decorated the Romanesque columns framing the doors with diamond-patterned
stonework celebrating the fossil bark of Lepidodendron trees. These long-extinct giants of the Carboniferous coal-swamps photosynthesized with narrow strap-like microphyll leaves.
Palaeobotanists infer the existence of auxin transport, and even its direction of travel, from the graining patterns recorded in specimens of fossil wood from
these ancient trees.69 Although metabolized quickly, auxin leaves behind a lasting record of its action on the growth of trees. The direction of transport along the stem is diagnosed from the arrangement of the water-conducting cells (tracheids)
that form the grain of the wood. When auxin is transported downwards from the
apex of the tree with an undisrupted flow, the tracheids align end-to-end, creating the smooth grain of wood. When the flow of auxin is impeded by a disruption,
such as a branch, it pools above the branch, causing tracheids to develop in swirls.
Such distortions reflect changes in the direction of the flow of the auxin signal.
Cut thin translucent sections of fossilized stems and roots of lycopsid trees from the Palaeozoic and you can observe, through a microscope, cellular disruptions in the dense matrix caused by tangled tracheids. These distortions are reminiscent of those caused by directional auxin transport in the wood of modern seed plants.
Distorted vascular tissues in the trees that dominated the moist Carboniferous
lowlands tell us that auxin regulated tree growth long before flowering plants
appeared on the scene. But then the diamond patterning on the stone pillars of
the museum entrance tells us this too. For auxin makes the diamonds, which are
really scars left by falling leaves on the bark of the giant Lepidodendron trees.
Auxin is not the only plant hormone—plants require collections of them to
manage different aspects of how they grow. Of all the challenges that living on
land brings, surmounting the fundamental problem of water stress must have
been key. This is where the hormone ethylene may have played a crucial role
because it enables the ‘submergence escape response’ of plants. It works because
ethylene diffuses more slowly in water than in air, leading to its entrapment and accumulation in submerged tissues. The accumulation of ethylene then triggers
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the escape response, which is essentially a growth spurt. The submergence of rice plants, for example, causes the ethylene escape response to kick in and trigger
rapid stem growth to escape complete submergence. Not for nothing are two of
the rice genes involved called SNORKEL1 and SNORKEL2. The ethylene link to early land-plant survival is obvious. Having made the transition from an aquatic
to a terrestrial habitat, land plants needed a mechanism for keeping their heads
above water when the rains came. Proof that it appeared early on in the scheme of things came with experiments on bryophytes. If you subject mosses to submergence for a few days, genes in the ethylene-signalling pathway are activated, causing cells to elongate and shoots to extend, as mosses struggle through the surface meniscus to emerge above the water line.70
This escape pathway originates in charophyte algae, which possess collections
of genes for the biosynthesis, transport, and perception of ethylene. Experimental work has now demonstrated that the cellular growth of the charophyte alga
Spirogyra responds to ethylene and that a flowering plant ( Arabidopsis) can use Spirogyra’s genes in its own ethylene-signalling pathway.71 Ethylene, then, was likely a functional hormone in the common ancestor of freshwater algae and land
plants that lived over 450 million years ago, and probably much longer ago than
that. Interestingly, the ethylene receptor gene itself seems to be far more ancient, having been acquired by plants from cyanobacteria over a billion years ago.
Chlorophytes had it and lost it. Charophytes had it and kept it.
Chlorophyte algae are evolutionary duds when it comes to giving rise to land
plants, whereas charophyte algae, we are coming to appreciate, really are special.
Why would the aquatic ancestors of land plants need an ethylene escape path-
way? The answer to that question is unclear—unless we suppose charophytes
were already living on land long before terrestrial plants evolved and got pushed back into freshwater by competition with the increasingly successful land plants
to which they had given rise (the ignominy!).72 If that is the case, the ethylene escape pathway could be regarded as a former trait, which they have not yet lost, from their days on land.
The fascinating story of ethylene shows how unravelling the history of a par-
ticular hormone shines new light on key events that laid the foundation of terrestrial plant life hundreds of millions of years ago. Our understanding of hormones in this context is undoubtedly limited, and largely confined to saying a few things about when particular genes originated and speculating about their function, but
Ancient genes, new pl Ants a 89
the powerful growth hormone gibberellin is an exception. Nick Harberd, also at
Oxford as it happens, has dissected how gibberellin works, how the genetic
machinery arose, and how it benefited early land plants.73 Gibberellin is named
after the fungal pathogen Gibberella fujikuroi (now called Fusarium moniliforme), the effects of which were first recognized in Japan in 1935. Rice seedlings infected with the fungus develop a disease known as ‘foolish seedling’ syndrome,74 caused by
the fungus secreting gibberellin. The symptoms include the rapid and excessive
elongation of rice seedlings with slender leaves, and drastic reductions in rice
yields.75 Why the fungus bothers to inflict these traumas on the rice plant by
secreting gibberellin only became clear when it was demonstrated that the gib-
berellin disables the plant’s immune system, allowing greater infection by the fungus and boosting its virulence as a result.76
Harberd elucidated the mechanism by which gibberellin stimulates the growth
of flowering plants and it is worth unpacking some of the detail to see how these DNA-based instructions had far-reaching consequences for the evolution of
terrestrial plant life.77 His team discovered that gibberellin allows growth by triggering the destruction of certain protein molecules, transcription factors called DELLAs. DELLAs are restraining orders for plants; anti-social behaviour orders
for shoots, preventing riotous growth.78 Gibberellin binds to a receptor molecule to form a chemical complex inside the cell’s nucleus. The details are complicated, but in short this stimulates the tagging of DELLAs with a small but crucially
important protein (‘ubiquitin’). These reusable protein tags are the kiss of death for DELLAs, labelling them for destruction by the waste disposal units of cells,
proteasomes.
The biochemical tagging of proteins through the attachment of special molecules
such as ubiquitin is actually a general mechanism by which cells destroy unwanted proteins. Cells of all living organisms use this method of protein destruction,
which goes by the unwieldy name of ‘ ubiquitin-mediated protein degradation’, and it won the three scientists who made the ground-breaking discovery (Aaron
Ciechanover, Avram Hershko, and Irwin Rose) the 2004 Nobel Prize for Chemistry.
In short, gibberellin causes DELLAs to disappear, and this removes a molecular
restraint on plant development and allows the growth-promoting genes to get
on with the business of actively growing the shoot. The molecular machinery
involved in plants is very ancient, with the full set of genetic instructions for regulating the architectural exuberance of sh
oots assembled in distinct stages over the
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past 400 million years.79 By the time seed plants had evolved, the complete genetic toolkit had appeared, and, because environmental cues modulate DELLA activity,
plants now had a mechanism for coping with changing environmental condi-
tions. When it is too hot or too cold, or the soil dries out during a drought, DELLA activity changes, telling the plant when it is time to slow down. When conditions improve, DELLA activity changes again and the plant ‘knows’ to resume growth.80
It provides a means of guiding plants successfully through the delicate game of
life on land by ensuring their survival during times of environmental crisis. In
Darwinian terms, this speaks directly to the ‘survival of fittest’.
If these intricate molecular details of the goings on inside plant cells seem rather esoteric and far removed from reality, nothing could be farther from the truth.
They have real world importance in explaining the Green Revolution of the 1960s,
led by Norman Borlaug (1914–2009), the ‘Father of the Green Revolution’, who
received the Nobel Peace Prize in 1970 in recognition of his contributions to world peace through increasing food supply. Selective breeding of crop plants for dwarfing traits brought about the spectacular increases in wheat and rice yields that
fuelled the ‘Green Revolution’. Before the Green Revolution, older varieties of wheat and rice plants had tall, weak stems unable to support the heavy package of grains loaded at the top of slim stalks, causing the plants to fall over in the wind. Lodging, as the process is known, reduces yields because the grain in the head of the stems is ruined on the flattened plants. Compact dwarf varieties of wheat and rice over-came the problem, with stout stalks easily supporting the grain-packed heads and
therefore being far more resistant to lodging by wind. After farmers adopted these
‘dwarf’ varieties, wheat yields in Europe, North America, and Asia soared. This
confounded the dire predictions of the Stanford ecologist Paul R. Ehrlich, who
forecast in his bestseller The Population Bomb (1968) that ‘The battle to feed all of humanity is over . . . In the 1970s and 1980s hundreds of millions of people will starve to death in spite of any crash programs embarked upon now’.
The Green Revolution was ushered into the molecular era with the identifica-
tion of the genes responsible for the new dwarf varieties of wheat and rice. As you might have guessed, alterations to the DELLA genetic toolkit were at the heart of it.81 Wheat varieties producing stout ramrod-straight stalks had mutated DELLA
genes, which prevented gibberellin from relieving their growth-repressing effects, causing the crops to become stunted. Rice varieties meanwhile had an impaired ability to synthesize gibberellin itself, meaning DELLA-opposed growth predominated,
Ancient genes, new pl Ants a 91
resulting in shorter plants. So DELLAs, along with irrigation, chemical fertilizers, and agro-chemicals, help feed the world today and have been underwriting the
solar-powered economy of nature since before the dawn of terrestrial plant life.
Deep insights into the origin and diversification of the land plants, woven into
the DNA of our modern terrestrial floras, are starting to tell us about wonderful long-hidden molecular events that facilitated the colonization of the land. We are edging towards a deeper understanding of the continued metamorphosis of plant
life as it evolved from simple freshwater algae to complex trees. The Devonian
‘big bang’, fuelled by the sorts of genetic toolkits regulating development pro-
grammes we have been considering, was really a Palaeozoic revolution, with
plant life continually reinventing itself. Variety in plant form across the Devonian Period was generated through the assembly and rewiring of genetic toolkits from
pre-existing genetic components. Evolution operated by working with what is to
hand to generate novelty. Similar modes of evolution enabled the evolutionary
metamorphoses of animals.82 Expansion and rewriting of genetic toolkits is
ex plaining how insects evolved wings, how beetles grew horns to fight over females, and how moths and butterflies decorated their wings with brightly coloured eyespots to ward off predators.83
The famous Oxford mathematician G.H. Hardy, who held the Savilian
Professorship of Geometry there between 1919 and 1931, gave biologists the
Hardy–Weinberg principle describing gene flows through populations of plants
and animals. He remarked in his classic essay A Mathematician’s Apology (1940) that mathematicians probably have the best chance of achieving immortality, because
of the fundamental nature of the mathematical proofs they produce. Hardy
thought this ‘very comforting for dons, and especially for professors of mathe-
matics’. He was writing at a time before we understood the secret of plants’ suc-
cess in colonizing Devonian landscapes. It is the same as their ability to defy
ageing and is found by looking at plants in botanic gardens. Their modular con-
struction is controlled by ancient networks of genes that permit organs like leaves and roots to be repeatedly renewed as they show signs of physical deterioration
with age and attack from pathogens.84 It also helps them avoid the gradual accu-
mulation of harmful mutations, as scientists showed when they sequenced the
genome of ‘Napoleon’s oak’ ( Quercus robur) on the campus of the University of Lausanne, Switzerland.85 The tree is so-called because it was planted as a young
individual (22 years old) in 1800 to commemorate the visit of the general and his
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troops on their way to conquer Italy. The mutation rate in this 234-year-old tree was 10 times lower than in the short-lived weedy annual Arabidopsis. How can this be for such an ancient tree? The answer is, of course, that the clusters of stem cells on the growing tips on the branches develop their own stems, leaves, and shoots
over and over again. Unlike humans, trees slow down ageing through renewal, or,
as Philip Larkin puts it in ‘The Trees’, ‘Their yearly trick of looking new’.86 The modular growth habit of trees means that harmful mutations may cause leaves or
branches to die off but will not kill off the whole tree.
The concept of plant growth based on repeated modules of shoots and roots
perplexed Charles Darwin. He wrote in his Origin of Species (1859) that:
All organic beings have been formed on two great laws – Unity of Type and the
Conditions of Existence. By unity of type is meant that fundamental agreement
in structure, which we see in organic beings of the same class, and which is quite independent of their habits of life. The conditions of existence are fully embraced by the principle of natural selection [which] acts by either now adapting the varying parts of each being to its organic conditions of life; or by having adapted them in long-past periods of time.
What Darwin really meant by his phrase ‘Unity of Type’ was that the body plan of
all plants is the same, conforming to a modular construction consisting of the
three vegetative organs we have been considering throughout this chapter: roots,
shoots, and leaves. This common body plan is repeated throughout the plant
kingdom, but with infinite variation in the details. What puzzled Darwin about
this view of the world was the thorny issue of the mechanism that simultaneously
allowed plants to retain a common body plan, and yet gave rise to the enormous
complexity of plant life we see today.87 The question has intrigued scientists for more than 150 years. We are now starting to find some answers: flexible green
/> genetic machinery generates diversity in the modules—leaves, flowers, roots, and
so on—while allowing plants to stick with the same successful basic body plan.
Beyond Hardy’s window, in the College grounds, ‘the trees are coming into leaf’
with the arrival of the warm spring sunshine, heralded by the voices of Magdalen
College choir. And, it is Larkin again in ‘The Trees’ who puts it so well, ‘Yet still the unresting castles thresh/In full grown thickness every May’: each leaf unfurls
studded with thousands of tiny mouths; each mouth is a sophisticated micro-
scopic gas valve for swapping gases with the atmosphere. The gas valves of
Ancient genes, new pl Ants a 93
modern trees are remarkably similar to those that first adorned the young naked
shoots of early vascular land plants over 410 million years ago. These structures have not yet got much of a mention, but proved to be one the most important
innovations in the kingdom of plants. They ushered in a new mode of plant life
that fundamentally changed the cycling of elements through the biosphere and
radically transformed the planet. In Chapter Five, we discover how.
5
GAS VALVES
‘Plants are like “beautiful strangers”—they are so different from us. They don’t
have neurons or brains, yet they cleverly sense the surrounding environment,
defend themselves and prosper.’
Keiko Torii, 2013, Current Biology, 23, R943–4
Walking through the groves of giant redwoods ( Sequoiadendron giganteum) in the Yosemite National Park gives you the ground-up perspective of these
magnificent towering trees. Giant redwoods are the largest trees on Earth, with
girths wide enough to drive a Cadillac through, should you choose to, but they
start life as tiny seeds measuring about a millimetre long. Gaze upwards from the darkness of the forest floor and the enormity of the trees as they point towards the sky, saluting the Sun, is immediately obvious. Beneath these leafy cathedrals is a tranquil sanctuary from the modern world created by the ancientness of trees
over millennia. Viewed from the air, a quite different perspective becomes appar-
Making Eden Page 14
