EVOLUTIONARY BIOLOGY: A Plant Perspective
THE FIRST LAND PLANTS
The emergence of green life from the
water was inevitable— the more abundant
resources available on land were not likely to
remain unexploited for long. The ancestors of
land plants— the charophyte algae- were
probably dependent on precipitation and
runoff from dry land as the primary source of
inorganic nutrients. With nutrient availability
as a primary limitation to plant growth in the
water, it was just a matter of time before the
appropriate innovations appeared to allow
colonization of terrestrial habitats. Survival
on land required overcoming severe drying
and exposure to sunlight; strong selection
gradients existed at the water’s edge where
periodic exposure favored desiccation
resistance. Under these circumstances any
adaptations that improved tolerance to drying
or the extraction of water and nutrients from
the substrate would have spread, allowing
early colonizers to incrementally invade drier
habitats.
These first stages of transition to
terrestrial habitats remain entirely unknown.
There are no living plants that retain the
morphological characteristics of the earliest
land plants, and we do not have any fossils
that can definitively be associated with
transitional forms. While plants in the
Bryophyta (mosses, liverworts, and
hornworts) are often referred to as
representatives of the earliest land plants,
they actually are quite divergent and possess
a number of complex traits that make them
much more similar to other land plants than
to streptophyte algae. For example, all
bryophytes have a multicellular sporophyte
stage (haplodiplontic life cycle) that is
complex in contrast to the unicellular zygote
of streptophytes (haplontic life cycle).
Furthermore, each of the bryophyte lineages
possesses suites of characteristics that are
unique compared to each other and to other
embryophytes, suggesting that they diverged
from a much simpler common ancestor (Qiu
et al. 2012). The characteristics shared among
bryophyte groups include a multicellular
sporophyte, parenchymous (i.e.,
undifferentiated cell) growth of the
gametophyte, apical growth, and complex
reproductive structures. The commonality of
these traits among bryophyte lineages
suggests that the common ancestor they share
with other land plants (vascular plants, the
Tracheophyta) probably possessed the same
set of traits. On the other hand, Bryophytes
differ from other vascular plants by having a
dominant gametophyte stage, a dependent
sporophyte stage, and the lack of true
vascular tissue (Tracheids). Sporophytes and
gametophytes of some mosses possess
conducting cells (Hydroids) that serve as
vascular tissue (the Hydrome; Ingrouille and
Eddie 2006), but since most bryophyte
lineages do not have this feature, it is more
likely that hydroids are independently
derived and not homologous to the vascular
tissue of the tracheophytes. This scenario is
supported by the observation that conducting
cells in moss sporophytes and liverwort
gametophytes lack the cell wall thickenings
and lignification present in the tracheids of
vascular plants (Ingrouille and Eddie 2006).
By considering the distribution of
shared traits among extant lineages of
embryophytes and streptophyte algae, we can
Mitchell B. Cruzan (2018) 1
 EVOLUTIONARY BIOLOGY: A Plant Perspective

make some logical guesses about the with consistent moisture availability and
probable characteristics of the first land some shade until adaptations appeared that
plants. We can infer that the first fully allowed them to survive in more exposed
terrestrial lineages were small plants that had sites.
a dominant gametophyte stage, and a diploid
As terrestrial lineages spread and
stage that was either a unicellular zygote or a
became more abundant, competition would
simple multicellular sporophyte that was
have ensued as habitat space with sufficient
dependent on the gametophyte (traits shared
moisture became limiting to growth.
with bryophytes and streptophyte algae). The
Selection on terrestrial populations would
gametophyte stage was probably a Thallus (a
have favored traits that contributed to their
flat plant body consisting of undifferentiated
ability to colonize new habitat and to
cells, lacking specialized tissues and organs)
compete with other members of the plant
that had apical growth and unicellular
community. For example improved
Rhizoids (hair- like extensions of cells that
resistance to desiccation would have allowed
serve the same function as roots)— traits
survival in drier habitats, better dispersal
shared with the gametophytes of hornworts,
ability, and more drought- resistant spores
liverworts, lycopods, and ferns. These plants
would have promoted the colonization of new
were restricted to areas of constant moisture,
habitats.
as they possessed little capacity to maintain
their internal water status. Other traits present The process of colonization of drier
in different embryophyte lineages such as habitats may have been facilitated by the
multicellular rhizoids, stomata, Poikilohydry, development of mutualistic associations with
and Vasculature, are not shared across the glomalean fungi, which had been present on
entire clade, so they are unlikely to have been dry land at least since the Ordovician
present in the earliest land plants and are (Redecker et al. 2000) and probably since the
probably independently derived in each Neoproterozoic. These fungi form symbiotic
lineage. relationships with plants (Mycorrhizae) and
may have been instrumental in the
The picture that emerges for the first
establishment and spread of plants across
terrestrial plants is one of small, thalloid
terrestrial habitats (Brundrett 2002; Bonfante
gametophytes with limited ability to maintain
and Genre 2008). Fossils of mycorrhizae date
their internal water status and so remaining
from the early Devonian, 460 mya (Remy et
closely appressed to a moist substrate. These
al. 1994), but mycorrhizal fungi are likely to
plants had a dominant gametophyte stage and
have been associated with the earliest land
probably produced motile sperm, so they
plants. The importance of plant- fungal
required water for successful reproduction.
mutualisms for the success of early land
The diploid stage would have been a
plants is supported by the observation that
unicellular zygote (similar to charophyte
DMI genes, which are important for plant-
algae) or a reduced multicellular sporophyte
microbe interactions, are present in all major
(similar to liverworts). These first terrestrial
embryophyte lineages (Wang et al. 2010).
plants may have been limited to locations

Mitchell B. Cruzan (2018) 2

 EVOLUTIONARY BIOLOGY: A Plant Perspective
ORIGIN OF THE LAND PLANTS
Dating the Origin of Embryophytes
Plants were not the first terrestrial
inhabitants. Microbes and fungi were well
established on dry land and had been there for
some time before plants first ventured out of
their aquatic environs (Fig. 2.2). There is
geological evidence that microbial mats
affected geochemical processes in terrestrial
environments during the Paleoproterozoic, as
early as 2,600 mya (Watanabe et al. 2000),
and the first microfossils of terrestrial
bacteria date from around 800 mya
(Horodyski and Knauth 1994). The first
eukaryote inhabitants of land were probably
fungi that were associated with cyanobacteria
to form lichen- like symbioses (Heckman et
al. 2001), which may have been important for
promoting the chemical degradation of rock
(Schwartzman 1999). Inferences from
molecular phylogenies are consistent with the
hypothesis that lichens inhabited land as early
as 720 mya, but the first unambiguous fossil
evidence of lichens comes from around 600
mya (Yuan et al. 2005). These early
terrestrial inhabitants, along with weathering
and erosion by wind and water, contributed to
the accumulation of fine- grained inorganic
material and the release of nutrients (e.g.,
nitrogen and phosphorous), which would be
important for the establishment and spread of
early land plants.
The timing of the emergence of the
first terrestrial plants remains equivocal, as
estimates from molecular phylogenies for the
origin of the embryophytes are consistently
much earlier than the dates indicated by
fossils (Fig. 2.2). The first fossil evidence of
terrestrial plants comes from the early
Paleozoic (~450 mya), but molecular clock
estimates date the split between
embryophytes and streptophyte algae much
earlier, between 568 and 815 mya during the
Neoproterozoic (Clarke et al. 2011). The
wide range of dates for the origin of land
plants from phylogenies is due to variation
among gene regions sequenced and the use of
different methods for date calibration;
however, even the youngest estimates fall
well before the age of the oldest embryophyte
fossils. There are several possible reasons for
the discrepancy between dates of the oldest
fossils and age
estimates from phylogenies. One is the
tendency for the fossil record to be biased
toward younger dates. Fossilization is very
rare and only occurs under specific chemical
and physical conditions (Willis and
McElwain 2002), so organisms that are
abundant and have been present for some
time are more likely to leave a record. Nearly
all organic matter— especially from
organisms that lack hard parts— will rapidly
decay and leave no trace of the original form.
In the rare cases where early land plants may
have left a record, most fossils were lost due
to geological processes occurring over
tremendous spans of time. It is likely that
streptophytes were present in terrestrial
habitats for a considerable amount of time
before geological processes captured
evidence of their existence.
A second reason for the appearance of
fossil land plants much later than their
divergence from the algal streptophytes
comes from difficulties with the
identification of fossils that represent the
earliest terrestrial plant forms. The early
fossil record contains many unidentified
objects referred to as Acritarchs (literally,
“confused origin”) that could represent key
evidence of the earliest land plants or could
be products of physical processes. For
consistency, it is necessary to
use unambiguous characters for the
identification of fossils. For example, some
of the first macrofossils that are clearly
representative of embryophytes come from
Mitchell B. Cruzan (2018) 3
 EVOLUTIONARY BIOLOGY: A Plant Perspective
the early Devonian (e.g., Cooksonia; Fig.
2.3). In this case the presence of terminal
sporangium was used to classify these fossils
as representatives of early land plants, but the
species represented by these fossils was far
removed from the first land plants as they
displayed more advanced traits such as a
hydrome- like vascular tissue and complex
reproductive structures (Ingrouille and Eddie
2006). More recent discoveries of microfossil
evidence have pushed back the appearance of
land plants to the late Ordovician (around 450
mya; Fig. 2.2); fossils that may once have
been passed over as acritarchs were classified
based on their close resemblance to the
spores of modern bryophytes (Rubinstein et
al. 2010). There may be other unidentified
microfossils that could provide key insights
into the origin of land
plants.
Fig. 2.3. A depiction of the fossil plant
Cooksonia. Plants were several decimeters tall
with terminal sporangia, and vascular tissue in
the stem and rhizomes. Original art by Michelle
Nicole Williamson.
For example, a particular class of
acritarchs from the Cambrian were not
associated with Coleochaetophytes until
these streptophyte algae were found to
produce similar structures when grown under
environmental conditions designed to mimic
an emergent aquatic habitat (Graham et al.
2012). Identification of these microfossils
provides important evidence that desiccation-
resistant streptophytes may have been present
on moist terrestrial substrates during the early
Paleozoic around 515 mya— a date that
corresponds more closely with estimates for
the origin of embryophytes from molecular
phylogenies. Given the large diversity of
unidentified fossils that occupy museums and
labs around the world, it is likely that there
are many more examples of acritarchs that
have the potential to provide important clues
about the nature of the earliest land plants.
The Transition to Land
There was a long road of
divergence— several hundred million
years— from the time of the emergence of the
first terrestrial streptophyte algae to fossils
that provide evidence of the earliest land
plants. We do not have fossils of the pivotal
transitional stages from aquatic to terrestrial
habitats, and there are no living descendants
that possess the mixtures of traits we would
expect to find in transitional forms. As
mentioned above, the earliest definitive
fossils are from the Ordovician and closely
resemble the spore stages of modern
bryophytes. Given the resemblance to
modern bryophytes, it is likely that these
plants had already acquired a complex life
cycle and a high level of morphological
complexity (e.g., modern bryophytes have a
multicellular diploid phase, stomata, vascular
tissue, and relatively complex reproductive
structures; Graham et al. 2012). In contrast,
the multicellular streptophyte algae bear little
resemblance to bryophytes as they have
Mitchell B. Cruzan (2018) 4
 EVOLUTIONARY BIOLOGY: A Plant Perspective
unicellular diploid life stages and their
gametophytes have simple anatomy and
morphology. From the difference in
morphological complexity between
streptophyte algae and bryophytes we can
infer that the first terrestrial plants must have
emerged much earlier than the oldest fossils
of bryophyte- like spores. It is also possible
that the lineage that ultimately produced
terrestrial embryophytes remained in aquatic
environments for some time before making
the transition to land. During the
Neoproterozoic (as early as 850 mya) the
green algae diverged into two major clades
with lineages of streptophyte algae
diversifying in fresh water habitats, while
the chlorophyte algae were restricted to the
oceans (Fig. 2.4; Becker and Marin 2009).
The oceans were dominated by unicellular
cyanobacteria and glaucophytes, unicellular
and multicellular rhodophytes, and
chlorophyte algae. While land plants share
many traits with all of the green algae,
phylogenetic evidence places the origin of
embryophytes firmly among streptophyte
lineages, which indicates that the transition
to land occurred from freshwater instead of
marine habitats (Fig. 2.4). During the late
Neoproterozoic through the early Paleozoic,
the streptophytes (including the charophytes)
were the only algae occupying fresh water; it
is likely that a combination of the ecological
conditions present in lakes and ponds and a
unique set of traits possessed by these algae
facilitated the transition to dry land.
Living in freshwater would have
provided an easier pathway to drier habitats
because the change in salinity between
aquatic and terrestrial environments was mild
compared to that between the ocean, with its
much higher salt content, and the land
(Becker and Marin 2009). The combination
of a strong salinity gradient along with
dehydration, gravity, extremes in
temperature, high irradiance, and ultraviolet
radiation made the transition to life outside of
water much more difficult for marine
organisms. We can assume that the osmotic
challenge for marine algae would
have been substantial during the
Neoproterozoic and early Proterozoic
because the salinity levels
in the oceans were at least as high as they are
today (Knauth 2005). The ecological
conditions afforded by freshwater habitats
and the evidence from molecular phylogenies
corroborate a scenario in which land plants
originated from streptophyte ancestors in the
lakes and ponds of continents rather than
from green algae inhabiting the ocean.
Fossil evidence indicates that ponds
and lakes were dominated by streptophyte
lineages through the Cambrian, until their
numbers declined as chlorophytes invaded
and diversified in continental aquatic habitats
starting around 400 to 490 mya (Becker and
Marin 2009). Divergence among the major
clades of multicellular streptophytes
(charophytes, coleochaetophytes,
zygnemataphytes, and embryophytes)
occurred much earlier during the
Neoproterozoic according to molecular clock
estimates (Fig. 2.4). With scant fossil
evidence available, we can only infer that
adaptations allowing colonization of drier
habitats were acquired at some point during
the Neoproterozoic, but we do not know
whether the terrestrial transition began at
origination of the embryophytes or at some
time later during the early Paleozoic. It is
possible that early embryophytes remained
aquatic through the end of the
Neoproterozoic, since the fossils of these
earliest plants may be difficult to identify and
descendants of the transitional forms did not
persist. It would be difficult to know whether
aquatic embryophytes had been around in the
Paleozoic since freshwater streptophyte
diversity declined by the end of the Permian
(250 mya) when they were replaced by
Mitchell B. Cruzan (2018) 5
 EVOLUTIONARY BIOLOGY: A Plant Perspective

Fig. 2.4. Phylogenetic relationships within the Archeaplastida and historical habitat distributions of the
major groups. Topology is based on Finet et al. (2012). Divergence dates are approximate.

any one of several algal streptophytes. The

chlorophytes. Descendants of the putative
ancestral aquatic embryophyte lineages may
have been lost due to competition with
chlorophyte algae during the Permian, and
other streptophyte algae continue to remain
much less common than chlorophytes
(Becker and Marin 2009).
Identifying the Closest Relatives
Embryophytes
The branching order among major
streptophyte lineages remains ambiguous
(Fig. 2.4 represents one hypothesis), so the
closest ancestor to embryophytes could be
charophytes have been proposed as the most
likely sister clade to embryophytes because
they possess apical growth and other
characters that superficially resemble land
plants. On the other hand, members of the
coleochaetophytes have been found to be
desiccation tolerant and to share additional
traits with embryophytes (Graham et al.
2012). By comparing characteristics of land
of plants with different groups of green algae we
can begin to piece together the history and
possible origin of the embryophyte clade.
All of the green algae share
characteristics with land plants, including
chlorophylls a and b as their primary
photosynthetic pigments and storage of
starch within plastids. This collection of
characters alone is not diagnostic, but a

Mitchell B. Cruzan (2018) 6

 EVOLUTIONARY BIOLOGY: A Plant Perspective

number of other traits place the origin of land
plants firmly within the streptophyte algae.
The most prominent of these is the retention
of the mitotic spindle during formation of
the cell walls between daughter cells. This
mode of cell wall construction
(Phragmoplast) allows for the development
of Plasmodesmata that connect the
cytoplasms of adjoining cells and establishes
the Symplast, which provides continuous
communication of cytoplasm throughout the
multicellular plant body. In the chlorophytes,
the spindle fibers dissolve prior to telophase
and plasmodesmata do not form. The
chlorophytes also possess an extra
external cell wall (the Theca), which restricts
the expansion of daughter cells. The lack of a
theca and the presence of plasmodesmata in
streptophytes were critical pre- adaptations
for the evolution of a multicellular plant.

Fig. 2.5. During the development of the phragmoplast remnants of the spindle microtubules remain. The new cell
wall develop as fragments along the equator of the mitotic spindle. Fragments fuse to form the new wall of each
daughter cell, but adjoining openings remain to form the plasmodesmata that connect the cytoplasms of each cell.

A phragmoplast is shared by all the lineages of streptophyte algae

multicellular lineages of streptophytes (Fig.
2.4), but the Charophyta is the only group of
macrophytes that also possess the capacity
for apical growth. The morphological
similarity of charophytes with land plants
(e.g., Chara) has led to the assumption that
they are sister clades; however, not all of the
available evidence points to any particular
streptophyte lineage as the closest relative to
the embryophytes. For example, the chemical
characteristics of the cell walls of several
(Zygnematales, Coleochaetales, and
Charales) are similar to embryophytes, and
lignin- like compounds, which are
characteristic of embryophytes, have been
found in species of Coleochaetales (Graham
et al. 2012).
There are also strong similarities
between the transcriptomes of land plants and
species in the Zygnematales and the
Coleochaetales (Timme and Delwiche 2010),

Mitchell B. Cruzan (2018) 7

 EVOLUTIONARY BIOLOGY: A Plant Perspective
and a number of proteins formerly thought to
be “plantspecific” have been found in several
different lineages of streptophyte algae
(Becker and Marin 2009).
This situation is further confused because a
number of embryophyte genes thought to be
important
for adaptation to terrestrial environments are
found in streptophyte algae, but not all of
them are present in any single group (Leliaert
et al. 2012). The distribution of land plant
genes suggests that a single common ancestor
possessed all of them, but different genes
may have been lost in some algal lineages and
not others. The stories told from molecular
phylogenies based on genomic regions that
are not associated with the terrestrial
transition are just as conflated, with separate
studies indicating the closest clades as the
Charales (Qiu et al. 2006), the Zygnematales
(Turmel et al. 2007), the Zygnematales
combined with the Coleochaetales (Wodniok
et al. 2011), while one broad phylogenomic
survey of taxa placed the embryophytes
nearest to the Coleochaetophytes
(Finet et al. 2012).
Such phylogenetic confusion may
indicate that the lineage with the closest
affinity to the
embryophytes has been long lost, and the
phenotypic and genomic compositions of the
remaining lineages have been modified as
they diverged over hundreds of millions of
years. Consequently, each remaining
streptophyte shares some characteristics with
others in the same clade and with the
embryophytes. Given the scattered nature of
shared characteristics across these two
groups, it is likely that the divergence of the
land plant lineage was basal within the clade,
indicating they were derived from an earlier,
and perhaps less complex, streptophyte alga
(Fig. 2.4; Finet et al. 2012).
Because embryophytes share
different sets of characters with several algal
lineages, it is most likely that they diverged
early in the history of the streptophyte clade.
Under this scenario, ancestral embryophytes
may have possessed many of their unique
traits at the time they diverged and may have
started occupying emergent habitats during
the late Neoproterozoic. Terrestrial forms
may have arisen later, so the green life
surrounding ponds and extending into
habitats with reliable water availability was
probably present for some time before they
left definitive fossil evidence of their
presence.
The collective evidence from
phenotypic and genomic studies supports an
early divergence of the embryophytes from
morphologically simple streptophyte algae in
the Neoproterozoic. This scenario suggests
that the first embryophytes may have been
aquatic and transitioned to land somewhat
later. It is also evident that the modern
representatives of clades that have been
viewed as the closest relatives to land plants
(e.g., Zygnematales, Coleochaetales, and
Charales) are substantially derived compared
to common ancestors with embryophytes. For
example, even though members of the
Charales display superficial resemblance to
some embryophytes— with node- like
regions and whorls of leaf- like structures
similar to land plants such as Equisetum—
their development and anatomy is quite
different from embryophytes (Ingrouille and
Eddie 2006;
Lee 2008).
It is also the case that we may not
expect land plants to display strong
similarities to any particular algal lineage
because the likely timing of emergence of
embryophytes does not correspond well with
the history of modern streptophytes. For
example, fossil evidence suggests that
Mitchell B. Cruzan (2018) 8
 EVOLUTIONARY BIOLOGY: A Plant Perspective

anatomically modern representatives of the

Charales and Coleochaetales did not appear
until the Silurian (excepting the
Coleochaetelike acritarchs discussed earlier
in this chapter)— well after the origin of
embryophytes. These streptophytes remain
aquatic even though they may have some
potential for survival out of water for short
periods (e.g., Graham et al. 2012).

Nonetheless, it is clear that the

earliest land plants were derived from
lineages that arose from within the
streptophyte clade. It is also apparent that
early streptophyte lineages possessed Key
Adaptations (e.g., phragmoplast,
plasmodesmata, apical growth, resistant
spores, etc.) that were critical for the
evolution of multicellular growth and success
in terrestrial habitats. Because of the probable
early divergence of streptophyte lineages,
further pursuit of a single closest lineage to
embryophytes may be difficult. There is
much to learn about the process of adaptation
to terrestrial conditions that occurred in the
earliest land plants, and the best path forward
in this endeavor may lie in genomic
comparisons of these groups (Becker and
Marin 2009; Leliaert et al. 2012).

Mitchell B. Cruzan (2018) 9