thin air, a hundred million years before vertebrates.
We might look to Darwin’s The Origin of Species for some answers to questions concerning the mysterious origins of terrestrial plant life. Yet after scrutiny of all
8 a All flesh is gr Ass
460 dense pages of the evolutionary master’s elegant prose, we finally discover
that his magnum opus remains silent on the thorny issue of the origins of land
plants. Darwin was no fool. He builds a highly original picture of the struggle for existence and evolution by natural selection through Herbert Spencer’s (1820–
1903) memorable phrase ‘survival of the fittest’. His theory of evolution was an
incendiary intervention in the midst of Creationist orthodoxy, but he refused to
be drawn into publishing his thoughts on the question of the origin of life, preferring instead to confine them to a private letter to his friend the botanist and
Director of the Royal Botanic Gardens, Kew, Sir Joseph Hooker (1817–1911). Here
he cautiously asks ‘if (and oh what a big if) simple life may have got going “in some warm little pond”…’. He showed similar reticence when it came to the evolutionary origin of land plants, for he wrote little about it in Chapter X, ‘On the
Imperfection of the Geological Record’ or Chapter XI, ‘On the Geological
Succession of Organic Beings’.
Ultimately, the challenge of explaining the mystery of how the barren rocky
continents acquired their cloaks of green awaited Frederick Bower (1855–1948).
Long-time occupant of the Chair of Botany at the University of Glasgow, Bower
stands out as a giant in the history of botany.20 He studied botany at Trinity
College, Cambridge as an undergraduate but was unimpressed by the teaching,
describing it as ‘moribund in summer and actually dead in winter’. Nevertheless,
he graduated with first-class honours, and as a young man in his twenties he was
fortunate to have witnessed the University of Cambridge awarding Darwin an
honorary degree.21 Who knows what inspiration the young Bower drew from this
experience? What we do know is that he went on to be an inspiring lecturer,
imbuing his students and colleagues with an enthusiasm for botany during its
heyday in the Victorian era. We also know that his own research began just as
Darwin’s findings from the Origin of Species were becoming effective in biology.
His great hypothesis for how land plants arose to conquer the terrestrial realm is set out in The Origin of a Land Flora (1908), its title a homage to Darwin’s great book .
Bower recognized ‘that certain algae represent in their general characters the
original source from which the land flora sprang’. Although he had no idea which
group of algae gave rise to land plants, Bower was right. He was also right with his conjectures about the evolutionary dodge required for successful reproduction
on the land. And yet, as befits our concerns with PB, few historical treatments of modern science mention Bower. John Gribbin’s richly entertaining Science: A
All flesh is gr Ass a 9
History,22 for example, overlooks Bower and Seward and, for that matter, the great botanical explorer Sir Joseph Banks (1743–1820), holder of the prestigious position of President of the Royal Society, London with distinction for over 40 years.
Ever since Bower’s time, if not before, scientists have been minded to persuade
Earth’s floras to tell secret tales of their remote past. Insights and discoveries from the frontiers of modern science over the past few decades have melded with the
great leaps and incremental steps taken by earlier generations of scientists. Rich new sources of knowledge and understanding of a vanished ecology are offering
answers to explain how a world without plants turned green. Our narrative of the
evolution of plant life on land stretches back over the past 500 million years. It is framed by the family tree that portrays the evolutionary relationships of the plant kingdom (Chapter Two). All land plants, we discover, arose from an ancestral
freshwater algal lineage that colonized the land only once—an evolutionary sin-
gularity that changed the world, forever. Over the next 500 million years, there
followed an unstoppable succession of green evolution, as ferns, forests, and
grasslands appeared and diversified. The success of sun-shot ferns and forests
testifies to the ‘pull of the land’ as they exploited the ecological opportunities created by making a living out of thin air. The greening of the land was an inevitable outcome of the plant kingdom’s sharply escalating power as it began annexing
more and more land.
Questions relating to ‘how’ the evolutionary action portrayed by the evolution-
ary tree might have taken place are addressed in two chapters reading the genetic code of plant life (Chapters Three and Four). Chapter Three shows how recovering
molecular memories stored in the genomes of living plants offers a new and highly original perspective on their evolutionary insistence and global success. Written into the genomes of photosynthesizers—from ubiquitous algae to towering
conifers —are clues to a shifting genetic make-up at critical moments in their evolutionary history. Often these coincide with critical moments in Earth’s history, and for good reason, because the stories of plants and the Earth’s are entwined.
Decoding the genomes of our modern floras is telling us new stories from the past about how the kingdom of plants diversified and survived the mass extinctions
that befell the animal kingdom. Indeed, the extraordinary suggestion that
genomes of many living plants duplicated millions of years ago points to a genetic impetus for the explosion of biodiversity that followed the origins of seed plants and flowering plants .
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Duplicating entire genomes is one thing. Wiring up and creatively recycling old
bits of duplicated DNA, some of it inherited from freshwater green algae, into
genetic toolkits for building land plants is quite another. The novelist J.G. Ballard anticipated the discoveries described here in Chapter Four. In a strange short
story called ‘Prisoner from the Coral Deep’23 Ballard writes of a school teacher
walking a deserted stretch of the Dorset coast. On finding a coiled, fossilized shell, the teacher asks ‘if only one could unwind this spiral, it would probably play back to us a picture of all the landscapes it’s ever seen—the great oceans of the
Carboniferous and the warm shallow seas of the Triassic’. Now, half a century
later, Ballard’s surrealist thought experiment is becoming a scientific reality. As Chapter Four reveals, we are now unwinding the coiled DNA strand inside
the nucleus of living cells to shed light on evolutionary events long ago. These
fascinating glimpses into the past come from evolutionary developmental
biology (‘evo-devo’), a branch of science uniting genetic processes within the
nucleus with the development of cells, tissues, and whole plants. Plants, we dis-
cover, evolved by modifying core genetic toolkits with many components
inherited from algae. Innovations such as roots and leaves, and essential chemical messenger systems informing the plant when and where to grow, and in what
direction, were made possible through expansion and repeated rewiring of dif-
ferent toolkits.
Although roots and leaves are often regarded as standout evolutionary accom-
plishments, ultimately they had to be combined with microscopic gas valves—
stomata—to build successful land plants. Stomata proved to be a secret of the
plant kingdom’s success on land (Chapter Five). The
se tiny mouths appear in the
fossil record millions of years before roots or leaves. Exquisitely tuned to the
environment, stomata adorned the delicate shoots of early land plants as they
poked their heads above primeval soils into the drying sunshine. They allowed
plants to control the loss of water evaporating from cells and tissues as carbon
dioxide moved in the opposite direction, fuelling photosynthesis. Their appear-
ance marked the beginning of a radical new mode of plant life based on exploiting water and nutrients obtained from the soil and enabled it to expand into places it had never gone before. Once plants evolved the ‘trick’ of making stomata, Earth’s floras breathed deeply, grew taller and spread outwards across the continents.
Plants evolved no better solution for swapping carbon dioxide for water and, over 400 million years later, modern plants still rely on stomata packed onto their
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leaves to breathe, made with the same genetic machinery that originated in their
distant ancestors.
Yet the triumph of the plant kingdom in dominating the continents involved
more than the development of innovative cells and tissues courtesy of a flexible
repertoire of genetic toolkits. The move to land required an often-overlooked
innovation: an enduring partnership between plants and symbiotic fungi. Coined
in 1877 by the German biologist A.B. Frank (1839–1900), the term symbiosis means
‘two species that live together’. Frank also came up with the term mycorrhiza for the association, from the Greek for fungus ( mykos) and root ( riza).24 Sadly, he did not live long enough to see his concept of mycorrhizal symbiosis gain a revolutionary new perspective with the discovery of 410-million-year-old fossilized fungal threads penetrating rootlets of early land plants.25 What these and other fossils don’t tell us—what they cannot tell us—is how ancient alliances between plants
and fungi may have operated to facilitate the emergence of terrestrial plant life (Chapter Six). Answering these questions takes us on a botanical expedition to
New Zealand’s South Island, where an ancient lineage of liverworts dwells in the
moss-draped old-growth southern beech forests. Liverworts are simple plants,
surviving relics from a forgotten world, and close living relatives of the earliest land plant pioneers. Fossils, DNA, and experiments with these odd-looking photosynthesizers are building a compelling new picture of how soil fungi helped
plants gain the land. Plants and fungi are locked in a tight symbiotic alliance, dating to the origin of the terrestrial biosphere, that underpins the health of forests, grasslands, and croplands worldwide.
But we should not imagine for a moment that the great greening of the land
occurred in isolation from the rest of the planet—far from it. The dramatic foresting of the landscape had consequences; the complex interdependence of energy
and matter demands it. It had consequences for the rocks into which trees sank
their roots, for the chemistry of the atmosphere, for the chemistry of the oceans, and for all life. It took decades to unpick what happened but diverse lines of evidence are building a new world view recognizing trees and symbiotic fungi as the
bioengineers of global change over millions of years. By destroying rocks and
minerals, the roots and networks of their ‘rock-eating’ fungal partners crumble
Earth’s rocky crust by breaking it down into soil, capturing the greenhouse gas
carbon dioxide in the process and storing it for millennia in the oceans. Chapter Seven explains how the transformation of the naked planet to a forested Eden
12 a All flesh is gr Ass
began sculpting climate and creating rich, nutritive soils to make Earth habitable.
As we shall discover, the secret lives of plants hold great relevance today, guiding us towards strategies for mitigating climate change by capturing and storing carbon dioxide emitted by our burning of fossil fuels for energy.
There is but one way to end this look at the profound transformation of the
planet by the greening of the land: by considering Eden’s future in the face of
escalating threats from humanity (Chapter Eight). What does the future hold for
the great diversity of plants that make up the spectacular floras of the world?
Humanity’s future hinges on how we treat the extraordinary green legacy of those
early land dwellers that adapted to life out of water half a billion years ago. Earth’s biodiversity is declining rapidly as we unsustainably exploit natural resources and destroy natural ecosystems to meet the rising food and energy demands of 7 billion people. Despite the considerable efforts of Peter H. Raven, the former director of the Missouri Botanical Garden, described by Time magazine as a ‘Hero for the Planet’, all the metrics agree. Our ‘ecological footprint’ has never been larger, and the threat to nature is escalating as the human population rises. Safeguarding the future of the planet, as I’ll argue in Chapter Eight, requires mitigation and adaptation as the only sensible responses26 if we are to avoid the sixth great wave of
extinction in the history of life on Earth.
The arch-Darwinian evolutionary biologist Richard Dawkins rightly claims
that evolution is ‘ The Greatest Show on Earth’.27 With characteristic flair, he writes
‘short of rocketing into space, it is hard to imagine a bolder or more life-changing step than leaving water for dry land’. Dawkins is actually writing about the evolutionary appearance of the first land animals, but never mind; he makes a good
point. It is indeed harder to imagine a bolder and more life-changing step than
moving from water to dry land. To be struck by the full force of what evolution
can achieve, there is no better group of organisms to look at than life-sustaining green plants. Not only did plants take the giant step on to dry land 100 million
years before four-legged vertebrates, but their diversity outnumbers that of vertebrates by 10 to 1. Understanding how plants made the transition from life in freshwater to dominate successfully the terrestrial environment has planetary significance now
and in the future. Understanding how a world without plants turned green is one
of the big unanswered questions in science, second only to the origin of life itself.
In Fortey’s words again, it ‘was an extraordinary transformation in the beauty of the world, not merely an opportunity for a great expansion in the compass of life’.
All flesh is gr Ass a 13
We are about to embark on an exciting but challenging journey that offers the
ultimate reward—a solution to one of the great mysteries in the history of life on Earth. Chronicled in the exquisite fossil record reaching back hundreds of millions of years of plant life is the story of what happened. Chronicled in the genes and ecology of organisms alive today is the story of how it happened; how the
world turned green.
2
FIFTY SHADES OF GREEN
‘Even a botanist must occasionally take off his rubber boots and log onto a data-
base. Kinships between plants are no longer determined by fiddling with petals
or reproductive organs but by comparing genetic sequences among species.’
Lone Frank, My Beautiful Genome, 2011
A road trip out of Los Angeles is admittedly not an obvious starting point for
a journey pursuing the remote ancestors of our modern land floras. The
natural landscape has long since vanished in the city, buried beneath a metropolis sprinkled with palm trees imported to add a refreshing splash of greenery for
urban citizens. Continue travelling north-east out of LA, though, and eventually
you encounter the stunning natural terrain of western North America with
moun
tain ranges and expansive deserts looming on the horizon. Before long, the
Mojave Desert (named after the Mohave tribe of Native Americans) makes its hot,
arid presence known as the heat haze shimmers above the parched land. Step outside the comfortable air-conditioned car and a furnace-like dry wall of heat immediately hits you. Under these conditions, it is easy to become distracted and over-
look the communities of photosynthetic organisms living beneath your feet.
These flattened crusts of life persist, scattered between the Joshua trees ( Yucca brevifolia) standing out against the cloudless desert sky, clinging to dusty desert rocks and thin soils. Drab and dull though they might seem, these crusts are actually hotbeds of biodiversity bristling with life,1 despite enduring some of the most extreme and inhospitable environments on Earth.2
Cryptobiotic crusts, as they are known, occur throughout the arid regions of
the world, and contain cyanobacteria, similar to the earliest terrestrial fossilized forms found in 1.2-billion-year-old rocks, living together with algae and fungi.3
They offer a fascinating glimpse of life on land long before the arrival of terrestrial
FiFty shades oF green a 15
plants. Before plants claimed the land, the naked continents were rocky, wind-
swept, and desolate. However, it would be wrong to think of them as totally
devoid of life. Photosynthetic communities of cyanobacteria and algae had
already arrived, quietly making a living for themselves, for perhaps a billion years or more. Dotting the landscape with the merest hints of green, they foreshadowed
what was to come. Through the subtle processes that chemically accelerate the
slow destruction of exposed bedrock, these crusts inadvertently prepared the
ground for the later spread of plant life. By binding together shattered rock grains with fragmentary particles of organic matter, they created patches of land with
the thinnest veneer of consolidated soil, preparing the way for a greener world.
Molecular sequencing of DNA is revealing the hidden diversity of free-living
Making Eden Page 3