Making Eden

by David Beerling

  the soil by roots penetrating between soil particles to absorb films of water and dissolved nutrients, these opportunistic colonizers prospered. Ferns diversified

  rapidly into prostrate crawlers, climbers, scramblers, and sprouters. Some occu-

  pied shady quarters of the forest floor and others colonized flood plains, regions decimated by wildfire, and the flanks of volcanoes. By far the greatest diversity sprang up in the tropics.61 Ferns reproduced by releasing spores from orange-brown packets located on the underside of fronds. Some of the stranger examples

  in our modern floras are the whisk ferns like Psilotum and the horsetails ( Equisetum).

  The stems of horsetails are encircled by rings of needle-like leaves that look quite unlike true ferns, and have spore-bearing cones on the tips of the shoots.

  Appearances can be deceptive, however. For many years, classifications based on

  morphology (the look of the thing) saw them separated from true ferns, only for

  the molecular characters of their DNA to reveal that whisk ferns and horsetails

  are actually true ferns, no matter how strange they look.62 Like their lycophyte

  cousins, the direct ancestors of horsetails reached lofty heights in the Carboniferous, at a time when giant dragonflies took to the wing.63

  New shades of green and a rich diversity of leafy textures followed, as seedless

  vascular plants began proliferating and filling out the landscape with angular new

  FiFty shades oF green a 29

  geometries. Really, though, it was the origin of seed plants that ratcheted up the unstoppable business of greening the planet, giving it significant extra energy and momentum. The first seed plants arose late in the Devonian, at least 365 million

  years ago, and a wide array of seed-bearing plant forms followed. All were prob-

  ably descended from an extinct seedless group of plants called the progymno-

  sperms that foreshadowed the forests that were still to come. Some members, like

  the tree Archaeopteris, attained heights of 17 metres or more, and occasionally formed extensive stands of trees. These early seed plants ultimately led to the

  appearance of gymnosperm trees that went on to dominate forests throughout

  the age of the dinosaurs, the Mesozoic Era.

  Just four living groups of gymnosperms survive in our modern floras—conifers,

  distinctive gnetophytes, cycads, and the maidenhair tree ( Ginkgo). Gymnosperms (from the Greek gymnospermos, meaning ‘naked seeds’) develop seeds either on the surface of scale-like appendages of cones or at the end of short stalks in the case of Ginkgo, with its distinctive fan-shaped leaves. Conifers are the largest group, with over 600 species, including the pines, spruces, larches, and firs that dominate vast tracts of boreal forest in the subarctic regions of North America and Eurasia.

  Gnetophytes are weird plants with features similar to conifers and flowering

  plants. None is stranger than Welwitschia, named after the Austrian botanist Friedrich Welwitsch (1806–1872) who discovered it in 1859. Confined to the Namib

  Desert in southern Africa, Welwitschia can live for decades or even centuries.

  Described as the ‘plant from Mars’, it is not hard to see why. The plants live a

  curious existence, persisting with two sprawling strap-like photosynthetic leaves that inch across the desert floor often reaching ungainly lengths of several metres.

  Cycads are the second most diverse and widespread lineage of gymnosperms,

  with about 300 species. They are distinctive for the dense whorl of leathery leaves sprouting near the top of a thick trunk. At first glance, cycads might be mistaken for small palm trees or even ferns, until you notice the striking heavy seed-bearing cones topping these sturdy trees, which once flourished amid the dinosaurs during the Jurassic. Today, they comprise relict components of our floras, representing the last remnants of their formidable past . 64

  Understandably, Michael Crichton could not resist the charms of cycads in the

  film, Jurassic Park. ‘Those trees to your left and right are cycads, prehistoric predecessors of palm trees. Cycads were a favourite food of the dinosaurs’, intoned the narrator as the occupants of the land cruisers drove through the park. We can

  30 a FiFt y shades oF green

  admire the botanical correctness of placing cycads amongst the dinosaurs but

  should note that scientists from the Natural History Museum, London, have since

  revised the story of cycad-eating dinosaurs.65 Once, the thick, tough stems and

  leaves and the extreme toxicity of the foliage were thought to have evolved as protection against dinosaurs. Sadly, this romantic notion has fallen to modern sci-

  ence. The toxicity of cycad foliage evolved sometime in the Permian, tens of

  millions of years before the dinosaurs appeared, probably as a by-product of

  primitive plant biochemical pathways. The idea that brightly coloured cycad

  seeds appeared as a means of attracting dinosaurs as agents of dispersal has also fallen to the same team from the Natural History Museum—fossilized dino-dung

  shows no trace of cycad seeds. The job of cycad seed dispersal back then fell to

  other exotic Cretaceous fauna, and to oceanic currents in the case of those lineages clinging to coastal regions.

  Ascending towards the upper branches of the plant tree of life, we leave the

  gymnosperms behind to encounter the angiosperms, or flowering plants, which

  burst onto the evolutionary stage, transforming the surface of the Earth with

  colour. The flower power revolution took off early in the Cretaceous, around 125

  million years ago. Molecular clocks suggest that flowering plants originated far

  earlier and indeed there have been scattered reports for their putative remains

  excavated from Triassic and Jurassic rocks. None of these claims, however, has yet stood up to critical scrutiny.66 Today, there are more than 223 000 species of

  flowering plants, dwarfing the diversity of all other plant lineages; 75–85% of all known plant species on Earth are flowering plants (Figure 2 and Plate 3). Molecular sequencing, combined with the rich fossil record of flowers, seeds, and leaves, has proved successful in resolving much of the gloriously detailed family history of

  the two main evolutionary lines—the ‘monocots’ and the ‘eudicots’.67 The mono-

  cot group, including lilies, orchids, sedges, and the grasses that gave us cereals, has only one seed leaf. Seedlings of the eudicots typically develop a pair of tiny green leaves quite distinct in shape from those of the mature leaves that develop subsequently. Most of the familiar trees, shrubs, and herbs in our woodlands and

  hedgerows are classified as eudicots.68

  Writing for the National Geographic, the American author John Updike (1932–

  2009) paints the natural history of the scene on land for us sometime late in the Cretaceous, when many of these groups of plants had evolved, like this:

  FiFty shades oF green a 31

  Lycophytes

  Ferns

  Gymnosperms

  Anglosperms

  Figure 2 The relative species richness of the major

  clades of plants.

  Bryophytes

  Charophytes

  Chlorophytes

  Rhodophytes

  Glaucophytes

  By the late Cretaceous the continents had something like their present shapes,

  though all were reduced in size by the higher seas, and India was still an island heading for a Himalaya-producing crash with Asia. The world was becoming the

  one we know: the Andes and the Rockies were rising; flowering plants had

  appeared, and with them, bees. The Mesozoic climate, generally, was warmer than

  today’s, and wetter, generating lush growths of ferns and cycads and forests of evergreens, ginkgoes, and tree ferns
close to the Poles; plant-eating dinosaurs grew

  huge, and carnivorous predators kept pace. It was a planetary summertime, and

  the living was easy.69

  The living was easy, of course, because green plants had won the land, no ques-

  tion, and become fabulously successful at the business of reproducing on dry

  land. The stars of those early green waves of colonization, the proto-bryophytes, bryophytes, lycophytes, and ferns, all reproduced with spores and not seeds, and

  remained dependent on water for fertilization. The same holds true for the strug-

  glers and the also-rans in land-plant evolutionary history, represented by extinct vascular plant groups, including obscure groups such as the rhyniophytes, trim-erophytes, and progymnosperms. All had acquired the ability to reproduce on

  land thanks to a dramatic shift in their life history that provided an enormous

  advance over the watery sexual mechanisms of their algal ancestors.

  32 a FiFt y shades oF green

  Take the weird sex life of the filamentous photosynthesizer algae of the order

  Zygnematales, a clue to which is in their common name—the conjugating green

  algae. Unlike most other green algae, they lack flagella and reproduce sexually

  through variations in the process of conjugation. Cells of opposite gender line up in parallel filaments and tubes form between corresponding cells. Strangely, the

  non-flagellated male cells then become amoeboid and crawl across to meet the

  egg cell. Here they fuse and form a zygote, which later undergoes cell division to produce offspring, with only the female passing chloroplasts on to her offspring.

  The business of reproduction is no less strange in the Coleochaetales. Bathed in a supportive and protective watery environment, adult plants develop specialized

  structures that produce a large egg and smaller free-swimming male sperm.

  Sperm fertilize the egg to form a zygote, which is retained on the parent plant and undergoes cell division to produce spores. Cells surrounding the zygote divide to produce a layer of sterile tissue that envelopes it, and possibly provides it with nourishment during spore production. Finally, the zygote ruptures and releases

  its cargo of swimming spores. We can see from this outline that Coleochaete is obviously totally dependent on water for sexual reproduction. Yet, at the same

  time, it has the beginnings of something resembling care of a developing embryo,

  one of the hallmarks of land plants.

  From this rather mixed bag of algal reproductive biology, land plants evolved a

  critical modification to their life history that would change the world. In some

  distant charophyte ancestor, after fertilization and the formation of a zygote,

  something different happened. Instead of directly producing spores, the cellular

  machinery was reprogrammed to produce a tiny erect multicellular plant, the

  ‘sporophyte’, for manufacturing spores. This small but momentous event gave

  plant life a new distinction between the ‘sporophyte’ and the parent plant that

  produced the eggs and sperm (gametes), called the ‘gametophyte’. The sporo-

  phyte grew, at least initially, attached to its amphibious parent, anchored into

  ‘soggy sediments’. The first such structures developing on tiny ancient green

  plants would hardly have qualified as bona fide ‘land plants’. While details of the life cycles of the proto-bryophytes that first took hold on the land are sketchy, some simple variant of this basic advance probably led to their persisting out of water for several generations.70 Merciless natural selection ensured only the fittest surviving descendants would live on to reproduce and turn the continents green.

  Land ahoy.

  FiFty shades oF green a 33

  This development represented a crucial and profound step forward, but at first

  the advantage of nurturing a multicellular sporophyte would have been subtle. The immediate benefit of sporophyte generation was to facilitate the production of millions of spores following a single fertilization event. And by growing above the

  ground surface, plants could release spores into more turbulent air currents found there, ensuring they travelled further and spread out to colonize new areas. In the longer run, the sporophyte phase became free to grow larger, more complex, and

  develop specialized tissues for survival and spore production and dispersal on land.

  The fossil record tells us it was not long, probably a few tens of millions of years, before land plants evolved large size differences between the gametophyte and

  sporophyte generations. By around 410 million years ago, sporophytes had

  advanced to become an autonomous generation, free of their smaller fleshy gam-

  etophyte parent that attached itself to muddy substrates by simple rootlets called rhizoids.71 Ever since, across the grand sweep of plant evolutionary history, the general trend has been one of an increasing dominance of the sporophyte generation at the expense of the gametophyte generation. The natural histories of bryophytes, ferns, and seed plants illustrate the trajectory that ultimately saw the reduction of the gametophyte generation in flowering plants to a less-than-conspicuous

  handful of cells.

  All three groups of bryophytes (mosses, liverworts, and hornworts) have life

  cycles reflecting those early stages of terrestrial events, with a dominant gametophyte generation and diminutive sporophyte generation. Take the life cycle of the prostrate liverworts. Sexual reproduction begins in the gametophyte generation

  when the flattened thallus of the male plant sprouts miniature umbrella-like

  structures that produce sperm, and the females sprout umbrella-like structures

  that make the female reproductive organs. For successful fertilization, and to

  avoid inbreeding, some liverworts have evolved remarkable tricks. Microscopic

  sperm released by the male plants are large and have flagella, making them strong swimmers. Often they are released simultaneously with lipid droplets, which aid

  their dispersal by carrying them on a lipid ‘skin’, perhaps only a single molecule thick, that spreads out over ten metres. The films of water carrying the sperm

  ascend the umbrella handles of the female plants by capillary action, aided by narrow grooves and little pegs to ensure water rises and delivers the sperm to the

  eggs. When sperm fertilize the female egg cell, the embryo plant or sporophyte

  generation develops. Protected in a sac suspended from beneath the stalk of the

  34 a FiFt y shades oF green

  umbrella, the miniature multicellular plant draws its nutrients from the female

  parent plant.72 Wrapped in a tough coating, the spores it makes gain protection

  from the elements and are released when gentle currents of air or rain drops buf-

  fet the tiny plant structure. When conditions are right, the spores germinate to

  produce a new thallus. On reaching maturity, up goes its umbrella to complete

  the life cycle.

  Details differ between bryophytes, and the life cycle described above is quite an intricate, advanced example. Mosses provide a simple example (Figure 3). In suitable conditions, spores germinate to give rise to a filamentous thread (protonema).

  Some of these give rise to the rhizoids, stems, and leaves that make up the adult Germinating

  spore

  Sporophyte

  generation

  Developing

  gametophyte

  Sperm (male gametes)

  Leafy gametophyte

  generation

  Male

  Male

  Female sex org

  F

  ans

  se

  s x

  e

  organ

  (antheridium)

  Figur
e 3 Lifecycle of a moss ( Physcomitrella) with an alteration of generations between the gametophyte and the sporophyte phases.

  FiFty shades oF green a 35

  gametophyte (also called the leafy gametophore) which carries the male (anther-

  idium) and female (archegonium) sexual organs (together called the gametan-

  gium). The antheridium produces flagellated sperm that actively swim in a film of water to the archegonium for fertilization. The resulting fertilized egg cell (zygote) gives rise to the embryo, the sporophyte represented here by the spore cap-

  sule (sporangium).

  The critical point is that it illustrates how a single species of plant can have two generations that are completely different to each other. The insertion of a multicellular sporophyte generation was a fundamental developmental innovation of

  land plants and allowed nurturing of the developing embryo, a defining feature of the biology of all land plants (which is why botanists call them embryophytes).

  The notion of plants as dual entities, having two distinct generations, which look completely different from each other, takes a bit of getting used to. No animals

  undergo this ‘alternation of generations’. Not that this has been a barrier to the imaginations of fiction writers—think of Robert Louis Stevenson’s 1886 classic

  The Strange Case of Dr. Jekyll and Mr. Hyde, or Marvel Comics’ The Incredible Hulk—

  where very different manifestations are imagined for the same creature. You

  might imagine that the remarkable transformative metamorphosis of caterpillars

  into butterflies is an example but it is not a true case of the alternation of

  generations. The adult butterfly appears to act like a sporophyte by laying eggs but the caterpillar is not acting in the role of a gametophyte, with male and female sex organs.

  By the time early vascular land lineages, such as lycophytes and ferns, appeared

  on the scene, the sporophyte generation had undergone significant evolutionary

  advances. It was no longer diminutive, and no longer dependent on its parents.

  Instead, it had become a large, dominant, and free-living plant, as the natural history of ferns illustrates. There are more than 10 000 fern species, with highly

  diverse forms, ranging from minute understory herbs to spectacular tree ferns.