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The evolution of the land plant life
cycle
Author for correspondence:
Karl J. Niklas
Tel: 001 607 255 8727
Email: kjn2@cornell.edu

Karl J. Niklas1 and Ulrich Kutschera2

1

Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA; 2Institute of Biology,

University of Kassel, Heinrich-Plett-Strasse 40, D-34109 Kassel, Germany

Received: 20 July 2009

Accepted: 1 September 2009

Contents
Summary

27

VII. Genomic re-deployment and embryophyte reproduction

35

I.

Introduction

28

VIII. Developmental homologies?

35

II.

Developmental constraint or a phyletic legacy?

29

IX.

Isomorphic or dimorphic?

36

III.

Green plant phylogeny

29

X.

Conclusions

38

IV. The ancestral green plant life cycle

31

Acknowledgements

39

V.

32

References

39

Haplobiontic or diplobiontic life cycles?

VI. Pseudo-archegonia, plasmodesmata, and parenchyma

33

Summary
New Phytologist (2010) 185: 2741
doi: 10.1111/j.1469-8137.2009.03054.x

Key words: alternation of generations,

archegonia, Chara, Cooksonia,
homeodomain gene networks, homology,
life cycle evolution, MADS-box genes.

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The extant land plants are unique among the monophyletic clade of photosynthetic eukaryotes, which consists of the green algae (chlorophytes), the charophycean algae (charophytes), numerous groups of unicellular algae (prasinophytes)
and the embryophytes, by possessing, firstly, a sexual life cycle characterized by an
alternation between a haploid, gametophytic and a diploid, sporophytic multicellular generation; secondly, the formation of egg cells within multicellular structures
called archegonia; and, thirdly, the retention of the zygote and diploid sporophyte
embryo within the archegonium. We review the developmental, paleobotanical
and molecular evidence indicating that: the embryophytes descended from a
charophyte-like ancestor; this common ancestor had a life cycle with only a haploid
multicellular generation; and the most ancient (c. 410 Myr old) land plants (e.g.
Cooksonia, Rhynia and Zosterophyllum) had a dimorphic life cycle (i.e. their haploid and diploid generations were morphologically different). On the basis of these
findings, we suggest that the multicellular reproductive structures of extant charophytes and embryophytes are developmentally homologous, and that those of the
embryophytes evolved by virtue of the co-option and re-deployment of ancient
algal homeodomain gene networks.

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I. Introduction
One of the most important biological events in the history
of life was the successful colonization of the terrestrial landscape by green, multicellular plants and their subsequent
rapid diversification during the early Paleozoic (Chaloner,
1970; Graham, 1993, 1996; Niklas, 1997; Raven &
Edwards, 2001; Taylor et al., 2009). This key event, which
was unknown to Darwin (1859), paved the way for terrestrial animal evolution, altered geomorphology by accelerating soil formation and modifying hydrology patterns, and
thus irrevocably changed the Earths climate (Chaloner &
Lawson, 1985; Willis & McElwain, 2002). Authorities

(a)

differ regarding when the land plants first appeared

(Fig. 1a). Some lines of evidence indicate that microfossil
assemblages of spores from the Lower Middle Ordovician
are the oldest remains of terrestrial plant life, whereas others
point to a SilurianEarly Devonian invasion (Gray et al.,
1974; Gray, 1985; Strother et al., 1996; Beck & Strother,
2001; Wellman et al., 2003), although reports of Neoproterozoic terrestrial soil crusts containing photosynthetic
organisms (of a cyanobacterial nature?) must be considered
(see Knauth & Kennedy, 2009). What can be said with
more certainty is that the modern-day descendants of the
first successful land plants comprise a monophyletic group,
the Embryophyta (Kingdom Plantae). The living repre-

(b)

Fig. 1 Reconstruction of an ancient aquaticterrestrial landscape, with the earliest multicellular land plants, adapted from a drawing of Z. Burian (c. 1945) (a). Comparison between the diplobiontic and haplobiontic life cycles with some representative botanical examples (embryophytes and two aquatic charophytes, Coleochaete and Chara, respectively) (b). In the diplobiontic life cycle, the haploid and diploid phases
(gametophyte, G, and sporophyte, S, respectively) are multicellular. In the haplobiontic-haploid life cycle, only the haploid phase is multicellular. The haplobiontic-diploid life cycle (in which the diploid phase exclusively expresses multicellularity, such as in our species and other animals)
is not shown. n = number of chromosomes per haploid cell.

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sentatives of this taxon include the paraphyletic nonvascular
plant lineages (colloquially referred to as the bryophytes)
and the tracheophytes (i.e. lycophytes, ferns, horsetails and
seed plants).
Numerous lines of evidence support the contention that
the embryophytes are monophyletic and closely related to
the green algae (Kingdoms Protista and Protoctista). However, the embryophytes are unique among all extant lineages
in possessing three important and interrelated reproductive
attributes. First, they possess a sexual life cycle that requires
an alternation between a multicellular haploid generation,
which produces sperm and egg cells (the gametophyte), and
a multicellular diploid generation, which produces meiospores with sporopollenin-rich walls (the sporophyte). Second, they develop multicellular, parenchymatous structures
that produce eggs and sperm (called archegonia and antheridia, respectively). Third, they retain the fertilized egg (i.e.
the zygote) within the archegonium, wherein the sporophyte embryo is nurtured and protected (Walbot & Evans,
2003). The retention of the diploid embryo within the
archegonium is the reason why the land plants are called
embryophytes and why the older literature referred to
them as the Archegoniatae (Campbell, 1905; Bower, 1908).

II. Developmental constraint or a phyletic

legacy?
Whether the archegoniate diplobiontic life cycle was essential for (or merely coincidental to) the evolutionary and ecological success of the first multicellular land plants remains
problematic. The retention of this life cycle may reflect a
developmental constraint or a phyletic legacy, that is, a feature that either could not be or was not lost once acquired
by the last common ancestor to all embryophytes. Alternatively, this life cycle may have been retained because it conferred functional advantages that prefigured (or were
requisite for) survival and reproductive success in an aerial
and potentially desiccating habitat (Fig. 1a). Ad hoc adaptive scenarios can be easily constructed to argue in favor of
the latter, whereas recent insights from plant developmental
genomics suggest that very ancient algal gene networks were
co-opted during the evolution of the embryophyte life cycle
and multicellular body plan (Niklas & Kutschera, 2009).
In the light of this uncertainty, this article has two goals.
The first is to review the available phycological, paleobotanical, developmental and molecular data that shed light on
how the archegoniate diplobiontic life cycle may have
evolved. The second is to explore how these data influence
the interpretations of developmental homologies among
embryophyte reproductive structures (i.e. antheridia, archegonia and sporangia). These goals dictate the structure of
this article, which conforms to a concept map dominated
by three axes (Fig. 2). The first of these axes focuses on the
environmental context in which early land plants evolved,

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Fig. 2 Concept map with three major themes (axes) underlying a

sequential exposition (steps 16) of the evolution of the land plant
life cycle. H-d, haplobiontic-diploid; H-h, haplobiontic-haploid. The
aquaticterrestrial axis is illustrated in Fig. 1a. See text for details.

grew and reproduced. The environmental context is pivotal

to tracing the evolution of any life cycle, because the most
ancient embryophytes required access to liquid water for
the successful fertilization of their eggs. The second axis
focuses on the plant body plan and the transition from the
unicellular to the multicellular condition. All the available
information indicates that the ancestral condition for each
of the major green plant lineages involved a unicellular
body plan, and that multicellularity is a derived evolutionary condition. The third axis deals directly with the life
cycle concept. For the purposes of our review, only two life
cycles are relevant, one in which two multicellular generations occur and another in which only one multicellular
generation exists, i.e. the diplobiontic and haplobiontic life
cycles, respectively (see Fig. 1b). Because terminology, such
as diplobiontic and haplobiontic, may be unfamiliar to
some (and used in different ways by others), we provide definitions for these and other technical words and phrases as
used in the context of this article (Table 1).

III. Green plant phylogeny

Concept maps help to establish logical transformational
alternatives among critical character states (e.g. terrestrial vs
aquatic, unicellular vs multicellular; haplobiontic vs diplobiontic life cycles). However, taken in isolation, they cannot
identify the polarity of evolutionary transformations (e.g.
aquatic to terrestrial vs terrestrial to aquatic). For our purpose, a stringent cladistic hypothesis is required, because the
phylogenetic relationships among the various green plant
lineages are very complex and because a well-supported
cladogram provides a framework with which to deduce the

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Table 1 Definitions of key words and phrases used in the context of this article
Antheridium
Archegonium
Body plan
Dimorphic

Diplobiontic

Gametangia
Gametophyte
Globule
Haplobiontic
Haplobiontic-diploid
Haplobiontic-haploid

Homologous
Isomorphic
Nucule
Oogonium
Parenchyma
Parenchymatous tissue construction

Plasmodesmata
Sporophyte
Streptophytes
Zygotic meiosis

The multicellular, sperm-producing structure of the embryophytes, consisting of a sterile jacket

of cells surrounding spermatogenous cells
The multicellular, egg-producing structure of the embryophytes, consisting of a neck,
neck canal cells and a venter surrounding the egg
The phenotypic architecture that distinguishes one group of organisms from another;
the processes that obtain an organisms organized growth and development
The presence of substantive phenotypic differences between the haploid and diploid phases
(generations) in the life cycle of an organism; in phycology, heteromorphic
(i.e. morphologically different haploid and diploid generations)
A life cycle that involves the alternation of two multicellular phases
(one haploid and another diploid) to complete sexual reproduction; also known as the
alternations of generations and as the diplohaplontic life cycle, e.g. mosses and ferns
Multicellular gamete-producing structures, e.g. antheridia, archegonia, globules and nucules
The multicellular haploid phase in a plant life cycle that produces gametes (sperm or eggs, or both)
Sperm-producing multicellular organ of charalean algae
A life cycle involving only one multicellular generation
A haplobiontic life cycle in which the only multicellular generation is diploid,
e.g. Homo sapiens and other vertebrates
A haplobiontic life cycle in which the only multicellular generation is haploid;
one in which the only diploid phase is the zygote; in phycology, equivalent to
haplontic, e.g. charophycean algae
One or more traits characterizing two or more phyletically related taxa that emerge as
a result of shared highly conserved ancestral structures, genetic networks or mechanism(s)
The absence of substantive phenotypic differences between the haploid and diploid phases
(generations) in the life cycle of an organism
Egg-producing multicellular structure of charalean algae
In phycology, a cell specialized to function as an egg
A tissue composed of not distinctly specialized and generally uniformly appearing living
cells with thin primary cell walls
A tissue in which cells have the capacity to divide in any plain with respect to the principal
body axis and in which primary or secondary plasmodesmata develop at the majority of cell
walls shared among neighboring cells
Microscopic channels traversing the cell walls of embryophytes and some algae that enable
intercellular symplastic transport and communication
The multicellular diploid phase in a plant life cycle that produces spores
An informal taxonomic term referring to the charophyteembryophyte lineage
Meiosis occurring after the fertilization of the egg without any intervening mitotic cell divisions.
In multicellular algae, zygotic meiosis obtains a haplobiontic-haploid life cycle

evolutionary transitions leading to the embryophyte life

cycle. In this section, we review the phylogenetic relationships among the green plant lineages as a prelude to mapping life cycle evolutionary transformations. All current
palaeobotanical, cytological, physiological and molecular
data indicate that the green algae (i.e. the Chlorophyta sensu
Smith, 1950) and the Embryophyta share a last common
ancestor (Mattox & Stewart, 1984; Mishler & Churchill,
1985; McCourt, 1995; Karol et al., 2001; Scherp et al.,
2001; Lewis & McCourt, 2004; Archibald, 2009), which
was a unicellular flagellate that evolved as a result of ancient
endosymbiotic events involving a prokaryotic host cell and
a cyanobacterial-like photoautotroph (Bhattacharya &
Medlin, 1995; Kutschera & Niklas, 2004, 2005, 2008)
(Fig. 3). Numerous lines of evidence further show that the
embryophytes descended from a last common ancestor
shared with the Coleocheatophyceae, Charophyceae and
possibly other lineages (such as the Zygnemophyceae and

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Klebsormidiophyceae), which collectively comprise the

green algae colloquially called the charophytes (Karol
et al., 2001; McCourt et al., 2004). Taken in isolation, the
ColeocheatophyceaeCharophyceae lineage is relatively
small in terms of species numbers and includes species with
unicellular and multicellular body plans, some of which are
adapted to, or at least capable of tolerating, some desiccation (Fig. 3).
The evidence for the monophyly of the charophyte
embryophyte lineage (collectively referred to as the streptophytes) is extensive. In addition to producing cell walls
containing cellulose, chloroplasts with stacked grana and
chlorophylls a and b, bi- or multiflagellated cells (when
motile cells are present) and starch as their primary photosynthate, the charophytes and embryophytes also share features not found in any other green algae, such as, for
example, several enzyme systems (e.g. glycolate oxidase),
motor organelles with asymmetrically inserted flagella,

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Fig. 3 Phylogenetic relationships among the

major green plant lineages based on an analysis of DNA sequence data. Dichotomous
branches shown as broken lines indicate
weakly supported portions of the tree. The
phyletic position of the Mesostigmatophyceae is particularly problematic (denoted
by ?). The distributions of different habitat
preferences, body plans and life cycles are
indicated by symbols (see lower box).
Adapted from Lewis & McCourt (2004).

dissimilar flagella roots with a multilayered structure, persistent mitotic spindles, open mitosis and phragmoplasts
(Mattox & Stewart, 1984; Graham, 1993; McCourt, 1995;
Graham & Wilcox, 2000; Karol et al., 2001; Scherp et al.,
2001; McCourt et al., 2004).
Nevertheless, although all green plants are monophyletic,
the most recent phylogenies consistently identify a deep
genomic dichotomy between the streptophytes and three
cladistically well-supported lineages (i.e. the Chlorophyceae,
Trebouxiophyceae and Ulvophyceae), which are collectively
referred to as the chlorophytes. Like the charophytes, the
chlorophytes are ecologically diverse and include species
with unicellular and multicellular body plans, some of
which can survive in subaerial or emergent habitats (Fig. 3).
The deep streptophytechlorophyte divide is occupied
by an assortment of lineages represented by unicellular
species, collectively called prasinophytes (Fig. 3), whose
phylogenetic relationships remain problematic (Sym &
Pienaar, 1993; Lewis & McCourt, 2004). Although the
existence of six or seven prasinophyte lineages is supported by molecular data (e.g. Zignone et al., 2002),
these algae are best viewed as a grade of cellular organization emerging from the base of the green plant clade. As
such, they have the potential to shed light on the features
characterizing the last common flagellate ancestor to the
entire green plant tree of life.

IV. The ancestral green plant life cycle

The precise phylogenetic relationships among the prasinophytes, chlorophytes and streptophytes will undoubtedly

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be modified as more taxa are examined and more data

are incorporated into cladistic analyses. However, given
current information, three conclusions can be drawn: the
green plants are monophyletic; the phyletic dichotomy
separating the chlorophytes and the streptophytes is occupied by prasinophytes; and the streptophytes descended from a unicellular freshwater alga. Here, we
review data that support two additional conclusions: the
ancestral life cycle in all of the major green algal lineages
involved zygotic meiosis and was thus haplobiontic (Fig.
1b); and the derived green plant diplobiontic life cycle
evolved at least twice, once among the chlorophytes
(Ulvophyceae) and again among the streptophytes (charophytes and embryophytes).
These assertions are based on two lines of evidence. First,
among extant unicellular and multicellular green algae (i.e.
prasinophytes, chlorophytes and charophytes) for which
sexual reproduction has been documented, most have a life
cycle in which the only diploid cell is the zygote (Smith,
1950; Bold & Wynne, 1978; Graham & Wilcox, 2000;
Lee, 2008). Second, although sexual reproduction has been
documented for very few species in the basal prasinophyte
lineages, those that have been corroborated involve zygotic
meiosis (e.g. Nephroselmis olivacea; Suda et al., 1989)
(Fig. 4a). Thus, for the majority of green algae, the adult
or mature organism in the sexual life cycle is haploid and
functions reproductively as the gametophyte generation in
the embryophyte life cycle (Graham & Wilcox, 2000; Niklas & Kutschera, 2009).
As noted, plant life cycles involving only one multicellular individual are called haplobiontic (in contrast with

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is whether (and where) multicellularity is developmentally
expressed.
In contrast with the broad phyletic distribution of haplobiontic-haploid life cycles, diplobiontic life cycles occur
in only one green algal lineage the Ulvophyceae (Fig. 3).
Three of the six orders within this class are reported to
contain species with diplobiontic life cycles (i.e. the Cladopherales, Trentepohliales and Ulvales; see Graham &
Wilcox, 2000; Lewis & McCourt, 2004; Lee, 2008 and
references therein). Among these species, some diplobiontic life cycles are isomorphic (e.g. Ulva), whereas others
are dimorphic (e.g. Derbesia). However, even among the
various Ulvophyceae, the diplobiontic life cycle appears to
be an evolutionarily derived condition, because molecular
data suggest that the Ulotrichales are basal in the Ulvophyceae (OKelly et al., 2004), and because ulotrichalean algae
have haplobiontic-haploid life cycles, e.g. Ulothrix and
Monostroma (Fig. 4b). The haplobiontic-haploid life cycle
is also well represented among the acellular (siphonous)
ulvophycean marine algae. These lines of evidence indicate
that the diplobiontic life cycles of the Embryophyta and
Ulvophyceae are the result of convergent evolution (see
Fig. 3).

V. Haplobiontic or diplobiontic life cycles?

Fig. 4 Diagrammatic comparison of the life cycles of the prasinophyte Nephroselmis olivacea (adapted from Suda et al., 1989) (a)
and the ulotrichean alga Monostroma grevillei (adapted from
Graham & Wilcox, 2000) (b).

diplobiontic life cycles with two multicellular individuals;

Fig. 1b). Two variants of the haplobiontic life cycle are possible. One in which the multicellular generation is diploid
(the haplobiontic-diploid life cycle; Hd) and one in which
the haploid generation is exclusively multicellular (haplobiontic-haploid; Hd) (see Fig. 2, node 4). Therefore, life
cycles involving zygotic meiosis are classified as haplobiontic-haploid (Table 1). Clearly, no multicellular generation
exists in the case of unicellular algae. The sexually mature
individual functions either indirectly or directly (i.e. with or
without intervening mitotic cell divisions) as the adult
organism and as a gamete. Therefore, the haplobiontic vs
diplobiontic terminology is largely irrelevant. Nevertheless,
the life cycles of unicellular algae, such as Nephroselmis olivacea, and multicellular algae, such as Monostroma grevillei,
are fundamentally the same (Fig. 4a,b, respectively). Both
are defined by zygotic meiosis. The only fundamental
distinction that conceptually separates the two life cycles

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Was the last common ancestor to the Charophyceae and

Embryophyta unicellular or multicellular? This question is
important because its answer provides an insight into the
evolution of the embryophyte life cycle. Consider that, if
the last common ancestor were unicellular, the capacity for
multicellularity could have evolved in either the haploid or
diploid generation, or both simultaneously (Fig. 5a,b) a
possibility that opens the door to many conceivable life
cycle variants as the ancestral condition. Alternatively, if the
last common ancestor were multicellular and had a life cycle
involving delayed zygotic meiosis, the diploid generation in
the embryophyte life cycle (i.e. the sporophyte) would be an
evolutionary innovation.
The phyletic distribution of unicellular species at the base
of the streptophyte lineage highlights the problematic nature of the answer to this question, as illustrated by the cladistic position of the monotypic Mesostigmatophyceae
(Fig. 3). Mesostigma vivida is an asymmetrical cell that was
originally classified as a charophyte on the basis of its flagellar ultrastructure (Melkonian, 1989). Subsequent molecular
analyses of 18S rRNA sequences indicated that the genus
was closely related to Chaetosphaeridum, which led to the
establishment of a new class, the Mesostigmatophyceae
(Marin & Melkonian, 1999). However, Delwiche et al.
(2002) demonstrated that Chaetosphaeridum is a charophyte
and, on the basis of rbcl sequences, concluded that Mesostigma is a sister taxon to the streptophytes. Subsequently, Yoshii et al. (2003) argued that Mesostigma represents an early

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(a)

(b)

Fig. 5 Diagrammatic rendering of the hypothetical transformation

of an ancient prasinophyte life cycle (a) (depicted as that of Nephroselmis olivacea; see Fig. 4a) into a diplobiontic life cycle (b). Delayed
zygotic meiosis and the intercalation of mitotic divisions results in a
multicellular sporophyte and mitotic divisions of meiospores before
plasmogamy results in a multicellular gametophyte.

evolutionary lineage and placed the Mesostigmatophyceae

among the prasinophytes (Fig. 3).
The phylogenetic position of Mesostigma remains contentious (see Lewis & McCourt, 2004). However, its phyletic
position at the base of the chlorophytestreptophyte
divide, in tandem with the antiquity of lineages containing
numerous semi-aquatic and terrestrial unicellular species
(i.e. Chlorokybophyceae, Klebsormidiophyceae and Zynemophyceae), suggests that a variety of life cycles may have
evolved (and disappeared) over the early course of charophycean evolution (see Fig. 3). Indeed, one intriguing line
of speculation is the prospect that important life cycle evolutionary innovations occurred among unicellular or filamentous charophytes serving as phycobionts in ancient lichenlike organisms. Currently, no lichen is known to contain a
charophycean phycobiont (Friedl & Bhattacharya, 2006).
However, it is possible that the ancient co-evolutionary history of the land plants and mycorrhiza was prefigured by a
mutually beneficial relationship between ancient charophytes and fungi that can be broadly thought of as lichenlike symbiotic organisms (McCourt et al., 2004).
Although the nature of the most ancient land plant life
cycle cannot be asserted currently, the available evidence
indicates that the ancestor to the streptophytes was multi-

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cellular and possessed a haplobiontic-haploid life cycle

similar to that of Coleochaete and Chara. If this supposition
is true, the land plant sporophyte generation was an evolutionary innovation resulting from delayed zygotic meiosis
and the intercalation of one or more mitotic cellular divisions. Put differently, the first embryophyte sporophyte was
a multicellular zygote. Whether this life cycle first appeared
in an aquatic, semi-aerial or aerial environment is conjectural. Although the transition from a haplobiontic-haploid
to a diplobiontic life cycle may have come at a cost with
regard to the growth of the haploid generation (as indicated
by studies on mosses; see Ehrlen et al., 2000; Rydgren &
kland, 2002), the diplobiontic life cycle confers adaptive
benefits across a broad range of habitats and environmental
conditions (e.g. the numerical amplification of zoospores or
meiospores resulting from possibly rare fertilization events,
and the possibility to occupy two different niches in the
same general environment), as attested by the reproductive
and ecological success of ulvophycean algae and embryophytes with free-living gametophytes.
Nevertheless, if the evolutionary transformation from a
haplobiontic-haploid to a diplobiontic life cycle occurred in
a fresh water or terrestrial habitat, which is almost a certainty, the first sporophytes would hardly qualify as land
plants, as they would have grown on maternal gametophytes
attached, in turn, to a hydrated substrate, and thus are more
properly thought of as air plants (see Fig. 1a).

VI. Pseudo-archegonia, plasmodesmata and

parenchyma
Whether the first charophycean algae to evolve a diplobiontic life cycle were archegoniates is another challenging and
unresolved question. The fossil record of the earliest land
plants is especially sparse and problematic, and there is
nothing in the diplobiontic life cycle concept that stipulates
the manner in which sperm or eggs are produced (Wellman
et al., 2003). In addition, as noted earlier, the diplobiontic
life cycle is not unique to the embryophytes (see Fig. 3).
However, it is very likely that the last common ancestor to
the streptophytes had reproductive structures that functioned in some, if not many, ways like the antheridia and
archegonia of embryophytes, such as Equisetum (Lycopodiacae), a seedless land plant (Fig. 6a,b).
This assertion rests on three observations. The zygotes of
many, albeit not all, species in the Coleochaetophyceae and
all species in the Charophyceae are retained by the gametophyte, during which many species nourish and protect them
for short, albeit developmentally substantive, periods of
time; and the most evolutionarily derived charophycean
species, such as stoneworts of the genus Chara, have multicellular and morphologically complex gametangia (Fig.
6c,d). In the case of Coleochaete (see Fig. 1b), sterile
filaments develop around the oogonium after fertilization.

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In the case of charalean species, sterile cells envelop the

oogonium before fertilization. Indeed, the sperm-producing
organ of Chara (the globule) is functionally (and developmentally) similar in many ways to the antheridium, whereas
the egg-producing structure (the nucule) can be called a
pseudo-archegonium on the basis of its capacity to protect
and provide the egg and zygote with nourishment for a not
inconsiderable time (Fig. 6c,d).
Another physiologically important feature shared by the
charophytes and embryophytes is the capacity to form plasmodesmata (Graham, 1982), which has evolved independently many times in different algal lineages and independently within the Chlorophyceae and again in the
Charophyceae (Raven, 1997). Among the streptophytes, the
ability to form these symplastic connections among adjoining cells is restricted to the Coleochaetophyceae (specifically
Coleochaete, see Fig. 1b), Charophyceae (Fig. 6c,d) and the
Embryophyta (Brown et al., 1994; Cook et al., 1998). The
ability to form plasmodesmata permits active polar transport
of large molecular weight solutes across adjoining cell walls,

(a)

(b)

(c)

(d)

which facilitates the targeting and nutrition of specialized

cells (see Jansen, 2001; Lucas et al., 2001). It can also play a
pivotal role in the physiological control of embryogenesis.
More detailed studies are required to determine whether charophycean plasmodesmata are typically primary or secondary
in nature. The former develop during cytokinesis and cell
wall deposition; the latter develop after cytokinesis and may
appear after secondary wall deposition. Whether primary
or secondary plasmodesmata form during or after histogenesis is important, because it helps to resolve whether
the tissues in which plasmodesmata develop are truly parenchymatous, and because primary and (complex) secondary plasmodesmata have different protein-trafficking functions, which can influence organogenesis (e.g. Itaya et al.,
1998). Regardless of these subtleties, primary plasmodesmata have been demonstrated for at least one species of
Chara (Brown et al., 1994; Cook et al., 1998), and
ultrastructural studies suggest that the nodal regions of
Chara have a parenchymatous tissue structure (PickettHeaps, 1975; Cook et al., 1998).

Fig. 6 Comparisons among the antheridium

and archegonium of the vascular land plant
Equisetum (a and b, respectively) and the
reproductive organs (nucule and globule,
with gamete-producing tissues) of the Charalean alga Chara (c and d, respectively). c,
coronal cells; e, egg; g, globule; n, neck cells;
nu, nucule; o, oogonium sc, spermatogenous
cells; sj, sterile jacket cells; spc, sperm cells; v,
venter.

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VII. Genomic re-deployment and embryophyte
reproduction
The ability to form plasmodesmata and parenchyma is not
a requisite for the formation of morphologically complex
multicellular structures, such as the gametangia of Chara
(Fig. 6c,d). The nucule and globule of Chara and other
charalean algae are composed of branched filaments, which
only give the appearance of having a parenchymatous tissue
construction. However, the ability to form parenchyma and
plasmodesmata is an important attribute of the embryophytes, because it establishes complex and physiologically
integrated symplastic interconnections via primary and secondary plasmodesmata formation that are required for sporophyte embryogenesis and development.
Indeed, recent studies of homeodomain-containing transcription factor genes suggest that an intriguing genomic
redeployment strategy has attended the evolution of the
archegoniate diplobiontic life cycle. For example, among
the best known of these genes is the MADS-box gene family, which has been extensively studied in the flowering
model organism Arabidopsis thaliana. This gene family is
divided into two subfamilies, referred to as type I and type
II. There are 45 type II genes, which are also referred to as
MIKC factors (for MADS DNA-binding domain, intervening domain, keratin-like domain and C-terminal domain);
the type II group can be further subdivided into MIKCC
and MIKC* genes on the basis of the inferred evolutionary
history of the family. MIKC* proteins tend to have longer I
domains and less-conserved K domains than do the MIKCC
proteins. Sequences encoding MIKCC and MIKC* factors
have been identified in bryophytes and lycopods, as well as
in gymnosperms and angiosperms, which suggests that the
MIKC* and MIKCC genes have evolved independently for
at least 450 Myr. The expression of MIKC-type genes in
angiosperms occurs only after the specification of the
vegetative to inflorescence meristem transition, which is
mediated by the transcription factor encoded by FLORICAULA LEAFY (FLO LFY). In ferns, FLO LFY homologs are
expressed predominantly in sporogenous meristematic
tissues, but MADS-box gene expression is not closely correlated, suggesting that these genes have not yet been subordinated to FLO LFY regulation. In the moss Physcomitrella,
two FLO LFY paralogs (PpLFY-1 and PpLFY-2) are
required for the first division of the zygote and early sporophyte embryogenesis (Henschel et al., 2002; Tanahashi
et al., 2005), whereas MADS-box gene expression occurs
during Chara globularis gametangium differentiation and
declines after fertilization (Tanabe et al., 2005).
It is therefore reasonable to suggest that MADS-box
genes originally functioned in the differentiation of haploid
reproductive structures (e.g. the nucule and moss archegonium) and were subsequently redeployed to function in the
formation of sporophyte reproductive structures (e.g. the

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fern sporangium). Such combinatorial homeodomain-based

transcriptional control of reproduction may have extremely
deep phylogenetic roots. Ectopic expression of the homeoproteins Gsp1 and Gsm1 in the plus and minus strains of
the unicellular chlorophyte Chlamydomonas activates vegetative haploid cells to form zygote-like structures (Lee et al.,
2008). Likewise, Gsp1 and Gsp2 are members of the TALE
(three amino acid loop extension) homeodomain-containing transcription factors, which include the class 1 KNOX
and class 2 KNOX proteins. Homeodomain gene networks,
similar to those in land plants, have been reported for prasinophytes (e.g. Micromonas), which are postulated to reveal
the attributes of the last common ancestor of all green
plants (Worden et al., 2009) (see Fig. 3).

VIII. Developmental homologies?

The recruitment and redeployment of homeodomain gene
networks underlying much of the evolution of streptophyte reproduction may help to explain why charalean
gametangia and embryophyte antheridia, archegonia and
sporangia share the same fundamental developmental choreography (Fig. 7).
Perhaps the most obvious shared attribute of these multicellular structures is that each develops from a single superficial meristematic initial. In the case of charalean globule
and nucule, this initial is a nodal cell (Fig. 7a); in the case
of embryophytes, it is typically an epidermal cell (Fig. 7b).
Charalean antheridium induction involves an unequal division of the nodal initial cell. The smaller of the two derivatives develops into a stalk; the larger, apical cell undergoes a
series of cellular divisions that eventually produce external
shield cells that surround stalks and branched structures
(manubria) from which sperm filaments radiate (PickettHeaps, 1975). The development of the charalean nucule
also begins from a single nodal cell that undergoes unequal
cell divisions to form a basal stalk and the tube cells that
gyrate around a centrally located oogonium (Pickett-Heaps,
1975). In much the same way, sporangial induction
involves periclinal division of one or more epidermal cells.
Among eusporangiate species, the innermost derivatives
give rise to sporogenous cells, whereas the outermost
develop into the sporangium wall (Fig. 7b). Embryophyte
gametangia (antheridia and archegonia) development also
begins when a single epidermal cell undergoes a periclinal
division. The innermost cells resulting from this division
develop into spermatogenous cells, or the neck canal and
egg cells (for details, see Campbell, 1905; Bower, 1908;
Gifford & Foster, 1989).
Numerous differences exist in the development of euand leptosporangia and in the development of antheridia
and archegonia. For example, the sporogenous cell initials
in the eusporangium develop from the innermost periclinal
derivatives of the superficial sporangial initials, whereas the

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sporogenous cells of the leptosporangium trace their developmental origins to outer periclinal derivative cells. Likewise, charalean and embryophyte development differ in
many ways. For example, the charalean oogonium occupies
an apical (albeit enveloped) position, whereas the embryophyte egg cell develops from a hypodermal derivative.
Likewise, the nucule and globule have a pseudo-parenchymatous (filamentous) tissue construction, whereas sporangia, antheridia and archegonia are parenchymatous (Gifford
& Foster, 1989; Graham & Wilcox, 2000).
Nevertheless, we suggest that there is sufficient developmental and molecular evidence to conclude that the
embryophyte sporangium is homologous to the antheridium archegonium as a result of homeodomain gene network recruitment from the gametophyte generation and
redeployment in the sporophyte generation. In this context,
we use the concept of homology sensu Shubin et al. (1997),
namely a correspondence in growth and differentiation
resulting from highly conserved and deeply ancestral genetic
mechanisms. Likewise, we believe that archegonia and antheridia are developmentally homologous to charalean gametangia, i.e. embryophyte gametangia are homologous to
the nucule and globule (Fig. 7). This perspective is consistent with current knowledge of the molecular developmental biology of streptophyte reproductive structures. It is also
consistent with the evolution of the embryophyte diplo-

biontic life cycle from the haplobiontic-haploid life cycle of

a charalean common ancestor. The alternative assertion that
embryophyte sporangia are homologous to leaves is far less
tenable (Kenrick & Crane, 1997a,b).

IX. Isomorphic or dimorphic?

We have argued that the ancient aquatic ancestor to all
green eukaryotes (Kingdoms Protoctista and Plantae) was a
single-celled flagellate (Fig. 3) with a life cycle that alternated between a haploid generation that functioned as the
adult + gamete and a more or less ephemeral single-celled
zygote (Fig. 1b). The traditional botanical view precludes
assigning such an organism a diplobiontic or a haplobiontic
life cycle, because multicellularity is not expressed in this life
cycle. Nevertheless, this kind of organism has an alternation of generations, albeit unicellular ones. Accordingly,
any consideration of the life cycle of the earliest Urform
(prototype) of all land plants necessarily begins by asking
whether the immediate ancestor to the streptophytes was
unicellular in both phases of its life cycle (as was its aquatic
precursor), or whether one or both of its life cycle phases
was multicellular. This consideration is cast in botanical tradition by asking whether the life cycle was isomorphic (both
life forms are the same) or dimorphic (two different life
forms) (see Fig. 2, node 5; Table 1).

(a)

(b)

Fig. 7 Comparisons among the development

of charalean gametangia (a) and the reproductive structures of embryophytes (b). The
charalean globule and nucule each develop
from a single superficial nodal cell initial (a).
The embryophyte eusporangium, antheridium and archegonium typically develop from
an epidermal cell initial (b). Tissues directly
involved with reproduction (e.g. sperm, egg
and sporogenous cells) are shaded.

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There are obvious advantages to multicellularity for an
organism living in a subaerial environment, e.g. protection
against UV exposure and dehydration (Niklas, 1997;
Raven, 1999, 2002). However, the most ancient green land
plants may have inhabited the soil or evolved from a lichenlike organism, and thus may have been protected by moisture-laden boundary layers (Stebbins & Hill, 1980; Read
et al., 2000). What is clear is that, over many generations,
the land plants became multicellular, and we necessarily
need to know whether this innovation occurred simultaneously in both the gametophyte and sporophyte generation, or whether one generation acquired multicellularity
whilst the other generation subsequently acquired this body
plan.
On the basis of the distribution of life cycles among
extant green plants (Fig. 3), it is logical to argue that the
series of life phase transformations achieving multicellularity began with the gametophyte generation, and that the
zygotes of the ancestors of the first green land plants were
preprimed for meiosis. If true, the vegetative phase of the
gametophyte generation is the primal (ancestral) and archetypical home for land plant gene expression and gene network interactions, as well as the effects of heritable
mutations on morphogenesis. Nevertheless, the alternative
possibility that multicellularity arose first in the diploid,
sporophytic phase cannot be excluded, especially from a
genetic perspective, as a single mitotic division before meiotic cell division generates eight (not four) potentially
recombinant genotypes from each zygote (with consequent
selective advantages), in contrast with a mitotic division
after meiosis, which generates two (not one) spore recombinant genotypes (with consequent effects on the stochastic
loss of a desirable combination of genes).
Another conceptually important, but as yet unresolved,
question is whether the most ancient embryophytes possessed an isomorphic or a dimorphic life cycle (Fig. 2,
nodes 5 and 6). Kenrick & Crane (1997a,b) and Steemans
et al. (2009) have argued that the isomorphic alternation of
generations is the most ancient, in part based on threedimensionally preserved gametophytes in the c. 410 Myr
old Rhynie Chert (see Kerp et al., 2004; Taylor et al.,
2005; Niklas & Kutschera, 2009). As discussed in the previous section, the gametophytes and sporophytes of the most
ancient embryophytes undoubtedly shared similar genomic
and developmental repertories, just as they shared genomic
similarities with their charalean common ancestor. Thus, in
the absence of phenomenologies, such as gene silencing, sex
chromosomes or epigenetic effects, differences in ploidy
may not have equated to significant gametophytesporophyte morphological differences. This perspective is
strengthened in the light of some modern-day mosses and
ferns, which can generate sporophyte morphologies directly
from their gametophytic cells (apogamy) and gametophyte
morphologies directly from their sporophyte cells (apo-

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spory). Apogamy and apospory show that the haploid and

diploid genomes contain much of the information required
to construct both the gametophyte and the sporophyte body
plans (Niklas & Kutschera, 2009).
A focus on apogamy rather than apospory is justified in
the context of our review, because the thesis developed thus
far is that the sporophyte generation evolved during the
transition from a charalean-like haplobiontic-haploid life
cycle to an embryophyte diplobiontic life cycle. Among
extant species, apogamy can be induced by cell trauma, low
light intensities, suitable concentrations of sugar or auxin. It
can also be induced by the deletion of the CURLY LEAF ortholog in the moss Physcomitrella (PpCLF). Okano et al.
(2009) have reported that gametophytic cells that usually
form protonema or gametophore apical cells generate meristematic apical cells that form branched morphologies,
which can be induced to form sporangium-like structures
with the exogenous application of PpCLF. The resulting
morphologies have been reported to be similar to very
ancient tracheophytes, such as Zosterophyllum or Cooksonia
(Figs 8 and 9).
These findings suggest that PpCLF regulatory gene networks may have participated in the early evolution of the
embryophyte sporophyte (Okano et al., 2009). Spontaneous mutation of the CURLY LEAF ortholog attending fertilization and zygote formation among ancient streptophytes may have participated in delayed zygotic meiosis,
and thus the formation of a multicellular diploid phase. It is
nevertheless doubtful that the mutation of any single gene
was sufficient for this important evolutionary transition.
Likewise, it is uncertain whether the sporophyte generation
evolved as a consequence of delayed zygotic meiosis or
precocious zygotic mitosis. Molecular analyses of angiosperm
mega- and microsporogenesis and mega- and microgametogenesis indicate that numerous complex gene networks are
involved in the initiation or suppression of meiosis. For
example, the male sterile multiple archesporial cell (mac1)
mutant in maize (Zea mays), which leads to the production
of extra diploid sporocytes in ovules and anthers, appears to
contribute to the restriction of the identity of cells competent for meiotic division (see Sheridan et al., 1996; Walbot
& Evans, 2003), whereas the Meiosis Arrested at Leptotene1
(MEL1) gene in rice (Oryza sativa) is required for sporocycte meiosis (Nonomura et al., 2007). More data from
taxa deeper within the streptophyte lineage are required to
shed meaningful light on the gene networks that participate
in early sporophyte embryogenesis.
Returning to the antiquity of the isomorphic vs diplobiontic life cycle, a number of lines of evidence indicate that
the most ancient embryophyte life cycles were dimorphic.
First, extant monoploid embryophytes do not develop
apogamous sporophytes, suggesting that gene duplication
and subsequent functional divergence presaged the evolution of multicellular sporophytes, which is consistent with

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the extensive analysis of the Physcomitrella patens genome

(Rensing et al., 2008). Second, embryophyte sporophytes
and gametophytes normally develop in very different physiological and mechanical environments. Young sporophytes
develop within archegonia; free-living embryophyte gametophytes develop from dispersed meiospores. Third,
numerous environmental factors influence early morphogenesis that fosters dimorphism (Sinnott, 1960). Fourth, if
the most ancient sporophytes were an intercalated multicellular generation, it is difficult to imagine that they were
morphologically elaborate indeed, they may have been
nothing more than the functional equivalent of a sporangium (Niklas, 1997). Fifth, the different functional obligations of the gametophyte and sporophyte generations would
have sustained and even amplified their ancestral di-

(a)

morphism. Sixth, the purported life cycles of Rhynie

Chert plants (dated to 410 Myr), such as Rhynia, are not
isomorphic (Kerp et al., 2004; Taylor et al., 2005; Niklas
& Kutschera, 2009). Seventh, there is some evidence
(albeit, at this point, very problematic) that more ancient
tracheophytes, such as Zosterophyllum and Cooksonia
(Figs. 8,9), may have had dimorphic life cycles (Probst,
1986; Niklas & Banks, 1990; Remy et al., 1993; Gerrienne
et al., 2006).

X. Conclusions
Many details regarding the phylogeny of the green plant
lineages (chlorophytes and streptophytes) remain unresolved and will require more data from more taxa, part-

(b)

Fig. 8 (a) Upper part of a mature sporophyte

(sporangium, indicated by an arrowhead) of
Zosterophyllum rhenanum, an Early Devonian (c. 410 Myr old) vascular land plant. A
fossilized spore is shown in the inset. (b)
Reconstruction of the phenotype of a cluster
of plants (adapted from Edwards, 1969; and
Probst, 1986).

(a)

(b)

Fig. 9 Purported sporophyte (sporangia indicated by arrowheads) attached to its gametophyte (see arrow and shaded region in
inset) of Cooksonia paranensis, an Early
Devonian (c. 415 Myr old) vascular land
plant (a) and reconstruction of the phenotype (b). No vascular tissues or spores were
recovered from this fossil. Although spores
have been isolated from similar structures on
other fossils assigned to the same species, it
remains possible that the entire fossil is a
gametophyte (adapted from Gerrienne et al.,
2006).

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icularly from those residing at the base of this ecologically
rich clade. The broad phylogeny of the green plants is
nevertheless sufficiently well resolved to permit a reasonably stringent phyletic scaffold upon which to trace the
character transformations attending the evolution of the
embryophyte diplobiontic life cycle. Using this approach,
two conclusions emerge that will probably stand the test
of future scrutiny. First, the ancestral organism for the
entire green plant clade (and for the lineage leading to the
charophytes) was a flagellated eukaryotic photoautotroph
(Fig. 3), and, second, the ancestral organism to the streptophytes (Coleochaetophyceae, Charophyceae, and Embryophyta) was a multicellular alga that had a haplobiontichaploid life cycle and morphologically complex gametangia reminiscent of those of Chara (Fig. 6c,d). With far less
certainty, we surmise that the earliest land plants
(Figs 1a,8,9) had a dimorphic diplobiontic life cycle in
which the haploid (gametophytic) phase dominated. Subsequent evolutionary divergence led to land plant forms
that retained this ancestral condition (represented today by
the extant bryophytes) and lineages in which the diploid
generation became dominant (represented by all extant tracheophytes, notably the seed plants, Fig. 1b). Although
speculative, we further suggest that there is sufficient
observational and molecular data to indicate that the
reproductive organs of embryophytes (i.e. archegonia, antheridia, and eusporangia) are homologous structures
(sensu Shubin et al., 1997) that, in turn are homologous
with the multicellular gametangia of the charalean algae
(the nucule and globule) (Fig. 7). These homologies
appear to be the result of the co-option and re-deployment
of ancient algal gene networks.
Much speculation surrounds the properties of genes,
gene networks, and even entire organisms that favor pivotal evolutionary transformations that nevertheless conserve structural and genomic homologies. Although the
evidence is sparse, speculation favors the effects of regulatory genes, in general, and transcription factors, in particular, as the most probable drivers of evolutionary
innovation (see Doebley & Lukens, 1998; Cronk, 2001).
However, the few detailed studies of plant developmental
gene interactions are insufficient to justify this view to the
exclusion of other potentially equally important mechanisms, as witnessed by the recent finding that the developmental patterning of the highly reduced angiosperm megagametophyte depends on an asymmetric, location-specific
gradient of auxin synthesis (Pagnussat et al., 2009). For
this reason, we conclude that future enquiries into the
developmental mechanism(s) by which the embryophyte
life cycle evolved would profit from detailed diagnoses of
the molecular drivers of the plant cell cycle, the induction
of meiotic versus mitotic cell division, and a host of other
fundamental phenomena. Scrutiny of meiotic gene candidates and factors that contribute to homologous chro-

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mosome pairing will be a particularly important and fertile

field of inquiry (see Able et al., 2009).

Acknowledgements
We thank Dr. P. Gerienne for providing Fig. 9a and Dr. J.
Raven (the University of Dundee, UK) for many useful suggestions. We also thank the College of Agriculture and Life
Sciences (Cornell University, Ithaca, USA) and the Alexander-von Humboldt-Foundation (AvH, Bonn, Germany) for
financial support (AvH-fellowship 2009, Stanford California, USA to U. Kutschera).

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