duplications. Genomics shows how rare but important duplications are tied to
innovation and diversification of plants at critical moments in their evolutionary history. The genomes of flowering plants show a wave of duplications dating to
between 75 and 55 million years ago.81 Precise dating of the event is uncertain but they all cluster suspiciously close to the end-Cretaceous mass extinction that saw off the dinosaurs and many other species, 66 million years ago.82 It was a time of catastrophic environmental change caused by the double whammy of a bolide
impact near Chicxulub, Mexico, and periods of massive volcanism, recorded in the
form of the Deccan Traps in India. In the face of such environmental instability, did whole genome duplications help plants survive by con fe r ring them with broader
environmental tolerances? Intriguingly, conifer genomes also record evidence for
an older duplication event, dating back to a broad window of geological time
spanning the even more devastating Permian–Triassic extinction, 251 million
years ago.83 Mutated fossil conifer pollen has been discovered in rocks dating to the end-Permian, when a prolonged bout of intense UV radiation pierced a damaged ozone layer drastically thinned by noxious gases emitted during the massive
Siberian volcanic eruptions of the time.84 Pollen is essentially a male sex cell (gamete) and, hit with high doses of UV radiation, it may not have undergone the nor-
mal reduction of its chromosome complement. Such a mutational bonanza
may have helped conifers survive the catastrophic end-Permian environmental
deterioration caused by the Siberian volcanism.
These speculative scenarios raise the question: why would plants that under-
went whole genome duplications be more likely to survive drastic global environ-
mental upheaval linked to mass extinctions? One explanation revisits our earlier
theme—generating novel gene functions by creating spare copies of genes for
evolution to work with. By increasing variation in gene expression patterns, and
rewiring some genetic networks of their developmental circuitry, plants have
greater potential for tolerating a wider range of environmental conditions than
their progenitors with a narrower gene base. In other words, duplicated genes
increase the organism’s chances of survival under new or harsh environmental
Genomes decoded a 65
conditions. If plants gained an extra genome by merging chromosome sets from
a closely related species, then novel combinations of genes might broaden their
ecological tolerance. We are dealing with the phenomenon of ‘hybrid vigour’.
Hybrid plants tend to be better at out-competing species that did not undergo
genome duplications because they generally have greater stress tolerance, faster
growth, and greater resistance to pests and diseases. No wonder hybrids are
frequently invasive species colonizing new or disturbed habitats.
If extraordinary claims for genome duplication events hold up, and the evi-
dence is mounting, we can tentatively conclude that genomic upheavals in the
past prompted the evolution of new plant life from ancestral forms and helped
generate the enormous diversity of plant life on Earth. Conversely, it follows that had large-scale genome duplication events not occurred, the world would be a
very different place. The kingdom of plants, as we know it, would probably not
exist, and neither would vertebrates. Aided in part by whole genome duplications
at critical moments in the past, plants survived the repeated mass extinctions that befell the animal world over the past half billion years. Quite how plant life managed the impressive evolutionary trick of co-opting and redeploying an expand-
ing genetic repertoire for their own ends to build leaves and roots out of bits of DNA inherited from algae is a story for Chapter Four.
4
ANCIENT GENES, NEW PLANTS
‘The attempted synthesis of paleontology and genetics.... may be particularly
surprising and possibly hazardous.’
George Gaylord Simpson, The Tempo and Mode of Evolution, 1944
Botanic gardens are often steeped in history, places where plants and the past
combine to enrich the magic of a visit. Founded in 1621, the Botanic Garden
of the University of Oxford is the oldest in Britain, a mere 76 years younger than the oldest botanic garden in the world: the Garden of Padua in northern Italy.
Founded in 1545, the Garden of Padua originated from a Benedictine collection of
medicinal herbs. Now a UNESCO world heritage site, it retains the original layout with a circular central plot, symbolizing the Earth, surrounded by a moat.
Similarly, the enchanting Oxford Botanic Garden also preserves its original lay-
out. Pass through a classical baroque-style stone gateway and you find the walled garden that originated in the seventeenth century, arranged around the oldest
tree, a magnificent creaking yew ( Taxus baccata). The tower of Magdalen College looms over the gardens, and each year the college choir celebrates the arrival of spring at 6am on May Day morning, when their voices rise high and clear singing
a Latin hymn.
For many years, an iconic black pine ( Pinus nigra) stood towards the far side of the walled garden. With its thick twisted branches snaking upwards carrying a
bristling canopy of needles, the tree was a favourite of the author J.R.R. Tolkien (1892–1973) and may have inspired his epic Lord of the Rings trilogy. One of the last photographs taken of Tolkien has him sitting companionably against its trunk.1
Sadly, though, in 2014 the decision was taken to cut down ‘Tolkien’s tree’ after two of its limbs creaked, groaned, and then finally collapsed, making it unsafe for
visitors to the garden. Hope is not lost, however. Future generations, and Tolkien
Ancient genes, new pl Ants a 67
fans, may yet get the opportunity to see it, as there are plans to attempt propagation of the magnificent tree from cuttings.
All told there are around 3000 botanical gardens worldwide, living repositories
of plant diversity that provide documented collections of plants for our enjoy-
ment, as well as for conservation and research.2 Over half of the world’s popula-
tion now lives in urban areas and botanical gardens provide them with green
oases (Figure 8). The telling statistic is that 250 million people visit these botanic gardens each year. It points to our deep-seated desire to experience the greenery missing from our sophisticated urban lives and, perhaps, kindle an interest in
understanding something of its evolutionary history. Clues to the past are there
for those who care to take a close look at the plants themselves. Notice the underlying unity in the way they are constructed. Everything, from ferns and trees to
shrubs and grasses, conforms to the same basic modular body plan of repeated
structures and organs that form shoots and roots. In fact, when you stop and
think about it, it is easy to appreciate that shoots are simply composed of bits of stem and leaf, iterated repeatedly until a flower or some such reproductive structure appears on the end. Land plants hit on this winning blueprint early in their evolutionary history and have stuck with it ever since.
Plants began colonizing the land back in the Ordovician (named after a Celtic
tribe living in Wales, the Ordovices), and their explosive diversification across the landscape followed in the Devonian Period (419–355 million years ago). Written in rocks of Devonian age is a geological diary beautifully documenting the process
of green hegemony that ensured the irreducible dependency of the world on the
photosynthetic produ
cts of plants. The habitats and ecological opportunities
created by evolving terrestrial floras set the stage for the subsequent appearance and diversification of animal life on the continents. Irresistibly dubbed the Devonian
‘big bang’, this remarkable burst of evolutionary innovation saw the escalating
ascendency of plant life over an interval of roughly 60 million years.3 The
Devo nian Period was named after the picturesque county of Devon in south-west
England by geologists who first studied the fossil-bearing deposits in its rocks.
We can liken the plant kingdom’s Devonian ‘big bang’4 on the land to the earlier
‘Cambrian explosion’ of the animal world in the oceans. The Cambrian explosion
began about 541 million years ago and saw most of the great animal phyla appear
in the fossil record over about 50 million years—suddenly, in geological terms.
Both events have the hallmarks of dramatic biological innovation at the start, and
People per 1,000 km2
0.01 – 0.1
0.1 – 1
1 – 10
10 – 100
100 – 1,000
1,000 – 10,000
Figure 8 Global network of over 3000 botanic gardens overlain onto a map of human population density.
Ancient genes, new pl Ants a 69
both ended with the assembly of a complex web of life, forming ecosystems
broadly analogous to their modern counterparts.5 By the end of the Devonian
‘big bang’, most of the major modern lineages of plants—bryophytes, lycophytes,
ferns, and seed plants—had originated, and with them striking organs and tissues
like leaves, roots, seeds, and wood.
Palaeontologists love to study the fossil record of this time, and for good
reason. A handful of sites continue to offer rich and rewarding new sources
of information on the evolution of the plants themselves. A few exceptional
localities have fossils in which soft tissue has been preserved, a consequence of unique conditions under which minerals have replaced the original organic matter to record astounding details of cellular anatomy. Still, the fact is that neither palaeontologists, nor anybody else for that matter, can do experiments with the
fossils to discover the details of how plants underwent such dramatic diversification in form and function. Fossils provide the framework for thinking about
what happened, but stay silent on the matter of how it happened. For insights into how the drama unfolded in the evolutionary theatre of the Devonian world, we
need to turn to the DNA record of living plants.
We have already seen how DNA helped solve the question of the origin of land
plants: they evolved from freshwater charophyte algae that surmounted the for-
midable challenges of life out of water. We have also seen how the genomes of
wayfaring plants changed during their spectacular transition from anatomically
simple freshwater algae to large, complex, multicellular organisms such as trees, cloaking the near-barren landscape with forests of leaves. Now we must concern
ourselves with how the genetic ‘toolkits’ within those plant genomes built the
innovations they needed for succeeding in the new rocky environment in which
they found themselves. We must give substance to claims that ancient genetic
programmes became co-opted, expanded, and were repeatedly fine-tuned by
evolutionary rewiring to give rise to the amazing diversity of plants alive today.6
This is really the everyday stuff of evolution revealed by a branch of science called
‘evo-devo’. Evo-devo deals with the evolution of developmental pathways regulating how plants (and animals) grow cell by cell from embryo to adult. By seeking to understand how the genetic circuitry of the cells operates, it provides fundamental insights into the nature of evolution itself. It seeks to document the Darwinian processes of natural selection and descent with modification across vast tracts of geological time.
70 a Ancient genes, new pl Ants
One of the first things the fossil record makes clear is a surprise: shoots evolved before roots. Leafless shoots came first, followed by leafy shoots, followed by
shoots with proper roots. The term ‘leafless shoots’ might be over-cooking it as a description of the earliest vascular land plants. These tiny plants that lived on land over 400 million years ago were little more than simple naked delicate axes,
only a few millimetres tall, anchored into sediments with simple fine rootlets.
Presumably, the naked stems of these minute photosynthetic pioneers were green,
perhaps like those of modern whisk ferns ( Psilotum) or sedges ( Carex), to allow them to conduct the daily business of photosynthesis, although there is no way currently of knowing for sure.7 Whatever the extent of ‘green-ness’, these land plants photosynthesized without leaves. That innovation appeared in its simplest form as a microphyll leaf, essentially a narrow strap-like structure with a single unbranched vascular strand running through the centre, which appeared a few millions years
later. Lycophytes had microphyll leaves and later gave rise to the giant trees that grew to heights of over 40 metres and dominated the Carboniferous swamp forests
300 million years ago. Today, this type of leaf is only to be found clothing the
miniature cone-bearing spires of the last surviving lycophyte lineages from those early days of plant life on land: clubmosses, spikemosses, and quillworts. Quillworts are small aquatic herbaceous plants that also possess another overlooked trait connecting them to the giant trees of the Carboniferous—their rootlets share a pat-
terned architecture similar to those found in fossils of the long-extinct trees.8
Leaves of a sort that are familiar to us, those with an arched flat blade and a
cantilevered support structure, begin to turn up in the fossil record 30 million
years after plants with microphyll leaves appeared on the scene. These laminated
structures are called megaphyll leaves. A megaphyll leaf is really a photosynthetic leaf blade irrigated with a complex, branching vascular network of tubes for efficiently delivering water to the photosynthesizing tissues.9 Among the oldest
examples are those of the rare specimen called Eophyllophyton bellum, whose fossils have been excavated from 390-million-year-old Devonian rocks in China.10 The
exquisite, deeply incised miniature leaves of Eophyllophyton fossils are preserved as thin films of carbon, black smears on rock surfaces reaching only a few millimetres across. The quality of preservation of these early Chinese fossil leaves is astonishing. Prepare them with sufficient care and patience, and it is possible to reveal intricate networks of branching veins within the fossilized tissues. By late in the
Ancient genes, new pl Ants a 71
Devonian, everything from ferns to seed plants converged on leaves as an optimal
solution for harvesting solar energy to power photosynthesis.11 The fossil record tells us that at least four different vascular plant lineages independently evolved the same variety of solar umbrella, including progymnosperms (extinct forerunners of gymnosperms), sphenopsids (extinct), ferns, and seed plants. Each of the
four lineages then followed the same evolutionary trajectory for making compli-
cated leaf shapes, a fact that genetics can explain, because all four inherited the same genetic toolkit for programming leaf development from a common ancestor, and there were only so many ways it could be rewired to make complex leaf
architectures.12 Leaves, then, have a certain inevitability about them. Re-run the evolutionary tape of life, to use a metaphor beloved of some evolutionary biologists, and it is a safe bet that sooner or later photosynthetic life forms colonizing the land will start making leaves.
Yet the fundamental questio
n is surely this: what was the underlying genetic
machinery that gave rise to leaves in the first place? How did plants evolve from tiny naked stems into leafy shoots? Answering that question means that we
first need to know something of how modern plants make leaves, and the
action starts with stem cells located at the apex of the shoot. Stem cells are
special and, rather confusingly, do not simply make stems. They provide a source
of new cells to grow or replace a variety of specialized tissues. To perform this function, they divide to renew themselves, leaving their descendants free to accumulate and form the new tissues. It follows, then, that stem cells possess the special property of being able to produce the full diversity of cell types a plant needs for growth and reproduction. Indeed, this was confirmed by classic experiments
in the 1970s which showed that virtually all the tissues of a shoot descend from
small groups of stem cells. This explains why entire plants with stems,
branches, leaves, flowers, and so on can be grown from small pieces of tissue,
or even a single cell.13 It also explains why all is not lost for Tolkien’s tree; regeneration ought to be possible. Stem cells are really the secret to the long
lifetimes of trees. They can regenerate and produce populations of unspecial-
ized stem cells over the lifetime of the plant to renew worn-out structures, shielded, somehow, from mutational meltdown. Anyway, the point is that leaves arise from
the cluster of self-renewing stem cells at the tip of the shoot, called a meristem (Figure 9).
72 a Ancient genes, new pl Ants
Adult plant
shoot meristem
Seedling
250mm
5 mm
root
meristem
Figure 9 Shoot and root meristems build whole plants.
One of the tasks of meristems in the shoot is to constantly ‘decide’ when it is
appropriate to continue growing and when to do some other more specialized
job like building a leaf or flower. Genes tightly controlling the balance between normal shoot growth and making leaves have a shared ancestry that reaches
back to the golden age of Devonian evolutionary innovation.14 Tight regulation
Making Eden Page 11