Making Eden

by David Beerling

  we may have been missing. The plants concerned were ancient grades of spore-

  bearing vascular land plants including the lycophytes and primitive ferns like

  adder’s-tongue ( Ophioglossum) and moonworts ( Botrychium) that are descended from some of the earliest known vascular land plants.39 The life histories of these plants fascinated W.H. Lang, who reported discoveries of fossilized Devonian terrestrial life at Rhynie. Lang was quick to appreciate what our modern flora can

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  contribute to understanding past evolutionary events.40 In the simple vascular

  land-plant groups, spores shed by adults germinate into diminutive plants

  (gametophytes) that are essentially small packets of cells, a few millimetres in

  diameter. Buried in soil and thick layers of leaf litter, the developing plants are a distinctive phase of the life cycle that lack chlorophyll and are unable to photosynthesize. Without being able to feed themselves by photosynthesis, it is easy to be

  fooled into thinking these small subterranean plants are making a living as saprotrophs, obtaining nourishment directly from decomposing leaf mould in the soil.41

  The truth is that the romantic notion of saprotrophic plants is a myth, decisively debunked by Leake, whose forensic dissection of the literature shredded the supposed supporting evidence.42 Clues to the unusual mode of nutrition supporting

  their growth surfaced when detailed microscopic observations revealed them to be

  colonized by fungi, which later DNA analyses identified as mycorrhizal fungi.43

  Instead of feeding themselves by photosynthesis, or acting as saprotrophs, these

  tiny plants hidden underground are supported by carbon energy subsidies sup-

  plied by mycorrhizal fungi. It is an unusual mode of nutrition and a remarkable

  case of plants parasitizing fungi. Now recognized in over 400 species, this way of life (known as myco-heterotrophy) evolved many times in different groups of

  plants, possibly as an evolutionary solution to living in the shaded forest understory where effective photosynthesis is difficult.44

  The story of plants parasitizing fungi took an intriguing new twist when

  re searchers at the University of Colorado discovered that subterranean gameto-

  phytes and photosynthetic sporophytes of several species of lycophytes and ferns

  associate with the same specific group of mycorrhizal fungi.45 The startling implication here is that adults (sporophytes) photosynthesizing in the sunlight above

  ground are feeding offspring (gametophytes) buried in soil with carbon supplied

  through shared networks of mycorrhizal fungi.46 In all, about 100 species belong-

  ing to several genera of early vascular land plants ( Lycopodium, Huperzia, Psilotum, Botrychium, and Ophioglossum) produce gametophytes that develop in soil or litter and lack chlorophyll. Unable to feed themselves by photosynthesis, they are entirely dependent on subterranean mycorrhizal networks connected to photosynthetic

  adults to supply carbon and nutrients. The idea is still in its infancy but it is a remarkable thought that green photosynthetic adults are nurturing progeny

  buried in soil via intergenerational carbon subsidies delivered through common

  networks of mycorrhizal fungi.47 If correct, the situation amounts to a case of

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  parental nurture by adults of the same species above ground. Given the antiquity of the plant groups involved, parental nurture through shared fungal symbiotic

  partners may have been a previously unrecognized feature of their ecology for

  millions of years.

  Consider how it might work over the life cycle of the adder’s-tongue fern

  ( Ophioglossum). As the spore germinates, it develops into a gametophyte fuelled by carbon energy supplied by photosynthetic adults above ground and delivered

  by its fungal partners. Following fertilization, the young sporophyte slowly develops by producing one or two small green photosynthetic leaves that emerge

  from the soil. Such an arrangement has the advantage of enabling sexual repro-

  duction to occur underground, with the gametophyte buried in the moist soil and

  afforded protection from desiccation.48 Thanks to relying on carbon subsidies

  from a mycorrhizal network to support their young, adults can produce prodi-

  gious numbers of dust-like spores. If you have ever dis covered ferns such as adder’s tongue in pastures and dune slacks, then you will appreciate that they often cluster together in large patches, containing hundreds of individuals. Conceivably, in

  such circumstances, adults are nurturing the youngsters of neighbouring plants

  via common mycorrhizal networks, and this arrangement amounts to a form of

  co-operative breeding in land plants.

  It is an extraordinary possibility and wrests the concepts of parental invest-

  ment and co-operative breeding away from the clutches of my zoological col-

  leagues along the corridor and into the hands of botanists. Ben Hatchwell,

  professor of behavioural ecology at the University of Sheffield, has made his name working out the details of co-operative breeding in long-tailed tits ( Aegithalos caudatus). These fascinating and highly social little birds are often heard before they are seen, flitting through gardens in flocks in the wintertime. During the spring, males and females pair up and work together to build intricate bottle-shaped

  nests with a hole at the top. If disaster strikes, and the chicks are eaten by a predator, the parents may abandon the nest and switch their attention to helping feed

  the chicks of a relative. This turn of events (which may seem surprisingly altruistic at first glance) sees the survival rates of these chicks improve thanks to ‘helper’

  birds raising the family. Extended family life continues after the fledglings become independent, with both parents and helpers investing time and effort for weeks

  afterwards to ensure survival. In long-tailed tits, Hatchwell has observed that

  individuals are more likely to help feed the chicks in nests belonging to a close

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  relative rather than distant relatives or unrelated individuals.49 Helpers are

  effectively improving the survival chances of their genes indirectly, even though their own attempts to pass on their genes directly by breeding have failed. We can marshal similar arguments for the lycophytes and ‘lower’ ferns, which grow in

  patches of closely related adults raising the offspring of close relatives to ensure the survival of their genes.

  If the notion of parental nurture of progeny via common mycorrhizal net-

  works in the plant world seems far-fetched, we should note that there may be a

  precedent for it in the orchids. Orchids are the most advanced group of plants on Earth and, with over 27 000 species, also the most diverse. They reproduce by releasing prodigious quantities of, typically, wind-dispersed dust-like seeds. Acting as tiny emissaries for the colonization of new habitats, the seeds require a symbiotic fungal partner for the provision of resources to germinate successfully and

  develop into a seedling. This strategy allows orchids, like the more ancient groups of lycophytes and ferns, to maximize seed production and wind dispersal through

  minimal maternal investment. Parent plants rely on symbiotic fungi to make

  good the deficiency in carbohydrates needed for seedling establishment.50 The

  analogy between advanced and primitive vascular land plants extends further.

  Subterranean orchid seedlings lack chlorophyll and form tuber-like structures

  that so closely resemble the non-photosynthetic gametophytes of lycophytes and

  ferns they share the same unique botanical term—a protocorm (Figure 21).

  Striking anatomical similarities exist among the struc
tures of the protocorms of

  these widely separated evolutionary groups of plants (orchids and lycophytes),

  which associate with very different groups of symbiotic fungi, to secure and

  sequester carbon supplies obtained from them.

  All this was unknown to Charles Darwin, who was fascinated by orchids and

  their spectacular floral diversity and published his classic work on this group, The various contrivances by which orchids are fertilized by insects in 1862. Not a trifling effort but a great labour of love, the book was written after 20 years of studying every facet of orchid biology. Yet germinating orchid seed proved beyond him. In frustration, Darwin wrote a letter in 1863 to his friend and mentor Joseph Hooker,

  Director of the Royal Botanic Gardens Kew, saying that despite having ‘not a fact to go on’, he had ‘a notion, (no, I have a firm conviction) that they [germinating orchid seeds] are parasites in early youth on cryptograms [i.e., fungi]’.51 Darwin was right, and ahead of his time. For the crucial involvement of fungi in orchid

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  Clubmoss ( Lycopodium obscurum)

  gametophyte with young

  sporophyte

  Orchid seedling

  ( Calanthe veitchii)

  Gametophyte of Adder’s

  Orchid protocorm

  tongue fern

  ( Dactylorhiza majalis)

  ( Ophioglossum pendulum)

  Figure 21 The soil-dwelling gametophyte of a fern bears a striking structural resemblance to the protocorm of a highly evolved orchid, as does the young sporophyte of a clubmoss and an orchid seedling. Scale bars = 100 mm in all diagrams except Lycopodium obscurum where it = 500 mm.

  seed germination was not discovered for another three decades, when it was

  reported in 1899 by the French botanist Noël Bernard (1874–1911).52 Darwin gave

  no reason for his ‘firm conviction’. Presumably, the tiny size of orchid seeds raised the possibility in his mind that they required additional food reserves from some other source (or organisms) to ensure successful germination—a situation that

  obviously parallels the dust-like spores of lycophytes and ferns, early-evolving vascular plant lineages.

  Darwin recognized that mutualistic associations like those between fungi and

  land plants apparently presented a major problem for his evolutionary theory.

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  How can co-operative associations between different groups of organism persist

  when natural selection favours selfishness and conflict? Despite his puzzlement,

  mutualistic associations are common in nature from fig trees and their fig-wasp

  pollinators, to fungus-growing ants, and to squids with their bioluminescent

  bacterial symbioses. The central evolutionary paradox of mutualistic associations is the uneasy co-operation between organisms. Uneasy because the relationship

  is inherently unstable and liable to break down if either partner selfishly exploits the other by taking but not giving anything back in return. There must be

  mechanisms for stabilizing it in the long run; otherwise, how could it have endured for millions of years?

  For land plants entering into mutualistic partnerships with mycorrhizal fungi,

  experiments are starting to reveal some answers to these questions. Plants, we

  discover, are very discriminating in their choice of mycorrhizal fungal partner,

  rewarding only those species that provide a steady supply of phosphorus with a

  greater supply of photosynthate, and sanctioning less co-operative partners by

  shutting down their carbon supply.53 The reciprocal arrangement is that roots

  supply more carbon to the fungus, which obtains more phosphorus in return.

  A continual reinforcement of this sort helps stabilize the partnership and may be one of the reasons why the symbiosis between plants and mycorrhizal fungi

  has endured for hundreds of millions of years. It is distinct from other examples of mutualism found in nature, where one partner often appears in control. In the

  mycorrhizal mutualism, both sides—plants and fungi—interact with multiple

  partners, making each resistant to being enslaved. Nature’s free market economy

  suggests an uneasy co-operation stabilized by competitive partners on both

  sides, remunerating those supplying the highest quality services.54

  Stability does not necessarily mean there are no freeloaders. ‘Cheater’ plant

  species lacking the ability to photosynthesize can break co-operative arrange-

  ments to become parasites. Sir David Read at Sheffield University uncovered a

  fascinating example of this phenomenon with the case of a liverwort ‘cheating’

  on a symbiotic partnership between trees and their fungal partners by ‘stealing’

  carbon. The cheat in question is a strange thalloid liverwort called ghostwort

  ( Aneura mirabilis) that lives in the litter and soils beneath European birch, pine, and oak forests and has lost the ability to photosynthesize. Ghostwort is the only known example of a non-photosynthetic bryophyte. It lives a subterranean

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  lifestyle and is dependent on symbiotic fungi for supplies of energizing carbon

  compounds and other nutrients, which it obtains by cheating—it parasitizes the

  symbiosis by tapping into a fungal ‘internet’ linking the roots of forest trees to their symbiotic fungi. In essence, these liverworts are stealing the carbon they

  need from the trees in the network rather than obtaining it from the soil itself.55

  In an evolutionary sense, Aneura appears to have ‘learned’ which clade of mycorrhizal fungus is a soft touch and can be tricked out of its persistent supplies of carbon delivered by the host tree. Aneura exhibits extreme fungal fidelity, only associating with a specific fungal clade that forms partnerships with pine and

  birch trees. How it manages to be so highly selective in forming this specific association rather than exploit those fungi connected to the roots of other tree species is an open question. Molecular geneticists soon became interested in the unusual

  story of this tripartite symbiosis between a tree, a fungus, and a liverwort.56 They discovered that exploiting fungal carbon sources relieves the liverwort of the need for the genes required for photosynthesis. And this seems to be rule rather than

  the exception for parasitic plants. The chloroplasts of the flowering plant species Epifagus virginiana, which is strictly parasitic on the roots of beech trees, have also lost the ability to photosynthesize, and with it, a similar number of genes.57

  Q

  Over 40 years ago, Pirozynski and Malloch presciently argued that the Devonian

  fossil record of plant life raised fundamental questions concerning the symbiotic origin of plant life on land. They provocatively raised the intriguing hypothesis that an ancient partnership between symbiotic fungi and land plants was essential to colonizing the continents. It challenged future generations to evaluate critically their speculative idea. Recent discoveries are giving greater clarity and

  offering new perspectives on the sequence of events that lay behind the origin of the terrestrial biosphere and the identity and roles of the fungal groups involved.

  Matters that had remained speculative for nearly half a century are being resolved, crystallizing a more complex and fascinating picture than Pirozynski and Malloch

  could have envisaged.

  Our best reconstruction for the earliest events is that primitive fungi formed

  part of early soil-forming communities in the Ordovician landscape, over 420

  million years ago. Some of these lineages included the pea truffles and their close

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  relatives, which operated in partially saprotrophic mode, feeding on decaying

&n
bsp; algae and cyanobacterial mats. As simple rootless early plant life made the transition to land, beneficial plant–microbe alliances developed. With plants offering a safe, carbon-energy-rich haven, some lineages of pea truffle fungi abandoned

  their saprotrophic lifestyle to forge symbiotic alliances with them. Plants, in

  return, gained access to soil nutrients captured by their fungal partners. As plant life on land evolved, and diversified, the first humus-rich soils developed and the economics of earlier arrangements shifted. Plants developed symbiotic partnerships with arbuscular mycorrhizal fungi specially adapted for mining and extract-

  ing elemental nutrients from rocks and minerals, especially phosphorus—an

  essential ingredient for building crucial biomolecules needed to run their metab-

  olism. Some pea truffle fungal groups reneged on the contract, abandoned the

  plants that had served them so well, and went back to decomposing the increas-

  ingly abundant organic matter to obtain energy. Other fungal groups stayed put,

  allowing some plants to benefit by collaborating with two different groups.

  The co-evolution of plants and symbiotic soil fungi continued, and in the next

  phase a new type of mycorrhizal association appeared in which ectomycorrhizal

  fungi began colonizing tree roots. The oldest fossils are of roots belonging to

  Pinaceae trees, and the tropical tree group Dipterocarpaceae, and date to around

  41–55 million years ago, although evidence from molecular clocks hints at much

  earlier origins during the Jurassic, about 180 million years ago. Ectomycorrhizal fungi evolved multiple times from saprotrophic ancestors and most reproduce

  sexually by developing fruiting bodies above ground—recognizable mushrooms

  like bolets, amanitas, and chanterelles. They associate mainly with the roots of

  boreal and temperate tree species, and support the health of forests by releasing enzymes to digest humus in the soil and extract nutrients otherwise not available, then transfer them to the trees.

  The sequencing of fungal genomes has shown how ectomycorrhizal fungi have

  shed unwanted genomic baggage inherited from their saprotrophic ancestors to

  make their symbiotic lifestyles possible.58 ‘Unwanted’ because saprotrophic fungi decompose dead plant tissue in soil litter for energy by secreting enzymes that