Making Eden
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72. Field, T.S. et al. (2011) Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences, USA, 108, 8363–6.
73. Betts, R.A. (1999) Self-beneficial effects of vegetation on climate in an ocean-atmosphere general circulation model. Geophysical Research Letters, 26, 1457–60.
74. Boyce, C.K. & Lee, J-E. (2010) An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity. Proceedings of the Royal Society, B277, 3437–43.
75. Spracklen, D.V., Arnold, S.R. & Taylor, C.M. (2012) Observations of increased tropical rainfall preceded by the passage of air currents. Nature, 489, 282–5. See also the commentary by Arago, L.E.O.C. (2012) The rainforest’s water pump. Nature, 489, 217–18.
76. Further details of Heath’s career are given in Mansfield, T.A. (1998) Oscar Victor Sayer Heath, 26 July 1903–16 June 1997. Biographical Memoirs of Fellows of the Royal Society, 44, 219–35.
77. Heath, O.V.S. (1948) Control of stomatal movement by a reduction in the normal [CO ]
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of the air. Nature, 161, 179–81. Heath, O.V.S. & Russell, J. (1954) An investigation of the light responses of wheat stomata with the attempted elimination of control by the mesophyll. Journal of Experimental Botany, 5, 1–15.
78. Keenan, T.F. et al. (2013) Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature, 499, 324–7.
79. Mansfield’s obituary of O.V.S. Heath was written for The Independent newspaper (June 24, 1997).
80. Franks, P.J. et al. (2017) Stomatal function across temporal and spatial scales: deep-time trends, land-atmosphere coupling and global models. Plant Physiology, 174, 583–602.
81. Sellers, P.J. et al. (1996) Comparison of radiative and physiological effects of doubled atmospheric CO on climate. Science, 271, 1402–6. A more recent analysis broadly con-2
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82. The mammalian version was reported by Chandrashekar, J. et al. (2009) The taste of carbonation. Science, 326, 443–5. The plant version was reported by Hu, H. et al. (2010) Carbonic anhydrases are upstream regulators of CO -controlled stomatal movements
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in guard cells. Nature Structural Biology, 12, 87–93. An excellent commentary drawing these two accounts together is provided by Frommer, W.B. (2010) CO mmon sense.
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83. See Hu et al. (2010).
84. Woodward, F.I. (1987) Stomatal numbers are sensitive to increases in CO from prein-2
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85. The earliest reliable observations of atmospheric CO were probably made on the 2
coast of France from 1871 to 1880, see From, E. & Keeling, C.D. (1986) Reassessment of late 19th century atmospheric carbon dioxide variations in the air of western Europe and the British Isles based on an unpublished analysis of contemporary air masses by G. S. Callendar. Tellus, 38B, 87–105.
86. Engineer, C.B. et al. (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO control of stomatal development. Nature, 513, 246–50.
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87. Gedney, N. et al. (2006) Detection of a direct carbon dioxide effect in continental river runoff records. Nature, 439, 835–38.
88. Monteith, J.L. (1976) Closing remarks. Philosophical Transactions of the Royal Society, B273, 611–13.
89. Beerling, D.J. (2015) Gas valves, forests and global change: a commentary on Jarvis (1976) ‘The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field’. Philosophical Transactions of the Royal Society, B370, 20140311.
6. Ancestral alliances
1. Mackie, W. (1914) The rock series of Craigbed and Ord Hill, Rhynie, Aberdeenshire.
Transactions of the Edinburgh Geological Society, 10, 205–36.
2. In plural, lagerstätten. Lagerstätten have been discovered scattered across the globe and throughout the geological column, and collectively span a billion years of the history of life on Earth. The Burgess Shale lagerstätte in the Canadian Rocky Mountains dates to the early Cambrian, 505 million years ago, and ranks as one of the most
famous for having yielded enormous insights into the sudden appearance of a wide
diversity of complex animal life in the oceans.
3. See Edwards, D., Kenrick, P. & Dolan, L. (2018) History and contemporary significance of the Rhynie cherts – our earliest preserved terrestrial ecosystem. Philosophical Transactions of the Royal Society, B373, 20160489.
4. Mackie later had his ‘if only’ moment when realizing that the discovery of what is one of the most extraordinary sites of Devonian life yet unearthed could have been made 35 years earlier. If only he had followed up his chance discovery of fossil plant-bearing chert in the same region back in 1880. Historical details of the site’s discovery are given in: Trewin, N.H. (2004) History of research on the geology and palaeontology of the
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Rhynie area, Aberdeenshire, Scotland. Transactions of the Royal Society of Edinburgh: Earth Sciences, 94, 285–98.
5. Kidston, R. & Lang, W.H. (1921) On Old Red Sandstone plants showing structure, from the Rhynie chert bed, Aberdeenshire. Part V. The thallophyta occurring in the peat-bed; the succession of the plants through a vertical section of the bed, and the conditions of accumulation and preservation of the deposits. Transactions of the Royal Society of Edinburgh, 52, 855–902.
6. Thomson, C.A. & Wilkinson, I.P. (2009) Robert Kidston (1852–1924): biography of a Scottish geologist. Scottish Journal of Geology, 45, 161–8. See also Lang, W.H. (1925) Robert Kidston—1852–1924. Proceedings of the Royal Society, B98, 14–22.
7. Pearson, H.L. (2014) Gender-bending in the Devonian at Rhynie and afterwards. The Linnean, 30, 7–10; Pearson, H.L. (2016) Gender-bending in the Devonian at Rhynie: some corrections. The Linnean, 32, 9–10.
8. Remy, W. et al. (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae.
Proceedings of the National Academy of Sciences, USA, 91, 11841–3.
9. Remy et al. (1994).
10. Taylor, T.N., Kerp, H. & Haas, H. (2005) Life history biology of early land plants: deciphering the gametophyte phase. Proceedings of the National Academy of Sciences, USA, 102, 5892–7.
11. Dotzler, N. et al. (2006) Germination shields in Scuellospora (Glomeromycota: Diversisporales, Gigasporacea) from 400 million-year-old Rhynie chert. Mycological Progress, 5, 178–84. Krings, M. et al. (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist, 174, 648–57. See also the commentary by Berbee, M.L. & Taylor, J.W. (2007) Rhynie chert: a window into a lost world of complex plant–fungus interactions. New Phytologist, 174, 475–9.
12. Pirozynski once helped Jane Goodall out at her camp in the Gombe Stream Reserve, East Africa, observing the chimpanzees that were to make her famous. Sitting in the dappled shade cast by the sparse canopies of savanna trees, he established the basis for our current estimates of global fungal biodiversity (Pirozynski, K.A. (1972) Microfungi of Tanzania. Mycological Papers, 129, 1–64). Reasoning that fungal species outnumbered plant species by 3 to 1, possibly even 5 to 1 in the tropics, gave him a conservative estimate in the region of 1.5 million species, similar to the modern figure (Hawksworth, D.L. (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited.
Mycological Research, 105, 1422–32).
13. Pirozynski, K.A. & Malloch, D.W. (1975) The origin of land plants: a matter of mycotropism. Biosystems, 6, 153–64. For the sake of historical accuracy, we should note that these authors, as they acknowledged, were following up on an idea sketched in outline only by Jeffrey, C. (1962) The
origin and differentiation of the Archegoniate land plants. Bot. Not. , 115, 446–54.
14. Ryan, F. (2003) Darwin’s Blind Spot: Evolution beyond Natural Selection. Texere, Thompson Corporation, London. For detailed histories of the ideas related to symbiosis see Sapp, J. (1994) Evolution by Association: A History of Symbiosis. Oxford University Press, New York.
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15. Smith, S.E. & Read, D.J. (2008) Mycorrhizal Symbiosis (3rd edn). Academic Press, London.
16. Tisserant, E. et al. (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences,USA, 110, 20117–22.
17. For a review of reasoning for this date, see Edwards, D., Kenrick, P. & Dolan, L. (2018) History and contemporary significance of the Rhynie cherts – our earliest preserved terrestrial ecosystem. Philosophical Transactions of the Royal Society, B373, 20160489.
18. Zambonelli, A., Iotti, M. & Hall, I. (2015) Current status of truffle cultivation: recent results and future perspectives. Micologia Italiana, 44, 31–40.
19. See Berbee, M.L. et al. (2017) Early diverging fungi: diversity and impact at the dawn of terrestrial life. Annual Review of Microbiology, 71, 41–60. An earlier molecular clock dating attempt is given here: Simon, L. et al. (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature, 363, 67–9.
20. Martin, F., Uroz, S. & Barker, D.G. (2017) Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science, 356, eaad4501.
21. Personal email communication to the author.
22. Margulis, L. (1998) Symbiotic Planet: A New Look at Evolution. Sciencewriters, Amherst, MA, USA.
23. See, for example, Ligrone, R. et al. (2007) Glomeromycotean associations in liverworts: a molecular, cellular and taxonomic analysis. American Journal of Botany, 94, 1756–77.
24. 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.
25. Krings, M. et al. (2007) An alternative mode of early land plant colonization by putative endomycorrhizal fungi. Plant Signalling and Behaviour, 2, 125–6.
26. Note the liverworts possess single-celled rhizoids rather than true roots (Chapter Four), and this means that strictly speaking we cannot refer to their partnership with fungi as forming mycorrhiza. Instead, we should really use the awkward but more technically correct terminology of ‘AM-like’, but I have avoided this clumsy wording in the text.
27. Bowman, J.L. (2016) A brief history of Marchantia from Greece to genomics. Plant and Cell Physiology, 57, 210–29.
28. Humphreys, C.P. et al. (2010) Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nature Communications, 1, 103, doi:10.1038/ncomms1105.
29. Bidartondo, M.I. et al. (2011) The dawn of symbiosis between plants and fungi. Biology Letters, 7, 574–7.
30. Berbee, M.L., James, T.Y. & Strullu-Derrien, C. (2017) Early diverging fungi: diversity and impact at the dawn of terrestrial life. Annual Review of Microbiology, 71, 41–60.
31. Puttick, M.N. et al. (2018) The interrelationships of land plants and the nature of the ancestral embryophyte. Current Biology, 28, 1–13.
32. Carafa, A., Duckett, J.G. & Ligrone, R. (2003) Subterranean gametophyic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi. New Phytologist, 160, 185–97.
33. Duckett, J.G., Carafa, A. & Ligrone, R. (2006) A highly differentiated glomeromycotean association with the mucilage-secreting, primitive antipodean liverwort Treubia (Treubiaceae): clues to the origins of mycorrhizas. American Journal of Botany, 93, 797–813.
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Species of Treubia are copious secretors of mucilage. Production involves glandular structures that swell and rupture to discharge their contents. By absorbing water the mucilage can double in volume.
34. Field, K.J. et al. (2014) First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO . New Phytologist, 205, 743–56.
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35. Field et al. (2014).
36. Wang, B. et al. (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants.
New Phytologist, 186, 514–25. See also the accompanying commentary by Bonfante, P. & Selosse, M.A. (2010) A glimpse into the past of land plants and of their mycorrhizal affairs: from fossils to evo-devo. New Phytologist, 186, 267–70.
37. For a review, see Strullu-Derrien, C. et al. (2018) The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytologist, doi: 10.1111/nph.15076.
38. Strullu-Derrien, C. et al. (2014) Fungal associations in Horneophyton lignieri from the Rhynie Chert (c. 407 million years old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses. New Phytologist, 203, 964–79. For a discussion of symbiotic strategies adopted by land plants during the ‘greening of the land’ see Field, K.J. et al. (2015) Symbiotic options for the conquest of the land. Trends in Ecology and Evolution, 30, 477–486.
39. Wikström, N. & Kenrick, P. (2001) Evolution of the Lycopodiaceae (Lycopsida): estimating divergence times from rbcL gene sequences by use of nonparametric rate
smoothing. Molecular Phylogenetics and Evolution, 19, 177–86.
40. Lang, W.H. (1899) The prothallus of Lycopodium clavatum. Annals of Botany, 13, 279–317.
Lang, W.H. (1902) On the prothalli of Ophioglossum pendulum and Helminthostachys zey-lanica. Annals of Botany, 16, 23–62.
41. Kenrick, P. & Crane, P.R. (1997) The origin and early evolution of plants on land. Nature, 389, 33–9.
42. Leake, J.R. (2005) Plants parasitic on fungi: unearthing the fungi in myco-heterotrophs and debunking the ‘saprotrophic’ plant myth. The Mycologist, 19, 113–22.
43. Read, D.J. et al. (2000) Symbiotic fungal associations in ‘lower’ land plants. Philosophical Transactions of the Royal Society, B355, 815–31.
44. Leake, J.R. (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytologist, 127, 171–216. For an update, see Merckx, V., Bidartondo, M.I. & Hynson, N.A. (2009) Myco-heterotrophy: when fungi host plants. Annals of Botany, 104, 1255–61.
45. Winther, J.L. & Friedman, W.E. (2007) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). American Journal of Botany, 94, 1248–55. Winther, J.L. & Friedman, W.E. (2008) Arbuscular mycorrhizal associations in Lycopodiaceae. New Phytologist, 177, 790–801. Winther, J.L. & Friedman, W.E. (2009) Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum. Journal of Plant Research, 122, 485–96. See also the commentary article drawing all this together by Leake et al. (2008).
46. As discussed by Leake, J.R., Cameron, D.D. & Beerling, D.J. (2008) Fungal fidelity in the myco-heterotroph-to-autotroph life cycle of Lycopodiaceae: a case of parental nurture. New Phytologist, 177, 572–6.
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47. This situation contrasts with the intergenerational transfer of carbon through the
‘atmospheric commons’ as a result of our combustion of fossil fuels, which is likely to have rather different consequences. Not only does it threaten the biodiversity of our land floras, as discussed in Chapter Eight, but it will also influence the climate of future generations not yet born, and who had no say in policies failing to regulate humanity’s carbon emissions.
48. Leake et al. (2008).
49. Russell, A.F. & Hatchwell, B.J. (2001) Experimental evidence for kin-based helping in a cooperatively breeding vertebrate. Proceedings of the Royal Society of London, B268, 2169–74.
50. Cameron, D.D., Leake, J.R. & Read, D.J. (2006) Mutualistic mycorrhiza in orchids: evidence from plant–fungus
carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytologist, 171, 405–16.
51. Quote taken from Burkhardt, F. et al. (2003) The Correspondence of Charles Darwin, Vol. II.
Cambridge University Press, Cambridge. It was recently unearthed and reported in a thorough review of Darwin’s orchid research and its placement in a historical context by Yam, T.W., Arditti, J. & Cameron, K.M. (2009) ‘The orchids have been a splendid sport’ – an alternative look at Charles Darwin’s contribution to orchid biology.
American Journal of Botany, 96, 2128–54.
52. Bernard, N. (1899) Sur la germination du Neottia nidus-avis. Competes Rendus Académie des Sciences, Paris, 128, 1253–5.
53. Kiers, E.T. et al. (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 333, 880–2. See also the commentary: Selosse, M-A. & Rouseet, F. (2011) The plant-fungal market place. Science, 333, 826–9.
54. Note that biologists are not always comfortable bringing economic theory into understanding symbioses between fungi and plants; for a discussion see Smith, F.A. & Smith, S. E. (2015) How harmonious are arbuscular mycorrhizal symbioses? Inconsistent concepts reflect different mindsets as well as results. New Phytologist, 205, 1381–4.
55. Bidartondo, M.I. et al. (2002) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proceedings of the Royal Society, B270, 835–42.
56. Wickett, N.J. et al. (2007) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Molecular Biology and Evolution, 25, 393–401.
57. dePamphilis, C.W. & Palmer, J.D. (1990) Loss of photosynthetic and chlororespiratory genes from the plastic genome of a parasitic flowering plant. Nature, 348, 337–9.
58. Plett, J.M. & Martin, F. (2011) Blurred boundaries: lifestyle lessons from ecomycorrhizal fungal genomes. Trends in Genetics, 27, 14–22.
59. Young, N.D. et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature, 480, 520–4.
60. Wang, B. et al. (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants.