green plants (Viridiplantae) and colonization of terrestrial habitats by streptophyte algae. Three stages are shown: (A) early evolution
of the viridiplant algae during the Neoproterozoic era; (B) colonization of terrestrial habitats by streptophyte algae during the Palaeozoic era; and (C) origin of
current freshwater ecosystems during the Palaeozoic to Mesozoic era. The smaller freshwater body illustrates an acidic bog-pool with zygnematalean algae. Green
algae and embryophytes are illustrated in different tones of green: dark (Streptophyta) vs. bright green (Chlorophyta).
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B. Paleozoic Era:
i Rapid adaptive radiation of
Chloro- and Trebouxiophyceae
i Gradual reduction in
diversity and abundance of
streptophyte green algae
(exception: evolutionary diversification
and speciation of the Zygnematales
during the Jurassic and Cretaceous Period)
Becker & Marin — Streptophyte algae and the origin of embryophytes
Early diversification and progressive extinction: explanations of
why an evolutionary key group such as the streptophyte algae
consists of only a few extant lineages
Extant streptophyte algae display a surprisingly low diversity (about 13 families, 122 genera), in contrast to the
Chlorophyta with about 100 families containing 700 genera.
The series of evolutionary events that shaped the current distribution and diversity of green algae can be tentatively reconstructed from molecular phylogenies and the scarce fossil
record of algae and early land plants (summarized in Fig. 2).
After their separation from ancient marine Chlorophyta, streptophyte algae conquered freshwater habitats worldwide, and
probably were the only eukaryotic freshwater algae during
the Precambrian (Fig. 2). They coexisted ‘side by side’ with
their embryophyte descendents, at least before the appearance
of the first aquatic embryophytes (Cretaceous; Martı́n-Closas,
2003), and with their marine ‘sisters’ (Chlorophyta). What
caused the failure of streptophyte algae to dominate the freshwater permanently? At first, two catastrophic events significantly reduced the streptophyte diversity, as is obvious from
the fossil record of the Charales: the Permian/Triassic and
the Cretaceous/Tertiary mass extinctions, both probably
related to volcanism and/or asteroid impact and accompanied
by climatic changes. For example, the Permian/Triassic
Boundary event (250 MY ago) marked the extinction of
those Charales with anti-clockwise oogonia, and from then
on, the enveloping cells of charalean oogonia display the
modern clockwise coiling pattern. The Cretaceous/Tertiary
extinction (65 MY ago), which is known as the end of the
Mesozoic dinosaur age, caused the extinction of the charalean
family Clavatoraceae, and an ongoing progressive reduction of
the diversity of the surviving Charales (Martı́n-Closas, 2003;
Soulié-Märsche, 2004; Martı́n-Closas and Wang, 2008).
Except for the Charales, the fossil record of streptophyte
algae is unfortunately rather poor, and thus we can only speculate about the disappearance of other ancient groups of streptophyte algae by mass extinctions. It is currently unclear whether
further catastrophes such as the recent ice ages have also
shaped the freshwater flora.
The second problem streptophyte algae were confronted
with was the invasion of freshwater habitats by other algae
and/or plants, followed by harsh competition for light, space
and nutrients. At first, modern groups of Chlorophyta ( primarily marine green algae) appeared after a new mode of cell division was introduced, the phycoplast, which enabled complex
multicellular growth (analogous to the streptophyte phragmoplast; Fig. 2B). Two of these derived groups, the classes
Chlorophyceae and Trebouxiophyceae, switched almost completely towards freshwater habitats. Since about the Permian/
Triassic mass extinction (250 MY ago; Fig. 2B, C), these
groups dominated the freshwater phytoplankton (Martı́nClosas, 2003) and apparently brought the hegemony of streptophyte algae in their original habitat to an end. It remains
unclear whether the appearance of (better-adapted?)
Chlorophyceae and Trebouxiophyceae was the main reason
for the reduction of streptophyte diversity via competition, or
whether they just radiated into a largely empty freshwater ecosystem after the previously dominant streptophyte algae had
already been reduced, like successive ‘dynasties’ of green
algae. Later, the first water embryophytes, dinoflagellates
(both since the Cretaceous, approx. 100 MY ago), diatoms
(Palaeocene, ca. 60 MY ago) and chrysophytes (Eocene,
approx. 40 MY ago) appeared in freshwater environments
(Martı́n-Closas, 2003), and further competed with the surviving streptophyte algae, which never again reached the diversity
and ecological dominance they once had.
CO NC L US IO NS
There is now agreement that embryophytes originated from
streptophyte algae. Their primary freshwater adaptation apparently played a key role in the colonization of dry land habitats.
However, the branching order of streptophyte algae is far from
settled. A complete understanding of the evolution of land
plants will require the remaining phylogenetic questions to
be solved and genome evolution within streptophytes to be
addressed. The latter requires genome information on streptophyte algae. While a growing number of genomes of chlorophyte algae have been sequenced, currently there is to our
knowledge not a single genome project (except ESTs) on
any streptophyte alga. Without any genome sequence of a
streptophyte alga for comparison, our picture of the evolution
of embryophytes remains far from complete.
ACK NOW LED GE MENTS
This paper is dedicated to Prof. Dr M. Melkonian on the
occasion of his 60th birthday, a pioneer in evolutionary
studies on green algae.
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meiosis, as the first adaptation to terrestrial life. The erect sporophyte morphology with terminal sporangia optimized the
long-range dispersal of spores, whereas the haploid gametophyte generation usually remained on the ground, since the
‘traditional’ oogamous fertilization (eggs and sperm cells)
required free water. The embryophytes of the Rhynie chert
Lagerstätte (early Devonian) already showed a size difference
between gametophytes and sporophytes [e.g. Cooksonia
(Gerrienne et al., 2006); Rhynia (Kerp et al., 2004);
Aglaophyton (Taylor et al., 2005)]. Initially a dependent
‘spore-producing organ’, the developmental potential of the
sporophyte generation to form highly differentiated and autonomous plant bodies was exploited only later by lycophytes,
ferns and seed plants.
Interestingly,
the
haploid/diploid
transition
in
Chlamydomonas is regulated by two homeobox proteins of
the KNOX/BELL protein family (Lee et al., 2008). In embryophytes BELL and KNOX homeodomain proteins are
involved in maintaining the shoot apical meristem (Ariel
et al., 2007) and form part of a large protein family
[homeodomain- (HD) containing proteins] associated with
various cell differentiation events. Members of the ‘plantspecific’ HD-ZIP subfamily have now also been reported
from streptophyte algae (Floyd et al., 2006). Thus it seems
likely that the sporophyte originated by simple changes in
the expression pattern of homeobox proteins of the BELL/
KNOX family followed by an expansion and diversification
of the HD-containing proteins to become important regulators
of cell differentiation.
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