Making Eden
Page 22
chemically break down the tough plant cell walls, and fungal pathogens use
similar enzymes to digest or rot living tissues. This makes it difficult, if not
impossible, for both fungal groups (saprotrophs and pathogens) to enter into a
symbiotic relationship with plants, because the enzymes would damage the host
146 a Ancestr Al AlliAnces
and elicit plant defence responses. By shedding whole families of genes encoding
for the enzymes that saprotrophic and pathogenic fungi use to degrade cell
walls aggressively, ectomycorrhizal fungi enjoy a beneficial symbiosis with trees.
Nevertheless, they still possess a small collection of genes encoding selected enzymes for mobilizing carbon and nitrogen from well-decomposed organic matter to help
prospecting fungal filaments survive in soil litter when not in engaged in a symbiosis with roots.
Most recently (geologically speaking), around fifty million years ago, in an
extraordinary twist to the symbiosis story, legumes such as peas and beans co-
opted the symbiotic genetic machinery for establishing partnerships between
plants and fungi to develop a new sort of symbiosis with bacteria. These plants
teamed up with specialized bacteria able to perform the remarkable metabolic
trick of converting atmospheric nitrogen into a form plants can use. Specialized
structures called root nodules host the symbiosis. These are the familiar white,
often pinkish, swellings found around the roots of beans, peas, and other mem-
bers of the legume family (Fabaceae or Leguminosae). The genetic toolkit for
establishing the nitrogen-fixing bacterial symbiosis inside the nodules derives from the pre-existing machinery used for establishing the symbiosis with arbuscular
mycorrhizal fungi. Sequencing of the genome of the legume Medicago truncatula revealed a whole genome duplication event, which occurred approximately 58
million years ago,59 that duplicated the mycorrhizal symbiosis toolkit genes. This seems to have created the gene copies necessary for nodulation and the nitrogen-fixation symbiosis to evolve. Once again, genome duplication provided spare
genetic material to enable evolutionary development, in this case a major new
plant–microbe partnership—the bacterial symbiosis.
Putting all this together, and adding a little more detail to fill in the gaps, allows us to sketch out a scenario for the evolution of plant–microbe symbiotic alliances as the continents turned green. Curiously, though, the fossil record offers rather little on the possible involvement of root–fungal associations as primitive forest ecosystems evolved and expanded on land during the Devonian. But by
Carboniferous times the mycorrhizal symbiosis had diversified, with the fungi
colonizing the fine rootlets of the rhizomes of the giant arborescent lycopsids that dominated the extensive low-latitude swamplands. They also colonized the roots
of lycophytes, and the early relatives of conifers, that formed large forests elsewhere on the continents at this time, alongside the seed ferns. On they marched, as
Ancestr Al AlliAnces a 147
their opportunistic spread into the plant kingdom continued by later colonizing
the roots of some gymnosperms (e.g., cycads, conifers) that dominated the land
flora between the Triassic and Cretaceous. Sometime later, in the Jurassic and
Cretaceous, the first ectomycorrhizal associations appeared. Finally, around the
Eocene Epoch, along came the nitrogen-fixing symbiosis between plants with
bacteria (Figure 22).
This emerging story of the evolving symbiotic lives of plants and microbes,
based mostly on fossil evidence, is also supported by evidence from molecular
biology. Discoveries in the field of molecular genetics have revealed that widely divergent host plant species use strikingly similar genetic toolkits to establish symbioses with fungi or bacteria. The implication is that plants share an evolutionary origin for this ancient symbiotic pathway that was inherited from a single common mycorrhizal ancestor that lived hundreds of millions of years ago.60 In
fact, not only do land plants share common genetic symbiotic machinery but
some of those components were inherited from an algal ancestor.61 This pushes
the origin of the symbiosis toolkit back to the most recent common ancestor of
extant land plants and green algae. That lineage of algae, for some reason, seemed to be pre-adapted for interacting with beneficial fungi, and later facilitated the colonization of the continents by plant life.
If this all sounds like tales woven from the ivory towers of academia with little relevance to modern society, we need a reality check. Finding alternatives to the production of nitrogen fertilizers is essential for sustainable food production. The roots of cereals establish arbuscular mycorrhizal partnerships and discoveries of how the nitrogen-fixing symbiosis operates in legumes raise the possibility of
engineering it into crops. Can we co-opt the pathway between mycorrhizal fungi
and the roots of cereal crops to allow the roots to host nitrogen-fixing bacteria?
This would solve the problem of pollution caused by overuse of artificial nitrogen fertilizers, and address shortages and high costs of fertilizers in developing countries, particularly sub-Saharan Africa.62 The first step to enabling crops to make their own fertilizer is to get cereals to exchange molecular crosstalk with nitrogen-fixing bacteria by releasing substances like flavonoids. Step two is far harder:
convince cereals to host the bacteria in their roots. Clues to the way forward may come from understanding how mycorrhizal fungi evolved root colonization
strategies to trick their way past plant defences by circumventing plant immune
responses.63
148 a Ancestr Al AlliAnces
Earliest
Lycopods
Early relatives
Conifers
Pines
Flowering plants
land plants
of conifers
Aglaophyton
Cordaites
Pinus
Casuarina
Lepidodendron
Telemachus
Quercus
Host plants
Horneophyton
Legumes
Symbioses
Arbuscular mycorrhiza-like
Arbuscular
Ectomycorrhiza
Arbuscular
Rhizobial Frankia
and/or Mucoromycotina
mycorrhiza
mycorrhiza
N-fixing
N-fixing
associations
Rise of the land flora
First forests
Rhynie Chert flora Coal swamp
Gymnosperm-dominated flora
Angiosperm-dominated flora
forests
Extant
Devonian
Carboniferous
Permian
Triassic
Jurassic
Cretaceous
Cenozoic
400
360
300
250
200
145
100
85
0
Millions of years ago
Figure 22 A speculative scenario for the evolution of beneficial alliances between plants and microbes over the past 400 million years.
Meanwhile, forests create a huge carbon ‘sink’ as they remove carbon dioxide
from the air to build leaves, wood, and roots, and to feed mycorrhizal fungi.
Although the sink varies from year to year, on average it absorbs one-quarter
of our carbon dioxide emissions from burning fossil fuels, with the forests
helped by mycorrhizal associations. They allow forests to overcome soil nut
rient
Ancestr Al AlliAnces a 149
limitations to promote carbon dioxide fertilization of plant growth and store carbon in biomass. Forecasting the future behaviour of this natural forest sink for
carbon dioxide will depend in part on incorporating the effects of these mutualistic microbes into our models of the global carbon cycle.64
We have seen how, over the great sweep of Earth’s history, from the Ordovician
~470 million years ago onwards, soil-borne microbial symbionts played a crucial
role in the evolutionary success of the plant world. These alliances facilitated the establishment of plant life on land, with major ramifications for understanding
the past, present, and future ecology of complex land-based ecosystems. Had
Kidston and Lang been alive today, they would surely have been delighted to
know how their lifetime’s work is inspiring new directions and new generations
of scientists. Lang, in particular, felt a ‘plant is a very mysterious and wonderful thing and our business as botanists is to try and understand it as a whole’.65 This admirable perspective resonates with our central theme of symbiotic associations
as evolutionary enablers promoting the amazing diversity of plant life on Earth.
Margulis puts the point more poetically. In her mind, this symbiosis ‘was the
moon that pulled the tide of life from its oceanic depths to dry land and up into the air’. In Chapter Seven we discover how, as plant–fungal alliances evolved,
turning the continents green, plants also began slowly, imperceptibly, to sculpt
the climate. The era of land plants as ‘bioengineers’ of planetary climate had begun.
7
SCULPTING CLIMATE
‘The most recent dream of the New York State Museum was realized when on
February 12, 1925, there was formally opened to the public the restoration of the extensive forests that flourished in eastern New York a few hundred million
years ago.’
Winifred Goldring, The Oldest Known Petrified Forest, 1927
In the 1850s, Minister Samuel Lockwood (1819–1894) discovered a remarkable
sandstone cast of a fossil tree stump near the former settlement town of Gilboa
(from the Hebrew for boiling springs) in New York State.1 Lockwood had already
found dinosaur fossils in the area but his fossil stump was special. It proved to be the first documented discovery of an ancient fossil tree in North America—a
palaeobotanical taster of things to come, because in 1869 workers quarrying rock
for repairing flood-damaged roads and bridges discovered fossil tree stumps
rooted in the position in which the trees originally grew. A few decades later,
another set of tree stump casts turned up in Riverside Quarry, Gilboa. Resembling Apollo spacecraft capsules, each sedimentary cast measured the span of your
hand at the neck, flaring to two or three times that at the base.
The casts are really voids, created by the decaying tree stump, that became
back-filled with sediment. Gathered together by palaeontologists, they formed
the start of the Gilboa fossil plant collections. Winifred Goldring (1888–1971)
(Figure 23), the first woman to hold the position of State Palaeontologist at the New York State Museum, later constructed the innovative Gilboa forest exhibit
documenting ‘the world’s oldest forests’.2 Neatly arranged outside the little
weatherboarded museum on the outskirts of Gilboa sit the same casts on their
bed of gravel, and inside you can find the story of their discovery (Plate 7).
Sculpting climate a 151
Figure 23 Winifred Goldring (1888–1971) in the field at Rensselaer Falls, New York, in 1939, the year she was named State Paleontologist of New York, a position she held until 1954.
Goldring published formal scientific descriptions and illustrations in 1927, and
concerted efforts nearly a century later by the palaeobotanists Chris Berry, Bill Stein, and their colleagues have transformed the scientific picture of these
ancient forests that once flourished near the shoreline of an inland sea. They
unearthed spectacular slender fossilized trunks and crowns of specimens
belonging to extinct trees with the catchy name of cladoxylopsids, known previ-
ously only from those sedimentary stumps.3 The reconstruction of trees from
such finds is a difficult task, but Stein and Berry are masters in the art of piecing together the fragmentary remains. They managed to assemble the entire structure of these unusual 8-metre tall trees by reuniting the crowns and trunks with
the bases. The cladoxylopsid trees left behind root mounds forming circular
craters with a diameter about the size of a football.4 Each depression is really a counterpart mould of the tree preserved as a sediment cast. Anchored into the
152 a Sculpting clim ate
soil by shallow rootlets that sprouted from the bulbous base of their trunks,
the trees had a similar arrangement of strap-like rootlets to that found around the base of tree ferns that are often planted in the glasshouses of botanic gardens.
Tree ferns share a similar basic body plan with those early trees, producing a
whorl of feathery branches unfolding from a central growing region located on
top of a stout trunk. The first Devonian giants of the plant kingdom achieved
their great stature with a similar economy of form, but, unlike tree ferns, these strange trees grew without leaves. Instead, they photosynthesized with a crown
of short-lived branches arranged geometrically above a single long-lived trunk
reaching a height of several metres.
The fossil trees of the early forests found in rocks near Gilboa date back ~385
million years to the Devonian. This was the remarkable time of explosive evolu-
tionary action when plants evolved from small primitive forms that barely
reached your ankle into large, complex trees. A spectacular variety of tree-sized photosynthesizers soon appeared and became progressively larger and complex
within ~20 million years. Scrambling forms sprouting from rhizomes appeared
alongside the cladoxylopsids, followed by progymnosperms, the forerunners of
conifers, made of woody trunks topped with leafy canopies and secured into soils
with woody rooting systems. These evolutionary events in the arboreal realm
changed the world forever, altering the course of Earth’s climate history by
entraining a web of planetary feedback processes that reshaped the chemistry of
the oceans and atmosphere.
Over twenty years ago, the pioneering Yale geochemist Robert Berner (1935–
2015) began unpicking linkages in the complex chain of cause and effect that con-
nects trees and Devonian global climate change. His interest in trees began ‘in
the early 90s while sitting on the banks of the Potomac River, upriver from
Washington, D.C., [when he] noticed plants apparently growing out of rocks.
I had seen this before and at that time I became interested in how plants affect
rock weathering’, before remarking ‘besides being an interesting phenomenon in
its own right, the study of plants and how they affect the rate of weathering is
important in the long-term carbon cycle’.5 By ‘how plants affect rock weathering’, he means how plants help chemically and physically break down rocks that then
react with carbon dioxide. The process has important consequences for climate
because over millions of years it slowly removes carbon dioxide from the atmos-
phere, weakening the greenhouse effect and cooling the planet. We shall unpack
Sculpting climate a 153
the det
ails shortly. By long-term carbon cycle, Berner is referring to the slow
transfer of carbon between rocks, the oceans, and the atmosphere. Acknowledging
his debt to earlier scholars from the 1950s, his subsequent series of scientific
papers took geochemists, botanists, and anyone else prepared to listen by the
hand and opened their eyes, explaining how Earth’s transition from a naked to a
forested planet revolutionized its climate history.6
Struck by his remarkable view of the place of trees in our planet’s climate his-
tory, in the spring of 1997 we invited Berner to speak at a scientific meeting organized at the Royal Society, London.7 Breaking all the usual rules of engagement we teach to graduate students, Berner stood with his back to the audience, facing the screen displaying his presentation, and gave a straight-talking narrative describing his scientific journey towards this new world view. Central to the talk were his discoveries about how trees accelerate the chemical weathering of basalt rocks in
the Skorradalur Valley, south-western Iceland.8 By analysing the chemistry of
stream water draining from small catchments populated with stunted birch/pine
trees, or barren rocks colonized by patches of lichens and mosses,9 he revealed the distinctive geochemical fingerprint of trees chemically dissolving basaltic rocks.
Berner’s thinking was that the tree-populated catchment represented an approxi-
mate analogue for early forested Earth, and the barren catchment a kind of ‘con-
trol’ for naked Earth; it had lost its trees sometime in the last century from
overgrazing by sheep.10 If these findings can be taken as any sort of guide to
chemical weathering regimes before and after the evolution of trees (pre- and
post-Devonian worlds, in other words), they suggest that the arrival of trees on
the evolutionary stage accelerated rock weathering by a factor of five. Subsequent interest in Berner’s results prompted similar studies by other scientific teams and, in the years that followed, they found that no matter which part of the world you are in, the activities of plants accelerate the chemical destruction of Earth’s rocky landscape.11 Berner had discovered a profound truth about how the world works:
the activities of forests and trees regulate a fundamentally important process—