Making Eden

by David Beerling

  view of the world is like this. Next time you take a walk through the countryside on summer’s day, it may be worth reflecting on the long and eventful history

  of stomata in the leafy canopies above your head, or the grass blades brushing

  against your knees. They are sensing the environment in the soil, the atmosphere, and in their surrounding cells and processing the information to make decisions

  about opening and closing. Collectively, millions of them are cooperating to

  maximize the beneficial uptake of carbon dioxide to grow the plant and minimize

  the loss of precious water supplies. Making these decisions are genes derived from an ancient core genetic toolkit that proved of fundamental importance to the

  earliest land plants nearly half a billion years ago.

  Today, tiny, exquisitely sophisticated stomata densely stud the leaves of virtu-

  ally every species of plant on the planet. Only a handful of specialized amphibi-

  ous species can live without stomata. Instead of capturing carbon dioxide from

  the air, these plants draw it up through their roots in dissolved forms from the

  sediments.65 The collective planetary gulp of carbon dioxide by the global population of stomata on the leaves of land floras is an impressive ~430 billion tonnes each year.66 About half of this is converted into new plant growth; the other half is released back into the atmosphere by respiration by plants and microbes. The

  enormous uptake and release of carbon dioxide by land plants creates a seasonal

  cycle in its atmospheric concentration, detectable by air measurements made

  across the world, which really reflect the ‘breathing’ of land floras. By permitting

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  land floras to safely refuel with carbon dioxide and grow, stomata help sustain

  a huge diversity of animals, from elephants to earwigs. They play an essential

  role in feeding the voracious appetite of herbivores across the globe. Unless you live exclusively on a diet of algae-grazing fish and squid, the same holds for

  humans too—most of us are composed of carbon atoms that have passed through

  stomata pores.

  John Updike, in The Centaur (1962), takes up this theme, writing that green plants

  ‘take in moisture and the carbon dioxide we breathe out and the energy of the

  sunlight, and they produce sugar and oxygen, and then we eat the plants and get

  the sugar back and that’s the way the world goes around’. To which we can now

  add that the carbon atoms in those carbon dioxide molecules have travelled

  through microscopic stomatal pores before the biochemical machinery processes

  it via by photosynthesis and makes it into sugar. Updike later writes poetically

  that ‘ultimately the energy for photosynthesis comes from the atomic energy of

  the sun. Every time we think, move or breathe, we’re using up a bit of golden sunshine’. Human society obtains energy by releasing the energy of golden sunshine

  trapped in fossil fuels, like coal. Coal is composed of concentrated carbon atoms that travelled through prehistoric stomata and were converted into biomass

  by prehistoric photosynthesis; for as everyone knows, coal is the fragmentary

  remains of ancient tropical swamp rainforests.

  Unlike the rainforests of the primeval swamplands, flowering plants dominate

  modern tropical rainforests and, luxuriating in year-round warmth, they are the

  most productive forests on Earth. But the remarkable productivity of these rain-

  forests is not simply a function of the warm climate. It is made possible because the evolution of stomata in flowering plants progressed hand-in-hand with evolution of the plumbing systems (veins) that distribute water to photosynthesizing

  leaf cells. Anatomically, the valves and tubes that make leaves work are arranged so that the veins supplying water to the leaf deliver it close to the sites of

  evaporation in photosynthesizing tissues, near to where stomata are located. The

  arrangement helps prevent leaves from dehydrating when stomatal pores open to

  allow the inward diffusion of carbon dioxide. As a rule of thumb, we can say that having plumbing systems better able to supply water to leaves is a good way of

  supporting productive plants. It is the core principle Joe Berry was alluding to

  with his Wall Street trader analogy, with leaves better able to trade more soil-

  water for atmospheric carbon dioxide. But the hidden cost to building leaves with

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  better hydraulic properties is that water-conducting tissues are expensive to construct, in terms of carbon.67

  Why has evolution driven the selection of leaves with a high capacity for

  transpiration given a high carbon penalty for their construction? The answer

  seems to be that it is partly the evolutionary legacy of dwindling atmospheric carbon dioxide levels since the age of the dinosaurs, early in the Cretaceous.68 Slowly falling carbon dioxide levels may have forced flowering plants to evolve leaves

  with larger numbers of miniaturized stomata to maximize their uptake of carbon

  dioxide for growth.69 This, in turn, drove the miniaturization of leaf-vein systems with the appearance of fine veins forming dense meshes to better supply water to

  leaf cells doing the photosynthesis.70 Only flowering plants evolved the novel

  developmental mechanism enabling this to happen and it gave them a much

  greater vein density per unit area of leaf.71 Fossil leaves document the pattern

  of increased investment in water supply tubes since the Cretaceous that helped

  ensure flowering plants could grow faster.72 According to the fossils, no other

  group of land plants—lycophytes, ferns, or gymnosperms—followed this

  evolutionary trajectory. Without it, leaves are not sufficiently well irrigated to safely open their stomata to absorb carbon dioxide to increase photosynthesis

  productivity. In effect, falling carbon dioxide levels, over millions of years, locked plants into a ‘hydraulic arms race’ between species. Armed with an ability to

  miniaturize stomata and water-supply vein networks, flowering plants had the

  edge and began to eclipse ferns and conifers in the world’s tropical zones.

  The leaves in modern tropical rainforests are a legacy of these past events and

  today these forests are the transpiration engines of the world, air-conditioning the planet by extracting water from deep in the soil profile and pumping it back to the atmosphere. In the Amazon, up to half the rainfall is recycled in this way each year and it makes the region around 5°C cooler than it would otherwise be, and substantially wetter.73 By helping to generate wetter tropical climates and complex

  habitats, tropical forests foster their own existence and a rich diversity of life.

  What might happen as we pursue a programme of deforestation, degrading

  the land surface until it is covered by vegetation like ferns, lacking the high

  transpiration rates of tropical trees? In a world without rainforests showering

  the atmosphere with transpiration, tropical climates, especially those in South

  America, would be hotter, drier, and more seasonal.74 Current and future defor-

  estation of the Amazon will affect the water cycle. Cut down the forests and you

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  halt the delivery of moisture to the air above, inhibit water recycling, and reduce rainfall. Some projections of forest loss by 2050 indicate it will cut rainfall by 20%

  in the dry season across the Amazon basin75 and exterminate species. At its sim-

  plest, the message here is this: no rainforests → no rain → extinction.

  The evolutionary dance between valves, tubes, and the carbon dioxide co
ntent

  of the atmosphere continues, with global consequences for Earth’s future climate.

  For stomata will have a say in how the planet’s climate system responds to the

  increasing atmospheric carbon dioxide concentration resulting from our ongoing

  combustion of fossil fuels. Decisive and meticulous experiments undertaken by

  the English plant physiologist Oscar Victor Sayer Heath (1903–1997), soon after

  the Second World War,76 established that an atmosphere enriched in carbon diox-

  ide causes stomata to close partially.77 Heath’s seminal experiments, undertaken

  on the stomatal behaviour of wheat, are fast becoming a new reality as we realize they hold for the majority of land-plant species. Already, the stomata of northern hemisphere forests are closing in the manner Heath anticipated, as atmospheric

  carbon dioxide levels climb and re-tune the physiology of trees to affect the wider planetary environment.78 The wider environment here is the global climate system and the significance of Heath’s discoveries for climate change are explained

  by the distinguished stomatal physiologist Terry Mansfield, as follows: ‘This alters the rate of transfer of water from the soil to the atmosphere, and it also affects the surface–atmosphere exchange of heat and contributes to global warming. Thus

  the ability of stomata to sense and respond to CO [carbon dioxide] in the atmos-

  2

  phere, once thought to be an obscure topic only of academic interest to Heath and a few other scientists, has become a major factor in our understanding of the

  forces that are driving climate change.’79

  As Mansfield explains, when stomata close, the transpiration stream that seeds

  rainfall and air-conditions the planet begins to shut down. Changes in atmos-

  pheric water vapour, clouds, and the exchange of energy between the land surface

  and the atmosphere follow. It is obviously challenging to assess the extent of carbon dioxide-related stomatal feedbacks on future climate change. Simulations of

  land carbon and water cycling by forests, and linkages within the global climate

  system, are uncertain on the detail.80 Nevertheless, in general they confirm that when the effects of elevated carbon dioxide on stomata are included, they modify

  both the climate and the hydrological cycle.81 Simulations of a carbon dioxide-

  rich atmosphere show that its simple effect of causing stomatal pores to open less

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  widely contributes some 30% additional warming across large areas of the boreal

  forests and the tropical rainforests (Figure 16). This additional warming is over and above that caused by the enhanced greenhouse effect resulting from the carbon dioxide-rich atmosphere (i.e., by trapping long-wave radiation).

  Half a century on from Heath’s important discovery concerning how carbon

  dioxide affects stomatal behaviour, we are discovering key genes involved in pathways mediating the perception of carbon dioxide and how it controls their devel-

  opment. Surprisingly, the important genes involved in perception of carbon

  dioxide in plants are remarkably similar to those possessed by humans and

  insects, even though the evolutionary pathways of humans and plants diverged

  over a billion years ago.82 Why mammals evolved a mechanism to sense carbon

  dioxide is unclear. Was it to alert them to rotting food, which releases carbon

  dioxide? Insects, like fruit flies, moths, and mosquitoes, sense carbon dioxide to find food items like decaying fruits, flowers, and people. The genes responsible

  function interchangeably between these groups of organisms and code for an

  enzyme called carbonic anhydrase. Carbonic anhydrase combines carbon dioxide

  and water and converts them into a simple acid (carbonic acid) plus bicarbonate

  0

  0.05

  0.1

  0.15

  0.2

  0.25

  0.3

  Figure 16 Fraction of total surface warming caused by the physiological effects of carbon dioxide on stomatal behaviour.

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  ions. The acidic signal interacts with the sour-cell taste-bud receptors on our

  tongues. In leaves, the bicarbonate signal activates molecular pumps in the walls of the guard cells that trigger the pore to close. If you transfer the gene for mammalian carbonic anhydrase into Arabidopsis plants lacking their own version, it restores the responsiveness of stomata to carbon dioxide.83

  Plants are also adapting to rising atmospheric carbon dioxide levels in another

  important way: by reducing the number of stomata developing on their leaves.

  Evidence from historical collections of leaves of trees from southern England

  suggests trees noticed the rise in atmospheric carbon dioxide levels and took

  action on it in this way,84 before we had started measuring the concentrations for ourselves.85 Steps towards solving the mystery of how plants reduce the numbers

  of stomata came thirty years after that evidence came to light, with the discovery that leaves sensing rising atmospheric carbon dioxide levels activate their ‘Twitter feed’ to produce more of a particular peptide, called EPF2.86 This blocks the

  formation of stomata in the epidermis of leaves at elevated carbon dioxide con-

  centrations. Other proteins known as proteases activate the EPF2 peptide. One in

  particular (coded for a gene called CRSP, Carbon dioxide Response Secreted Protease) is crucial for activating EPF2 and is responsive to atmospheric carbon

  dioxide levels. This part of the newly discovered pathway acts as a carbon dioxide-regulated volume control on gene expression, offering a sensitive means of bal-

  ancing stomatal development as the atmospheric carbon dioxide concentration

  changes. You can imagine that such a ‘sensing and response’ mechanism involv-

  ing two genes ( CRSP and EPF2) may offer scope to engineer crop varieties for improved performance with a changing global climate.

  An early warning sign that rising atmospheric carbon dioxide levels might be

  closing stomata, or causing leaves to be made with fewer of them, is the recent

  increased delivery of freshwater from the land to the oceans. Roots take up less

  water from the soil if forest canopies are constructed of less porous leaves, all else being equal, and this means more water drains from soils into rivers and ultimately into coastal waters. British scientists have reported that the terrestrial biosphere is already feeling the effects of our carbon dioxide emissions and responding in

  this way.87 According to their analyses, a trend of increasing amounts of freshwater flowing off the continents to the oceans began around the beginning of the

  twentieth century, when carbon dioxide levels started to climb more steeply.

  Climate and land use over the same period are ruled out as possible causes, meaning

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  that it is the direct effect of rising carbon dioxide levels, linked to the stomatal suppression of evaporation from global forests.

  Q

  Back in 1976, the UK suffered a severe heatwave and widespread drought killing

  trees and causing crop failure. That same year the distinguished meteorologist

  John Monteith (1929–2012)88 closed a prescient meeting at the Royal Society,

  London, on plants and the water cycle by quoting the Victorian poet Alfred, Lord

  Tennyson’s lines written at the time of the potato famine in Ireland:

  Science moves but slowly, slowly, creeping on from point to point

  Slowly comes a hungry people, as a lion creeping nigher,

  Glares at one that nods and winks behind a slowly dying fire.

  Crops and crop production were very much on Monteith’s mind, and with
r />   intellectual poise he suggested Tennyson’s lines had modern relevance. He asked

  ‘whether we are the people nodding and winking behind sophisticated research

  projects while hunger and malnutrition remain an immense global problem’.

  Urgently improving our ability to feed a growing human population that may

  reach 11 billion by 2100 is very much a modern research priority. Stomata are now prime targets for boosting yields of major crops by making them more efficient

  in using water in a warmer, drier future climate. Continued progress in this area depends on better understanding the complex development and physiology of

  stomata, and the roles they play in allowing plants and global ecosystems to

  manage their watery economics.89

  Meanwhile, continuing our progress in understanding how global ecosystems

  ‘greened’ the continents means we need to think more broadly. We need to move

  beyond thinking in terms of accumulating a succession of evolutionary adapta-

  tions to build successful land plants. Plants also succeeded on land by forging alliances with another group of organisms—soil microbes. That story, which set in

  motion a chain of events that was to fundamentally transform global ecology and

  the chemistry of oceans and atmosphere, unfolds in Chapter Six.

  6

  ANCESTRAL ALLIANCES

  ‘Sam Gamgee planted saplings in all the places where specially beautiful or

  beloved trees had been destroyed, and he put a grain of precious dust from

  Galadriel in the soil with the root of each. . . . Spring surpassed his wildest hopes.

  His trees began to sprout and grow, as if time was in a hurry and wished to make

  one year do for twenty.’

  J.R.R. Tolkien, Lord of the Rings ( The Return of the King, 1955)

  Rhynie is a small, unremarkable village in a fertile valley of the Old Red

  Sandstone area in Aberdeenshire, Scotland. Amongst palaeontologists,

  though, Rhynie is internationally renowned for exquisitely preserving the fossil-

  ized anatomy of a terrestrial ecosystem of the early Devonian Period. Beneath the green fields and mantle of soil lies a snapshot, frozen in time, of terrestrial life from 400 million years ago that includes primitive land plants, fungi, algae,