Another reason for chlorophytes not making land is that there seems to be
something intrinsically difficult about switching from the salty oceans to terrestrial habitats. Being pre-adapted to freshwater somehow predisposes you towards
successful colonization of dry land.27 It is perhaps easy to imagine the gradual
movement of plants from freshwater to land by way of moist habitats that were
subject to drying up from time to time and refreshed when the rains came.28
Moving out of the salty oceans into freshwater, on the other hand, appears simply too dramatic and presents serious physiological challenges not easily overcome.
Drastic metabolic adjustments are required to protect against the osmotic
onslaught that ensues. If you take a freshwater species and submerge it in saltwater, life-sustaining moisture is drawn out through permeable membranes, caus-
ing death by dehydration. A saltwater species submerged in freshwater will
succumb to the same osmotic action in reverse. Interesting evolutionary parallels can be drawn here between plants and animals that reinforce the idea. Insects
originated in freshwater rather than marine environments, and amphibians and
insects are still completely absent from the oceans.29 Likewise, very few flowering plants moved into the sea after evolving from freshwater algae. Seagrasses are one of the few exceptions, and in so doing they shed parts of the genome for surmounting physiological obstacles to living on land.30 A highly unusual group of
flowering plants, seagrasses carpet the floors of shallow seas with strap-like leaves to form coastal meadows, with an astoundingly high level of productivity, comparable to that of fertilized maize fields or sugarcane plantations.
We are left with the charophyte algae as the closest living relatives of land
plants, a fact regarded as ‘proven beyond reasonable doubt’. The question of
which charophyte lineage is the closest immediate ancestor of the earliest land
plants is being hotly pursued. The answer would allow us to uncover the key fea-
tures enabling such algae to make the important transition to a terrestrial life-
style. In the 1980s, many botanists were convinced that a distinctive group of
pondweeds called stoneworts (the Charales) were the closest living algal relatives of land plants,31 with the Coleochaetales32 ranking a close second. Rank outsiders, at that time, were a third group called the Zygnematales33 (Plate 2). None of them is exactly a household name, and none trip off the tongue, so a few words of
explanation are in order.
FiFty shades oF green a 23
Forced to pick which of the above three groups of algae best resembles a proto-
land plant, you would probably take a punt on the stoneworts.34 This intriguing
group, consisting of several hundred species worldwide, has cell walls that are
heavily calcified and a tendency to become encrusted in calcium carbonate (lime-
stone)—hence the name.35 Their characteristic calcification has resulted in some
closely related 400-million-year-old fossil specimens, beautifully preserved, with similar distinctive male and female reproductive structures.36 Modern forms can
look suspiciously more like vascular plants than green algae, with a central stem formed from giant cells linked end-to-end for tens of centimetres, and whorled
‘branches’ budding off at nodes along the stem. Dwelling in ponds, and more
exotically in deep, clear volcanic crater lakes, these relicts are among the largest and most complex of all freshwater green algae and are often the first to colonize ponds that dry up in the summer. When the family tree of the charophytes is drawn based on inherited characteristics and their DNA, we find a satisfying stepwise
evolutionary progression in complexity, moving from simple single-celled forms
to more structurally complex multicellular forms appearing immediately prior to
the origin of land plants.37
Elegant and apparently satisfying though this story may be, new large-scale
DNA sequencing projects are radically revising our thinking about the origins of
land plants, and suggest this earlier interpretation is quite wrong. Land plants
instead likely arose from what are now far simpler algae,38 with the finger of taxonomic suspicion now pointing to those within two ancient groups: Coleochaetales
and the Zygnematales. Composed of microscopic branching filaments, some-
times equipped with flagella for swimming, Coleochaetales algae could not
look more different from the complex Charales. Superficially, the Coleochaetales
have few physical features in common with land plants, but they share hidden
biochemical and structural features with them,39 and a few modern forms can
stubbornly survive and reproduce on mineral grains after a week or so out of
water.40 Fossils bearing a strong resemblance to some members of the living genus Coleochaete turn up in 400-million-year-old early Devonian strata, although these are substantially larger than any known extant representatives.41 The last of the ancient groups of charophytes, and also the largest and most diverse of the
living groups of green algae, the Zygnematales, look even less like land plants
than the Coleochaetales, but are the current favourites to be the closest algal
ancestors of plants. Forming single cells, filaments, chains of cells, and colonies,
24 a FiFt y shades oF green
they have been observed under the microscope for their scientific interest and
intrinsic beauty, and yet overlooked as possible progenitors of land plants, for
over a century.
If the Zygnematales or Coleochaetales are most closely allied with land plants,
we might wonder how the simple structure of their modern forms can be recon-
ciled with complex terrestrial plants. It appears to run counter to our expectation that evolution produces complex life forms from simpler ancestors. The answer is
that it is quite possible, probable in fact, that over time there have been reductions in the complexity of modern forms compared to their more complex ancestors.
Since they last diverged from a common ancestor, each algal group has followed
its own evolutionary trajectory for hundreds of millions of years, and in the case of the Zygnematales this may have led to a reduction in complexity of modern
forms. So we should be mindful that the appearance of the modern forms we see
today can be misleading.
Nevertheless, probably by virtue of being in the right place at the right time,
charophyte algae gave rise to the first plants that ventured onto land to make a
living beneath the sky. As those elementary grades of land plants slowly took
hold, creeping over muddy sediments, they flecked the desolate, windswept valley
floors with new shades of green. The closest surviving relatives of those early
land-seeking pioneers are simple plants called the bryophytes, whose life history and biology open a window on their long-extinct ancestors.42 The bryophytes
comprise the liverworts, mosses, and hornworts. These organisms are typically
small plants, reaching a few centimetres in height, and grow under damp conditions.
Some are tolerant of desiccation and able to endure extreme heat, like our Mojave Desert mosses. The evolutionary relationships among the bryophytes, and between
them and vascular land plants, are controversial. Almost all possible permuta-
tions have been proposed at one time or another, a situation reflecting what is
widely regarded as one of the most recalcitrant and frustrating problems in land
plant evolutionary biology.43
Regardless of the confusion surrounding the kinship of bryophytes
, there is a
close resemblance between the fossilized spores of the earliest land plants and
those of liverworts. Charles Wellman of the University of Sheffield made the
discovery after his detailed investigations of ~460-million-year-old Ordovician
rocks from Oman.44 His fossils included spores and remarkable fragments of
FiFty shades oF green a 25
spore-producing plants in the form of specialized reproductive structures called
sporangia, still loaded with spores. Slicing through the fossil spores, he discovered that the wall is constructed in distinctive layers, sandwiched together in a way
similar to that found in modern liverwort spores. The oldest fossilized bryo-
phytes are also classified as liverwort-like, and are older than those thought to represent mosses and hornworts by hundreds of millions of years.45 We have
thick mats of fossilized liverworts excavated from 380-million-year-old sedi-
ments by quarrying in New York State46 and a rare liverwort specimen in rocks
from South-west China dated as 411–407 million years old.47 These discoveries
provide direct fossil evidence for advanced groups of liverworts on land over 400
million years ago.
And there, frustratingly, the trail of fossil evidence runs cold, but a clue to what the mysterious earlier forms might have looked like comes from the latest taxonomic hierarchy of liverworts, identifying the extreme antiquity of the Haplomitriopsida.
Comprising just three genera, Treubia, Apotreubia, and Haplomitrium, this class of primitive liverworts may have an ancestry reaching back 450 million years.48
Strange-looking plants, they are quite unlike the 400-million-year-old fossilized liverworts discovered in the USA and China. Those of the genus Treubia have prostrate green shoots adorned with small leaf-like structures folded upwards like
miniature wings, giving the plants a ruffled appearance. Those in the other
significant genus, Haplomitrium, are different. They grow with subterranean rhizomes and erect stems adorned with rounded leaf-like structures.49 Could these
plants, belonging to the least celebrated and oldest living liverwort lineage, be furnishing us with a tantalizing glimpse of the earliest terrestrial plant life?
Fossil spores extracted from ancient rocks hint at the nature of land floras back in the Ordovician (485–444 million years ago), when simple proto-bryophyte
plants began to give Earth’s continents a patchy green photosynthetic veneer.50
But does the record of fossilized spores accurately date when plant life began to make tentative moves on to land? As we have seen, this would have been a subtle
event, involving very simple photosynthesizing life forms that had evolved from
algae. Little, if anything, of this change may have survived in the fossil record.
Those first land plants still had to become sufficiently numerous and widespread
to be captured by accidents of fate and preserved in stone. Fossils therefore tend to post-date the actual time of land-plant origination by some unknown duration,
26 a FiFt y shades oF green
usually providing what is regarded as the youngest age estimate for when land
plants appeared. The ‘unknown duration’ constitutes a ‘known unknown’ and is
contingent on measures like the ecology of the organisms, their preservation
potential, and the nature of the rock record.
Philip Donoghue at Bristol University elegantly addresses these sorts of
seemingly impossible questions by exploiting the clock-like properties of
DNA molecules.51 Nobel Prize-winning chemist Linus Pauling (1901–1994)
and his colleague the Austrian-born French biologist Émile Zuckerkandl
(1922–2013) originally proposed the concept while working on haemoglobin
molecules back in the 1960s. It is based on observations showing that genetic
mutations, although random, occur at a relatively constant rate, which means that the number of differences between any two gene sequences increases at a
predictable rate over time. At least in theory. In other words, instead of meas-
uring time in the usual units of seconds, hours, days, and so on, molecular
clocks measure time as the number of mutations in a particular gene sequence.
As with regular timepieces, molecular clocks have to be calibrated, and this is
usually done with a dated fossil specimen for a specific lineage. Once the rate
of mutation is determined, calculating the time of divergence of that species is
relatively straightforward. If the rate is 5 mutations every million years, and
you count 25 mutations in your DNA sequence, then your sequences diverged
5 million years ago.
Of course, there is more to it than this, but the basic idea holds true, and
Donoghue is a whizz at crunching complex numerical algorithms with com-
puter software. Molecular clocks, calibrated by fossils, give a timescale by which the plant tree of life has unfolded that may help in overcoming the unreliability of fossils for dating the origin of land plants. If Donoghue’s team have a sensible grasp on Pauling and Zuckerkandl’s molecular chronometers, the sensational
outcome of their latest work is to propose nothing less than redrawing the time-
line of green evolution.52 Their suggestion is that plant life emerged onto land
sometime in the middle Cambrian–early Ordovician world (515–470 million
years ago). We have no firm fossil evidence for land-plant existence towards the
older end of this range, as his team readily acknowledges, but should this be an
obstacle to accepting the DNA evidence? Wellman gives the idea short shrift,
arguing that his spores are indestructible and once land plants began reprodu-
cing by wind-blown spores they would soon be dispersed and turn up in marine
FiFty shades oF green a 27
and terrestrial rocks. Could a dusting of such spores around the planet have
been hidden from rocks cleaved by the blows of a geologist’s hammer or their
vats of rock-dissolving hydrofluoric acid for so long? Wellman, and his palaeo-
botanical colleagues who collaborate with Donoghue, doubt it, but the fact is
few unequivocally terrestrial rock formations that could document the con-
quest of the land by plants much older than 450 million years are still in exist-
ence.53 The upshot is that Donoghue’s controversial early date for the origin of
land plants is hard to test54 but it has prompted palaeobotanists to turn their
attention towards the more complete geological record of marine rocks that
might capture crucial evidence of the tough powdery spores. If we lean towards
the younger end of the range, it fits together with dates for the arrival of animals that fed on plant remains, such as arthropods and their relatives,55 but that date is also obtained using molecular clocks with algorithms suffering similar issues
of uncertainty. Understandably, the prevailing opinion is one of scepticism. Yet
ancient Scottish deposits have yielded fossil discoveries pointing to the exist-
ence of freshwater algae in pools a billion years ago.56 Were ancient freshwater
algae plus a few hundred million years sufficient to boot up simple forms of
terrestrial plant life?57
Regardless of the exact timing of the origin of our land floras, once plant life
established itself on land, the stage was set for evolutionary escalation; there was no turning back. The green fuse of land-plant evolution was lit, and was not about to be extinguished anytime soon. The pull of a terrestrial lifestyle proved
irresistible . Limitless supplies of solar energy rainin
g down from the sky and a luxurious carbon dioxide-rich atmosphere fuelled photosynthesis.58 Despite the
challenges of coping with intermittent supplies of water and nutrients from thin
primitive soils, the ‘pull of the photon’ made living on land irresistible. Endless ecological possibilities offered by the open terrestrial landscape were soon
exploited as successive waves of vascular plants followed the early photosynthetic pioneers in populating the continents.59 Vascular plants appeared with their hallmark stiffened stems, with internal tubes conducting water and dissolved mineral
nutrients taken up from the soil. Some vascular lineages rose to great ecological success, shining brightly in the terrestrial world for tens of millions of years before fading and being replaced by other more successful groups. The story is chronicled by DNA and fossils, precious stony way-markers of the directionality of
plant life’s emboldened exploration of the terrestrial realm.
28 a FiFt y shades oF green
The living descendants of this botanical drama are still with us in the shape of
clubmosses and their relatives (lycophytes) and ferns (pteridophytes). Lycophytes have the distinction of being the oldest living lineage of vascular plants. Their fossil history is thought by some to reach back to a fossil plant called Baragwanathia, controversially dated to 420 million-year-old Silurian strata in Australia. Fossilized shoots of Baragwanathia bear close comparison with those of its modern lycophyte relatives. Lacking true leaves or roots, and reproducing with spores rather than
seeds, the lycophytes represent an interim step in plant evolution. Stems were
cloaked in small scale-like leaves adorned with microscopic stomatal pores, and
underground parts of the plants were anchored into the fine substrate by simple
rootlets.60 Supported by woody or lignified shoots, vascular plants began to grow upwards in the struggle for light. Long-extinct relatives of lycophytes grew to be giants, reaching magnificent heights of over thirty metres. They towered over the primordial Carboniferous swamp forests 300 million years ago.
Other groups of fern-like plants soon appeared, joining the burgeoning diver-
sity of bryophytes and lycophytes in greening the landscapes of the Devonian
world. With upgraded leaves for harvesting solar energy, and stems plumbed into
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