Making Eden

by David Beerling

  16. The highly controversial claim for evidence of fossil remains of a past Martian biota was originally reported here: McKay, D.S. et al. (1996) Search for past life on Mars: possible relic biogenic activity in Martian meteorite ALH84001. Science, 273, 924–30.

  17. Delwiche, C.F. & Timme, R.E. (2011) Plants. Current Biology, 21, R417–22.

  18. Delwiche & Cooper (2015).

  19. Becker, B. & Marin, B. (2009) Streptophyte algae and the origin of embryophytes.

  Annals of Botany, 103, 999–1004.

  20. Harholt, A., Moestrup, P.O. & Ulvskov, P. (2016) Why plants were terrestrial from the beginning. Trends in Plant Science, 21, 96–101. DeVries, J. & Archibald, J.M. (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytologist, 217, 1428–34.

  21. See Delwiche & Cooper (2015) for a discussion.

  22. Delwiche & Timme (2011).

  23. Becker, B. (2013) Snowball earth and the split of Streptophyta and Chlorophyta. Trends in Plant Science, 18, 180–3.

  24. His argument rests on clues deciphered from the ancient metabolic pathways of algae.

  The first major Snowball Earth glaciation, known as the Sturtian glaciation, some 720

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  million years ago, was brought about by plummeting atmospheric levels of carbon

  dioxide that imposed conditions of carbon dioxide starvation on algae who struggled to photosynthesize. Chlorophytes living under dimly lit oceanic conditions beneath

  thick sea ice evolved energy conservation strategies for coping with carbon dioxide deprivation. Charophyte algae, on the other hand, living in temporary freshwater pools on top of the snowball, where sunlight was brighter, were not subject to the same energy constraints, and evolved energy-intensive metabolic strategies for survival.

  25. Becker & Marin (2009).

  26. Church, A.H. (1919) Thalassiophyta and the subaerial transmigration. Oxford Botanical Memoirs, 3, 1–95.

  27. Becker & Marin (2009).

  28. Such conditions may even have prompted a primordial unicellular ancestor to undergo an evolutionary transition to a semi-terrestrial lifestyle that proved decisive in the origin of our land floras, see Harholt, A., Moestrup, P.O. & Ulvskov, P. (2016) Why plants were terrestrial from the beginning. Trends in Plant Science, 21, 96–101.

  29. Vermeij, G.J. & Dudley, R. (2000) Why are there so few evolutionary transitions between aquatic and terrestrial ecosystems? Biological Journal of the Linnean Society, 70, 541–54.

  30. Olsen, J.L. et al. (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature, 530, 331–5.

  31. Karol, K.G. et al. (2001) The closest living relatives of land plants. Science, 294, 2351–3; Lewis, L.A. & McCourt, R.M. (2004) Green algae and the origin of land plants. American Journal of Botany, 91, 1535–56.

  32. Finet, C. et al. (2012) Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Current Biology, 22, 1456–7. The authors use transcriptome data to derive phylogenetic relationships between Streptophytes and land plants. Nuclear DNA sequences of 77 genes from all lineages of Streptophytes and land plants produced a tree with Zygnematales and Coleochaetales as a sister group to land plants.

  33. Wodniok, S. et al. (2011) Origin of land plants: do conjugating green algae hold the key?

  BMC Evolutionary Biology, 11, 104). The authors used transcriptome data to derive phylogenetic relationships between Streptophytes and land plants. A nuclear sequence of 129 genes from all lineages of Streptophytes and land plants produced trees with either Zygnematales or Zygnematales + Coleochaetales as sister to land plants.

  34. During sexual reproduction, each female sex organ (oogonium) contains one large, immobile egg, and each male sex organ (antheridium) produces one small, biflagellate sperm.

  35. When crushed, these living relicts, the ancient relatives of which may have given rise to the terrestrial biosphere, release a strange garlic aroma. Only a few hundred species exist today, but they have a rich fossil record reaching back some 425 million years into the Silurian that documents their former glory.

  36. Kelman, R. et al. (2004) Charophyte algae from the Rhynie chert. Transactions of the Royal Society of Edinburgh: Earth Sciences, 94, 445–55.

  37. McCourt, R.M., Delwiche, C.F. & Karol, K.G. (2004) Charophyte algae and land plant origins. Trends in Ecology and Evolution, 19, 661–6.

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  38. Large-scale sequencing projects are now pointing to a new possibility—that the immediate ancestors of all land-dwellers belong to a clade of charophyte algae containing the Coleochaetales and the Zygnematales: Timme, R.E., Bachvaroff, T.R. & Delwiche, C.F. (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS One, 7, e29696. In this study, the authors used transcriptome data to derive phylogenetic relationships between Streptophytes and land plants. They sampled the nuclear DNA sequences of 160 genes from all lineages of Streptophytes and land plants and the analyses resulted in trees with Zygnematales as sister to land plants. See also discussion by Bowman, J.L. (2013) Walkabout on the long branches of plant evolution.

  Current Opinion in Plant Biology, 16, 70–7.

  39. This view was championed by Linda Graham at the University of Wisconsin. See, for example, Graham, L.E. (1984) Coleochaete and the origin of land plants. American Journal of Botany, 71, 603–8, and Graham, L.E. (1985) The origin of the life cycle of land plants.

  American Scientist, 73, 178–86.

  40. Graham, L.E. et al. (2012) Aeroterrestrial Coleochaete (Steptophyta, Coleochaetales) models early plant adaptation to land. American Journal of Botany, 99, 130–44.

  41. Niklas, K.J. (1976) Morphological and otogenetic reconstruction of Parka decipiens Fleming and Pachytheca Hooker from the Lower Old Red Sandstone, Scotland.

  Transactions of the Royal Society of Edinburgh, 69, 483–99.

  42. See, for examples, Shaw, A.J., Szovenyi, P. & Shaw, B. (2011) Bryophyte diversity and evolution: windows into early evolution of land plants. American Journal of Botany, 98, 352–69.

  43. Puttick, M.N. et al. (2018) The interrelationships of land plants and the nature of the ancestral embryophyte . Current Biology, 28, 1–13. See also: Chang, C., Bowman, J.L. & Meyerowitz, E.M. (2016) A field guide to plant model systems. Cell, 167, 325–39.

  44. Wellman, C.H., Osterloff, P.L. & Mohiuddin, U. (2003) Fragments of the earliest land plants. Nature, 425, 282–5.

  45. Ligrone, R., Duckett, J.G. & Renzaglia K.S. (2012) Major transitions in the evolution of early land plants: a bryological perspective. Annals of Botany, 109, 851–71.

  46. Hernick, L.V., Landing, E. & Bartowski, K.E. (2008) Earth’s oldest liverworts Metzgeriothallus sharonae sp. nov. from the Middle Devonian (Givetian) of eastern New York, USA. Review of Palaeobotany and Palynology, 148, 154–62.

  47. Guo, C-Q. et al. (2012) Riccardiothallus devonicus gen. et sp. nov., the earliest simple thalloid liverwort from the Lower Devonian of Yunnan, China. Review of Palaeobotany and Palynology, 176–7, 35–40.

  48. Heinrichs, J. et al. (2007) Evolution of two leafy liverworts: estimating divergence times from chloroplast DNA sequences using penalized likelihood with integrated

  fossil evidence. Taxon, 56, 31–44. Crandall-Stotler, B., Stotler, R.E. & Long, D.G. (2009) Phylogeny and classifications of the Marchantiophyta. Edinburgh Journal of Botany, 66, 155–98.

  49. Some botanists have looked at the spores of Haplomitrium and found them to be very simple, with thin spore walls that presumably afforded limited protection from desiccation. Some have suggested that this limits the scope for their preservation, leading to the notion that the early land plant spore record is not preserved (Renzaglia,

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  K.S. et al. (2015) Permanent spore dyads are not ‘a thing of the past’: on their occurrence in the liverwort Halpomitrium (Haplomitriopsida). Botanical Journal of the Linnean Society, 179, 658–69). But the fact is that spores te
nd to preserve, no matter how thin the wall. Sporopollenin is so robust that it always preserves. In fact, some of the early land-plant spores do have relatively thin walls compared to many modern

  spores and still preserve.

  50. Edwards, D. et al. (2014) Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytologist, 202, 50–78.

  51. Donoghue, P.C.J. & Yang, Z. (2016) The evolution of methods for establishing evolutionary timescales. Philosophical Transactions of the Royal Society, B371, 20160020.

  52. Clarke, J.T. et al. (2011) Establishing a time-scale for plant evolution. New Phytologist, 192, 266–301. See also the commentary: Kenrick, P. (2011) Timescales and timetrees. New Phytologist, 192, 3–6. See also: Morris, J.L. et al. (2018) The timescale of early land plant evolution. Proceedings of the National Academy of Science, USA, 115(6), E2274–E2283.

  53. Kenrick, P. et al. (2012) A timeline for terrestrialization: consequences for the carbon cycle of the Palaeozoic. Philosophical Transactions of the Royal Society, B367, 519–36.

  54. Others have tried their hand at testing the early origin of land plants by crunching the DNA, dating the event to being close to the age of the oldest fossil spores (480–471

  million years ago). See Magallón, S., Hilu, K.W. & Quandt, D. (2013) Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany, 100, 556–73.

  55. Rota-Stabelli, O., Daley, A.C. & Pisani, D. (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Current Biology, 23, 392–8. See also the commentary: Dunn, C.W. (2013) Evolution: out of the ocean. Current Biology, 23, R241. Lozano-Fernandez, J. et al. (2016) A molecular palaeobiological exploration of arthropod terrestrialization. Philosophical Transactions of the Royal Society, B371, 20150133.

  56. Strother, P. et al. (2011) Earth’s earliest non-marine eukaryotes. Nature, 473, 505–9.

  57. Controversial claims have been made that a distinctive geochemical signature in 850

  million-year-old carbonate rocks lacked an obvious link to any sort of geological event. Instead, the explanation might be the activities of a photosynthetic terrestrial biosphere made up of algae, proto-land plants, and fungi; see Knauth, L.P. & Kennedy, M.J. (2009) The late Precambrian greening of the Earth. Nature, 460, 728–32. For some issues with interpretation, see Arthur, M.A. (2009) Carbonate rocks deconstructed.

  Nature, 460, 698–9.

  58. Berner, R.A. (2004) The Phanerozoic Carbon Cycle: CO and O . Oxford University Press, 2

  2

  New York.

  59. Kenrick, P. & Crane, P.R. (1997) The origin and early evolution of plants on land. Nature, 389, 33–9.

  60. Matsunaga, K.K.S. & Tomescu, A.M.F. (2016) Root evolution at the base of the lycophyte clade: insights from an Early Devonian lycophyte. Annals of Botany, 117, 585–98.

  61. DiMichele, W.A. & Phillips, T.L. (2002) The ecology of Paleozoic ferns. Review of Palaeobotany and Palynology, 119, 143–59.

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  62. Delwiche & Timme (2011).

  63. As discussed in relation to the oxygen-rich atmosphere of the time in Beerling, D.J. (2007) The Emerald Planet. How plants changed Earth’s history. Oxford, Oxford University Press.

  64. Nagalingum, N.S. et al. (2011) Recent synchronous radiation of a living fossil. Science, 334, 796–9. See also the accompanying commentary: Renner, S.S. (2011) Living fossil younger than thought. Science, 334, 766–7.

  65. Butler, R.J. et al. (2009) Testing co-evolutionary hypotheses over geological timescales: interactions between Mesozoic non-avian dinosaurs and cycads. Biological Reviews, 84, 73–89.

  66. Herendeen, P.S. et al. (2017) Palaeobotanical redux: revisiting the age of the angiosperms. Nature Plants, 3, doi:10.1038/nplants.2017.15.

  67. Angiosperm Phylogeny Working Group III (2009) An update of the Angiosperm

  Phylogeny Group classification for the orders and families of flowering plants: APG III.

  Botanical Journal of the Linnean Society, 161, 105–21. Chase, M.W. & Reveal, J.L. (2009) A phylogenetic classification of the land plants to accompany APG III. Botanical Journal of the Linnean Society, 161, 122–7.

  68. Around 97% of all living flowering plant species belong to one of these two major classes, but what of the fascinating remainder, the 3% that do not? They form a special group of plants that includes evolutionary lines with archaic features, a number of which arose before the great split between the monocots and the eudicots. Until

  recently, they had been lumped in with the monocots, but DNA evidence and fossils have since corrected the drawing of this part of the evolutionary tree. Probably the best known of these is a small collection of distinctive beautiful plants, the water lilies (Nymphaeales). Water lilies became adapted to a freshwater habitat during Cretaceous times and have remained in that watery milieu ever since. But the first of the surviving lineages to have split from the others is the family Amborellaceae, which consists of a single sickly-looking evergreen shrubby species restricted to the South Pacific Island of New Caledonia called Amborella trichopoda; of which more in Chapter Three. For now we should note Amborella is among the most primitive flowering plants alive today, with simple flowers. This fits together with evidence from one of the earliest flowering plants, a 120 million-year-old fossil plant called Archaefructus, which also has small unprepossessing flowers. So opinion over the past decade has shifted decisively

  towards the view that the original flowers possessed by early flowering plants were smaller and simpler than the exuberant examples we enjoy today. See Sun, G. et al.

  (1998) In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science, 282, 1692–5. Note that subsequent radiometric dates placed Archaefructus in the Cretaceous rather than the Jurassic, see Sun, G. et al. (2002) Archaefructaceae, a new basal angiosperm family. Science, 296, 899–904.

  69. Updike, J. (2007) Extreme dinosaurs. National Geographic, December. http://ngm.

  nationalgeographic.com/print/2007/12/bizarre-dinosaurs/updike-text.

  70. Niklas, K.J. & Kutschera, U. (2010) The evolution of the land plant life cycle. New Phytologist, 185, 27–41.

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  71. Taylor, T.N., Kerp, H. & Hass, H. (2005) Life history biology of early land plants: deciphering the gametophyte phase. Proceedings of the National Academy of Sciences, USA, 102, 5892–7. See also: Kenrick, P. (2017) How land plant life cycles first evolved. Science, 358, 1538–9.

  72. Ligrone, R., Duckett, J.G. & Renzaglia, K.S. (1993) The gametophyte–sporophyte junction in land plants. Advances in Botanical Research, 19, 231–317.

  73. Eisley, L. (1958) The Immense Journey. Lowe and Brydone, London.

  74. Most researchers would accept that flowering plants evolved from wind-pollinated gymnosperm ancestors, but the nature of the fossil evidence makes it hard to offer definitive claims. For a discussion on the difficulties, see Friis, E.M., Crane, P.R. & Pedersen, K.R. (2011) Early Flowers and Angiosperm Evolution. Cambridge University Press, Cambridge.

  75. We should be careful not to fall into the trap of imagining wind-pollination as a primitive condition. About 10% of today’s flowering plant species rely on wind

  pollination, including those of grasslands and saltmarshes. As a method of reproduction, it evolved at least 65 separate times from animal-pollinated ancestor plant groups, raising the question: if it is such a wasteful mode of reproduction why has it evolved repeatedly in this manner? One answer seems to be that it evolves when animals

  become unreliable agents of pollen transfer; in this context wind pollination provides the reproductive assurance needed for setting seed. For discussion of these issues, see Barrett, S.C.H. (2010) Understanding plant reproductive diversity. Philosophical Transactions of the Royal Society, B365, 99–109.

  76. These twin reproductive advantages follow from the
process of double fertilization, a major contributing factor to the success of the angiosperms. Double fertilization takes place when a pollen grain extends into the flower, conveying two non-motile sperm cells to the ovule. One fertilizes the egg located inside the ovule, and the other initiates sexually formed embryo-nourishing tissue called endosperm. Cut open a maize seed

  and inside you’ll find a visible illustration of the products of double fertilization.

  Pressed to one side is the plant embryo, the result of the first fertilization event, and surrounding it is the endosperm, a smooth substance filling the rest of the kernel, the product of the second fertilization event. Gymnosperm seeds enjoy no such benefits: only one of the two sperm cells conveyed by the pollen tube fertilizes the egg; the other degenerates. In a recent twist, William Friedman of Harvard University has

  shown that the gnetophytes have a rudimentary form of double fertilization that produces extra embryos. As we have already seen, gnetophytes ( Ephedra, Gnetum, and Welwitschia) are gymnosperms closely related to flowering plants. It is easy to fall into the trap of thinking Friedman’s findings suggest double fertilization already existed in some form in the common ancestor of flowering plants, but the molecular tree of life indicates this wasn’t the case. The gnetophytes independently arrived at this innovative aspect of plant reproductive biology. For a review with historical context, see Friedman, W.E. (1998) The evolution of double fertilization and endosperm: an ‘historical’ perspective. Sexual Plant Reproduction, 11, 6–16.

  77. Herendeen et al. (2017).

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  78. Cardinal, S. & Danforth, B.N. (2013) Bees diversified in the age of eudicots. Proceedings of the Royal Society, B280, 20122686. Epiphytes, living on trunks and branches of trees, also seized the opportunities created by flowering plants, deriving moisture and nutrients from the rain and decomposing debris accumulating around them. Only DNA

  can tell us the story of epiphyte diversification, for these plants are rarely fossilized, and the spores they leave behind are often plain and unornamented, preserving no