Making Eden

by David Beerling

  5. Bateman et al. (1998).

  6. See the following two helpful reviews. Dolan, L. (2009) Body building on land—

  morphological evolution of land plants. Current Opinion in Plant Biology, 12 , 4–8. Pires, N.D. & Dolan, L. (2012) Morphological evolution in land plants: new designs with old genes. Philosophical Transactions of the Royal Society, B367, 508–18.

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  7. Some are re-interpreting the fossil evidence to suggest miniature early vascular plants like Cooksonia were not hardy pioneers of the terrestrial landscape with adaptations later successfully exploited by vascular plants: see Boyce, C.K. (2008) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in vascular land plants. Paleobiology, 34, 174–94. Instead, Boyce (2008) suggests Cooksonia plants are simply structures for efficiently dispersing spores from miniature torpedo-shaped sacs at the tips of the stems. In this view, they are regarded as dependent—parasitic—upon that parental plant for nutrients and

  water, in an analogous manner to the sporophytes of mosses discussed in Chapter

  Two. Such arguments rest on size constraints. The very narrow axis diameters of

  some fossils—less than a millimetre—may be too small to house sufficient photo-

  synthetic tissue to allow the plant to be free-living. Perhaps it was nourished by an unpreserved parental plant? Stimulating though these ideas are, they overlook the crucial benefit to photosynthesis and growth of very small plants of an atmosphere rich in carbon dioxide, with levels containing 10 or even 20 times as much as today’s atmosphere.

  8. Hetherington, A.J., Berry, C.M. & Dolan, L. (2016) Networks of highly branched stig-marian rootlets developed on the first giant trees. Proceedings of the National Academy of Sciences, USA, 113, 6695–700.

  9. I have previously discussed at length the argument that falling atmospheric carbon dioxide levels through the Devonian relieved an environmental constraint on the evolutionary origins and spread of flat-bladed (megaphyll) leaves. It is an example of how feedbacks between the slow geochemical cycling of carbon and plant activities constrained the evolution of plant form. See Beerling, D.J. (2007) The Emerald Planet: How Plants Changed Earth ’s History. Oxford University Press, Oxford.

  10. Hao, S.G., Beck, C.B. & Wang, D.M. (2003) Structure of the earliest leaves: adaptations to high concentrations of atmospheric CO . International Journal of Plant Sciences, 164, 2

  71–5.

  11. Boyce, C.K. & Knoll, A.H. (2002) Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology, 28, 70–100.

  Boyce, C.K. (2010) The evolution of plant development in a palaeontological context.

  Current Opinion in Plant Biology, 13, 102–7.

  12. At least for seed-plant lineages we already have candidate gene families explaining the common evolutionary trajectories generating the diversity of leaf shapes: see Nardmann, J. & Werr, W. (2013) Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches.

  New Phytologist, 199, 1081–92.

  13. Weigel, D. & Jurgens, G. (2002) Stem cells that make stems. Nature, 415, 751–4.

  14. Sarkar, A.K. et al. (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature, 446 , 811–14.

  15. See Weigel & Jurgens (2002).

  16. Kempin, S.A., Savidge, B. & Yanofsky, M.F. (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science, 267, 522–5.

  17. See Weigel & Jurgens (2002).

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  18. Vollbrecht, E. et al. (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature, 350, 241–3.

  19. Schneedberger, R. et al. (1998) The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development, 125, 2857–65. Tsiantis, M. et al. (1999) The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science, 284, 154–6.

  20. Harrison, C.J. et al. (2005) Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature, 434, 509–14.

  21. Byrne, M.E. et al. (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature, 408, 967–71.

  22. See Harrison et al. (2005).

  23. Floyd, S.K. & Bowman, J.L. (2007) The ancestral developmental tool kit of land plants.

  International Journal of Plant Science, 168, 1–35. Floyd, S.K. & Bowman, J.L. (2006) Distinct mechanisms reflect the independent origins of leaves in vascular plants. Current Biology, 16, 1911–17. Floyd, S.K. & Bowman, J.L. (2010) Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? Journal of Plant Research, 123, 43–55.

  Zalewski, C.S. et al. (2014) Evolution of the class IV HD-Zip gene family in streptophytes. Molecular Biology and Evolution, 30, 2347–65.

  24. Bower, F.O. (1935) Primitive Land Plants. Macmillan, London.

  25. See Floyd & Bowman (2006) and also the interesting commentary on reconciliation of the differences of interpretation between Harrison et al. (2005) and Floyd & Bowman (2006): Kidner, C.A. (2007) Leaf evolution: working with what ’s to hand. Evolution and Development, 9, 321–2.

  26. Raven, J.A. & Edwards, D. (2001) Roots: evolutionary origins and biogeochemical significance. Journal of Experimental Botany, 52, 381–401. Algeo, T.J. & Scheckler, S.E. (1998) Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes and marine anoxic events. Philosophical Transactions of the Royal Society, B353, 113–30.

  27. Kenrick, P. & Strullu-Derrien, C. (2014) The origin and early evolution of roots. Plant Physiology, 166, 570–80.

  28. Jones, V.A.S. & Dolan, L. (2012) The evolution of root hairs and rhizoids. Annals of Botany, 110, 205–12.

  29. Xue, J. et al. (2016) Belowground rhizomes in paleosols: the hidden half of an early Devonian vascular plant. Proceedings of the National Academy of Sciences, USA, 113, 9451–6.

  30. Kidston, R & Lang, W.H. (1920) On Old Red Sandstone plants showing structure, from the Rhynie Chert bed, Aberdeenshire. Part III Asteroxylon mackiei, Kidston and Lang.

  Transactions of the Royal Society of Edinburgh, 52, 643–88. A recent assessment of where it fits into the modern framework of plant evolution is given in Kenrick, P.R. & Crane, P.R. (1997) The Origin and Early Diversification of Land Plants: A Cladistic Study. Smithsonian Institution Press, Washington, DC.

  31. Hetherington, A.J., Dubrovsky, J.G. & Dolan, L. (2016) Unique cellular organization in the oldest root meristem. Current Biology, 26, 1629–33.

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  32. Dolan, L. (2016) Q & A. Current Biology, 26, R83–101.

  33. Menand, B. et al. (2007) An ancient mechanism controls the development of cells with a rooting function in land plants. Science, 316, 1477–80.

  34. Menand et al. (2007).

  35. Zimmer, A. et al. (2007) Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Molecular Genetics and Genomics, 278, 393–402.

  36. Pires, N.D. et al. (2013) Recruitment and remodelling of an ancient gene regulatory network during land plant evolution. Proceedings of the National Academy of Sciences, USA, 110, 9571–6.

  37. Jang, G. et al. (2011) RSL genes are sufficient for rhizoid system development in early diverging plants. Development, 138, 2273–81.

  38. See Pires et al. (2013).

  39. Lewis, D. (1983) Cyril Dean Darlington. 19 December 1903–26 March 1981. Biographical Memoirs, 29, 113–57.

  40. Harman, O.S. (2004) The Man Who Invented the Chromosome: The Life of Cyril Darlington.

  Harvard University Press, Cambridge, MA.

  41. Willis, A.J. (1994) Arthur Roy Clapham. 24 May 1904–18 December 1990. Biographical Memoirs, 39, 72–90. See also Pigott, D. (1992) Obituary: Arthur
Roy Clapham, CBE, FRS

  (1904–1990). Journal of Ecology, 80, 361–5.

  42. Horton, P. (2012) David Alan Walker. 18 August 1928–13 February 2012. Biographical Memoirs, 60, 413–32.

  43. Proust, H. et al. (2016) RSL class I genes controlled the development of epidermal structures in the common ancestor of land plants. Current Biology, 26, 93–9.

  44. Bowman, J.L. et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell, 171, 287–304.

  45. Puttick, M.N. et al. (2018) The interrelationships of land plants and the nature of the ancestral embryophyte. Current Biology, 28, 1–13.

  46. Bonnot, C. et al. (2017) Functional PTB phosphate transporters are present in streptophyte algae and early diverging land plants. New Phytologist, 214, 1158–71.

  47. Datta, S. et al. (2011) Roots hairs: development, growth and evolution at the plant–soil interface. Plant Soil, 346, 1–14.

  48. Dolan, L. (2017) Root hair development in grasses and cereals (Poaceae). Current Opinion in Genetics and Development, 45, 76–81.

  49. Wingen, H.R. et al. (2016) Mapping of quantitative trait loci for root hair length in wheat identifies loci that co-locate with loci for yield components. Journal of Experimental Botany, 67, 4535–43.

  50. Han, Y. et al. (2016) Altered expression of TaRSL4 gene by genome interplay shapes root hair length in allopolyploid wheat. New Phytologist, 209, 721–32.

  51. See Kenrick, P. (2017) How land plant life cycles first evolved. Science, 358, 1538–9.

  52. Bowman, J.L. et al. (2016) Evolution in the cycles of life. Annual Reviews of Genetics, 50, 133–54.

  53. Master switches controlling such transitions are also involved. See for example, Horst, N.A. et al. (2016) A single homeobox gene triggers phase transition, embryogenesis

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  and asexual reproduction. Nature Plants, 2, article number 15209. See also the commentary: Hasebe, M. (2016) Starting BELL for embryos. Nature Plants, 2, article number 16004.

  54. Sakakibara, K. et al. (2013) KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science, 339, 1067–70. See also the associated commentary article: Friedman, W.E. (2013) One genome, two ontogenies. Science, 339, 1045–6.

  55. Sano, R. et al. (2005) KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not haploid meristems. Evolution and Development, 7, 69–78.

  56. Bowman et al. (2016).

  57. For an accessible introduction into epigenetics, see Carey, N. (2012) Epigenetics: How modern biology is rewriting our understanding of genetics, disease and inheritance. Icon Books, London.

  58. Originally discovered by research on fruit-flies ( Drosophila), PcG may in fact be a universal protein complex present through the plant and animal kingdoms.

  59. Mosquna, A. et al. (2009) Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development, 136, 2433–44.

  60. Okano, Y. et al. (2009) A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proceedings of the National Academy of Sciences, USA, 106, 16321–6.

  61. Okano et al. (2009).

  62. Mosquna et al. (2009).

  63. For a dispatch from the frontline, see also Kenrick, P. (2017) How land plant life cycles first evolved. Science, 358, 1538–9.

  64. Went, F. (1935) Auxin, the plant growth hormone. Botanical Review, 1, 162–82. Not long after this triumph, Went left Utrecht to pursue his interests in plant science in Caltech in Pasadena, California, and went on to become the Director of Missouri Botanic

  Gardens in 1958, a position Peter Raven has held since 1971 (Chapter Eight); the web of such connections between the past and the present that reaches across the history of botanical science and discovery is built from such threads. For an accessible review of Darwin’s work in a modern genomic context, see Holland, J.J. et al. (2009)

  Understanding phototropism: from Darwin to today. Journal of Experimental Botany, 60, 1969–78.

  65. Lau, S., Jurgens, G. & De Smet, I. (2008) The evolving complexity of the auxin pathway.

  Plant Cell, 20, 1738–46. De Smet, I. et al. (2011) Unravelling the evolution of auxin signalling. Plant Physiology, 155, 209–21.

  66. Boot, K.J.M. et al. (2012) Polar auxin transport: an early invention. Journal of Experimental Botany, 63, 4213–18. See also the extended commentary: Raven, J.A. (2013) Polar auxin transport in relation to long-distance transport of nutrients in the Charales. Journal of Experimental Botany, 64, 1–9.

  67. Viaene, T. et al. (2012) Origin and evolution of PIN auxin transporters in the green lineage. Trends in Plant Science, 18, 5–10.

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  68. Viaene, T. et al. (2014) Directional auxin transport mechanisms in early diverging land plants. Current Biology, 24, 1–6.

  69. Sanders, H., Rothwell, G.W. & Wyatt, S.E. (2011) Parallel evolution of auxin regulation in rooting systems. Plant Systematics and Evolution, 291, 221–5.

  70. Yasumura, Y. et al. (2012) Studies of Physcomitrella patens reveal that ethylene-mediated submergence responses arose relatively early in land-plant evolution. The Plant Journal, 72, 947–59.

  71. Ju, C. et al. (2015) Conservation of ethylene as a plant hormone over 450 million years of evolution. Nature Plants, 1, 1–7.

  72. Harholt, J., Moestrup, O. & Ulvskov, P. (2016) Why plants were terrestrial from the beginning. Trends in Plant Science, 21, 96–101.

  73. The unfolding story of Harberd’s discovery of the mechanisms by which DELLA proteins interact with gibberellin (GA) and the GID1 receptor to regulate plant growth is related in his engaging 2006 book Seed to Seed: The Secret Life of Plants (Bloomsbury, London).

  74. Yabuta, T. & Sumiki, Y. (1938) On the crystal of gibberellin, a substance to promote plant growth. Journal of the Agricultural Chemical Society of Japan, 14, 1526.

  75. Stimulation of plant growth by GA can be demonstrated in genetically transformed Arabidopsis plants lacking a gene coding for an enzyme in its biosynthetic pathway.

  Transformed plants are effectively unable to synthesize their own gibberellin and develop a severely stunted appearance. Providing the plants with a source of GA corrects these developmental problems and identifies it as the causal agent responsible.

  76. Navarro, L. et al. (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Current Biology, 18, 650–5.

  77. Three reviews capture the main details and timeline of the discoveries. Hirano, K. et al.

  (2008) GID1-mediated gibberellin signalling in plants. Trends in Plant Science, 13, 192–9.

  Harberd, N.P., Belfield, E. & Yasumura, Y. (2009) The angiosperm gibberellin-GID1-DELLA regulatory mechanism: how an ‘inhibitor of an inhibitor’ enables flexible

  response to fluctuating environments. The Plant Cell, 21, 1328–39. Sun, T. (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signalling module in

  plants. Current Biology, 21, R338–R345.

  78. DELLA is an acronym derived from the five amino acid building blocks that stay the same in all members of the DELLA family of proteins. The five amino acids are aspartic acid (D), glutamic acid (E), leucine (L) (twice), and alanine (A). Amino acids have a one-letter code assigned to them, in a scheme created by pioneering bioinformatician

  Margaret Dayhoff (1925–1983), and are not always labelled by the first letter of their name to avoid repeats of the same letter. Single-letter abbreviations helped Dayhoff keep data-file sizes down in an era of punch-card computing.

  79. Since the late 1950s, the presence of gibberellin has been reported in both seed plants and non-seed plants, including unicellular and multicellular algae, mosses, and ferns.

  Beyond implying great antiquity in the underlying genetic toolkits, nothing much else was known about what was going o
n. Yasumura, Y. et al. (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land plant evolution.

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  Current Biology, 17, 1225–30. See also key research by Hirano, K. et al. (2007) The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moe-llendorfii but not in the bryophyte Physcomitrella patens. The Plant Cell, 19, 3058–79.

  80. Achard, P. et al. (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology, 18, 656–60.

  81. Peng, J. et al. (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature, 400, 256–61. Sasaki, A. et al. (2002) A mutant gibberellin-synthesis gene in rice. Nature, 416, 701–2.

  82. De Robertis, E.M. (2008) Evo-devo: variations on ancestral themes. Cell, 132, 185–95.

  Carroll, S.B. (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell, 134 , 25–36.

  83. Monterio, A. & Podlaha, O. (2009) Wings, horns and butterfly eyespots: how do complex traits evolve? PLoS Biology, 7, 209–16.

  84. He was also writing before we realized that plants do rather better than the fourteenth-century alchemist Nicolas Flamel in postponing mortality. Flamel claimed to have succeeded in solving the twin magical puzzles of turning lead into gold and achieving immortality for his wife and himself. You have to question his conviction of his own immortality, though, when you discover he designed his own tombstone, which can still be found to this day preserved at the Musée de Cluny in Paris, the city where he lived into his 80s.

  85. Schmid-Siegert, E., et al. (2017) Low number of fixed somatic mutations in a long-lived oak tree. Nature Plants, 3, 926–9. See also the commentary: Kuhlemeier, C. (2017) How to get old without aging. Nature Plants, 3, 916–17.

  86. Larkin, P. (2011) Poems. Selected and with an introduction by Martin Amis. Faber and Faber Ltd, London.

  87. See Niklas, K.J. & Kutschera, U. (2009) The evolutionary development of plant body plans. Functional Plant Biology, 36, 682–95.

  5. Gas valves