Making Eden
Page 33
1. Graham, L.E. (1993) Origin of Land Plants. John Wiley and Sons, Inc., New York.
2. Edwards, D., Davies, K. & Axe, L. (1992) A vascular conducting strand in the early land plant Cooksonia. Nature, 357, 683–5.
3. Edwards, D., Kerp, H. & Hass, H. (1998) Stomata in early land plants – an anatomical and ecophysiological approach. Journal of Experimental Botany, 49, 255–78. Edwards, D. (1998) Climate signals in Palaeozoic land plants. Philosophical Transactions of the Royal Society, B353, 141–57.
4. Koch, G.W. et al. (2004) The limits to tree height. Nature, 428, 851–4. See also the accompanying commentary: Woodward, F.I. (2004) Tall storeys. Nature, 428, 807–8.
5. Dawson, T.E. (1998) Fog in the Californian redwood forest: ecosystem inputs and use by plants. Oecologia, 117, 476–85.
6. See Dixon, H.H. & Joly, J. (1895) On the ascent of sap. Philosophical Transactions of the Royal Society, B186, 563–76. The mechanism by which water is raised against gravity to the upper foliage of tall trees puzzled plant physiologists for a long time. For a modern
EndnotEs a 221
perspective on the cohesion theory as an exclusive mechanism of long-distance water transport in plants, see Zimmermann, U. et al. (1994) Xylem water transport: is the available evidence consistent with the cohesion theory? Plant, Cell & Environment, 17, 1169–81.
7. Nutrients synthesized by leaves flow in the opposite direction and in 1930 the German plant physiologist Ernst Münch (1876–1946) proposed an intuitive hypothesis to
explain how. Nutrients should flow from areas with higher concentration (i.e., in the leaves, where sugars are synthesized and added to the system) to areas with lower concentration (i.e., the roots and fruits, where sugars are taken out). The flow of nutrients is passive and involves no expenditure of energy by the plant; an alternative would be a more complicated active system that uses energy to transport the nutrients through the tree. The Münch hypothesis has been described as ‘super simple and super plausible’, and is currently under detailed investigation in hard-to-access cells of tall trees.
8. Quote from Tyree, M.T. (2003) Plant hydraulics: The ascent of water. Nature, 423, 923.
9. Beerling, D.J. (2015) Newton and ascent of water in plants. Nature Plants, 1, 15005.
10. For balance, see also this critique: Tyree, M.T. (1997) The cohesion-tension theory of sap ascent: current controversies. Journal of Experimental Botany, 48, 1753–65.
11. Conover, E. (2015) Gravity-defying trees explained by Newton. Science, February 2 2015.
http://www.sciencemag.org/news/2015/02/gravity-defying-trees-explained-newton
12. Koch et al. (2004).
13. See Dawson (1998).
14. Berry, J.A., Beerling, D.J. & Franks, P.J. (2010) Stomata: key players in the Earth system, past and present. Current Opinion in Plant Biology, 13, 233–40.
15. See Berry et al. (2010).
16. See Berry et al. (2010).
17. Hetherington, A.M. & Woodward, F.I. (2003) The role of stomata in sensing and driving environmental change. Nature, 424, 903–8.
18. Choudhury, B. et al. (1998) A biophysical process-based estimate of global land surface evaporation using satellite and ancillary data—II. Regional and global patterns of seasonal and annual variations. Journal of Hydrology, 205, 186–204.
19. Two papers provide the basis for this thinking. The first is a classic paper on the role of vegetation in influencing climate. It illustrates the role of plants in the current climate system and provides a good basis for speculating about the climate before the
advent of vascular plants. See Shukla, J. & Mintz, Y. (1982) Influence of land-surface evapotranspiration on the earth’s climate. Science, 215, 1498–501. The second is a more recent example of the experiment above with a modern global climate and land surface model. It provides a good discussion of the role of vegetation in climate and how the climate system works. Read this if you want to go deeper than the Shukla and
Mintz paper. Kleidon, A., Fraedrich, K. & Heimann, M. (2000) A green planet versus a desert world: estimating the maximum effect of vegetation on the land surface climate.
Climatic Change, 44, 471–93.
20. Dahl, E. et al. (2010) Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. Proceedings of the National Academy of
222 a EndnotEs
Sciences, USA, 107, 17911–15. Wallace, M.W. et al. (2017) Oxygenation history of the Neoproterozoic to early Phanerozoic and the rise of land plants. Earth and Planetary Science Letters, 466, 12–19.
21. See Dahl et al. (2010). This fascinating idea has generated discussion. Butterfield, N.J. (2011) Was the Devonian radiation of large predatory fish a consequence of rising atmospheric oxygen concentration? Proceedings of the National Academy of Sciences, USA, 108, E28. Dahl, E. et al. (2011) Reply to Butterfield: The Devonian radiation of large predatory fish coincided with elevated atmospheric oxygen levels. Proceedings of the National Academy of Sciences, USA, 108, E29.
22. As discussed by Berry et al. (2010).
23. Sack, F.D. & Chen, J.-G. (2009) Pores in place. Science, 323, 592–3.
24. Personal communication. Reflections on Berry’s scientific career can be found in: Berry, J.A. (2012) There ought to be an equation for that. Annual Reviews in Plant Biology, 63, 1–17.
25. A valuable source of historical information on stomatal research covering anatomy, physiology, and evolution is: Meidner, H. (1987) Three hundred years of research into stomata. In Stomatal Function (eds Zeiger, E., Farquhar, G.D., and Cowan, I.) pp. 7–27.
Stanford University Press, Stanford.
26. Grew, N. (1682) Anatomy of Plants. W. Rawlins, London.
27. Bergmann is a protégé of Chris Somerville, who played a leading role in launching Arabidopsis on unsuspecting plant biologists. Prompted by James Watson, the Nobel Prize-winning co-discoverer of DNA, Somerville drove forward the sequencing of its compact genome. A historical perspective is provided by Somerville, C. & Koornneef, M. (2002) A fortunate choice: the history of Arabidopsis as a model plant. Nature Reviews Genetics, 3, 883–9.
28. A profile of Torii is given in here: Torii, K.U. (2013) Q & A. Current Biology, 23, R943–4.
29. Ohashi-Ito, K. & Bergmann, D.C. (2006) Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell, 18, 2493–505.
30. MacAlister, C.A. et al. (2007) Transcription factor control of asymmetric cell divisions that establish stomatal lineages. Nature, 445, 537–40. Pillitteri, L.J. et al. (2007) Termination of asymmetric cell division and differentiation of stomata. Nature, 445, 501–5.
31. DeSmet, I. & Beeckman, T. (2011) Asymmetric cell division in land plants and algae: the driving force for differentiation. Nature Reviews Molecular Cell Biology, 12, 177–87.
32. They belong to a family of proteins called basic-Helix-Loop-Helix (bHLH) transcription factors. These ancient proteins get their name from the fact that part of the chain of amino acids they code for contains a sequence of roughly 100 amino acids that are chemically attracted to each other in such a way that a characteristic loop forms as the chain folds around on itself. bHLH proteins are ubiquitous in eukaryotic organisms and likely evolved up to a billion years ago, before the divergence of the plant and animal kingdoms. Algal genomes have about five types, whereas the genomes of
land plants, including mosses, lycophytes, and flowering plants, have over a hundred.
EndnotEs a 223
The diversity of bHLH proteins in green plants today appears to be a legacy of events over 400 million years ago when land plants originated and diversified. It is easy to imagine why. Expanding numbers of bHLH proteins could have orchestrated the evolutionary development of specialized cells and tissues required for adaptations to cope with the mounting environmental challenges faced by plants encountering
harsh terrestrial environments (see Pires, N. & Dolan, L. (2009) Origin and diversification o
f basic-helix-loop-helix proteins in plants. Molecular Biology and Evolution, 27, 862–74).
33. MacAlister, C.A. & Bergmann, D.C. (2011) Sequence and function of basic helix-loop-helix proteins required for stomatal development in Arabidopsis are deeply conserved in land plants. Evolution and Development, 13, 182–92.
34. The story is, as always, more complex than this. Mutant lines of Arabidopsis lacking SPCH were not rescued by the moss gene SMF1; for details see MacAlister & Bergmann (2011).
35. Kanaoka, M.M. et al. (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell, 20, 1775–85.
36. Chater, C.C. et al. (2016) Origin and function of stomata in the moss Physcomitrella patens. Nature Plants, 2, doi: 10.1038/nplants.2016.179.
37. Olsen, J. L. et al. (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature, 530, 331–5.
38. Chater, C.C. et al. (2017) Origins and evolution of stomatal development. Plant Physiology, 174, 624–38.
39. MacAlister et al. (2007).
40. Raissig, M.T. et al. (2016) Grasses use an alternatively wired bHLH transcription network to establish stomatal identity. Proceedings of the National Academy of Sciences, USA, 113, 8326–31. Raissig, M.T. et al. (2017) Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science, 355, 1215–18.
41. Chen, Z.H. et al. (2017) Molecular evolution of grass stomata. Trends in Plant Science, 22, 124–39.
42. Franks, P.J. & Farquhar, G.D. (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology, 143, 78–87.
43. Raissig et al. (2017).
44. Hetherington & Woodward (2003).
45. Dow, G.J., Bergmann, D.C. & Berry, J.A. (2014) An integrated model of stomatal development and leaf physiology. New Phytologist, 201, 1218–26. Dow, G.J., Berry, J.A. & Bergmann, D.C. (2014) The physiological importance of developmental mechanisms
that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytologist, 201, 1205–
17. Dow, G.J. & Bergman, D.C. (2014) Patterning and processes: how stomatal development defines physiological potential. Current Opinion in Plant Biology, 21, 67–74.
46. Rychel, A. L., Peterson, K. M. & Torii, K. U. (2010) Plant twitter: ligands under 140
amino acids enforcing stomatal patterning. Journal of Plant Research, 123, 275–80.
47. Details have been reviewed and synthesized in Pillitteri, L.J. & Torri, K.U. (2012) Mechanisms of stomatal development. Annual Review of Plant Biology, 63, 12.1–12.24.
224 a EndnotEs
48. Reviews of these processes are given in: Bergmann, D. C. & Sack, F. (2007) Stomatal development. Annual Review in Plant Biology, 58, 163–81. Rowe, M. H. & Bergmann, D. C. (2010) Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development. Current Opinion in Plant Biology, 13, 548–55.
49. Caine, R.S. et al. (2016) An ancestral stomatal patterning module revealed in the non-vascular land plant Physcomitrella patens. Development, 143, 3306–14.
50. Davies, W.J. & Zhang, J.H. (1991) Root signals and the regulation of growth and development of plants in drying soils. Annual Review of Plant Physiology and Plant Molecular Biology, 42, 55–76.
51. ABA was originally discovered in the 1960s by research groups investigating compounds that control bud dormancy and the shedding (abscission) of leaves and fruits.
It is now recognized as an important hormone regulating many of the developmental and metabolic responses plants deploy when threatened by environmental dangers
like a drying soil.
52. Root-to-shoot chemical communication of changes in water availability is of great commercial significance. Since the early 1990s, for example, Australian vineyards have exploited it by adopting a technique in which part of the vine’s root system is allowed to dry while the other part is kept well-watered. Those roots experiencing the drying soil produce ABA signals that cause the stomatal pores on the leaves of the grapevines to partially close, reducing rates of water lost in transpiration. Partial-root-drying, as the technique is known, saves irrigation water and exerts no adverse effects on the quality of the grapes or wine, in some cases improving both. Saving water is important for the Australian viticulture industry as supplies for irrigation are an especially precious resource. Other major wine-making regions of the world, including South
America, South Africa, California, and Southern Europe, are now trialling this promising approach to water conservation. A review in this area is given by Davies, W.J., Wilkinson, S. & Loveys, B. (2002) Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytologist, 153, 449–60.
53. Garner, D.L.B. & Paolillo, D.J.J. (1973) On the functioning of stomates in Funaria. The Bryologist, 76, 423–7.
54. Chater, C. et al. (2011) Regulatory mechanism controlling stomatal behaviour conserved across 400 million years of land plant evolution. Current Biology, 21, 1025–9.
A commentary on this paper is given by Bowman (2011) Stomata: active portals for
flourishing on land. Current Biology, 21, R540–1.
55. Lind, C. et al. (2015) Stomatal guard cells co-opted ancient ABA-dependent desiccation survival system to regulate stomatal closure. Current Biology, 25, 1–8. See also Cutler, S.R. et al. (2010) Abscisic acid: emergence of a core signalling network. Annual Review of Plant Biology, 61, 651–79.
56. Discovery of OST1 came when Arabidopsis mutants were subjected to a drought and screened with thermal imaging. Those plants with abnormally open stomata had
cooler leaves than those without: see Mustilli, A.C. et al. (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts
EndnotEs a 225
upstream of reactive oxygen species production. Plant Cell, 14, 3089–99. This screening technique would have appealed to Francis Darwin, who was captivated by the movement of guard cells over a century ago and a pioneer of a branch of botany called stomatal physiology, suitably encouraged and supported in his research at Cambridge
University by A.C. Seward, whom we met in Chapter One. He recognized as early as
1904 that the transpirational flow of water through stomata cools plants, much as sweating cools our skin. Darwin, F. (1898) IX. Observations on stomata. Philosophical Transactions of the Royal Society, B190, 531–621.
57. Lind et al. (2015).
58. Julian Schroeder at the University of San Diego, and colleagues, published a colour heat map showing the similarity of all proteins involved in ABA perception,
metabolism, and signalling in green plant functions relative to Arabidopsis (Hauser F., Waadt, R. & Schroeder, J.I. (2011) Evolution of abscisic acid synthesis and signalling mechanisms . Current Biology, 21, R346–55). A similar exercise is performed here but with a greater emphasis on stomatal functioning: Cai, S. et al. (2017) Evolutionary conservation of ABA signaling for stomatal closure. Plant Physiology, 174, 732–47.
59. Earlier suggestions that the ABA response evolved in lineages that evolved into ferns have proved unfounded and not stood the test of time. Brodribb, T.J. & McAdam, S.A.M. (2011) Passive origins of stomatal control in vascular plants. Science, 331, 582–5.
McAdam, S.A.M. & Brodribb, T.J. (2012) Fern and lycophyte guard cells do not respond to endogenous abscisic acid. The Plant Cell, 24, 1510–21.
60. Investigations with the lycophyte Selaginella confirmed ABA induces a dose-dependent closure of stomata response. Selaginella employs a version of OST1 that is closely related to that found in Physcomitrella; when substituted into Arabidopsis mutants lacking their own copy, it rescues their normal ABA-induced stomatal closing response. See
Ruszala, E. et al. (2011) Land plants acquired active stomatal control early in their evolutionary history. Current Biology, 21, 1030–5. Ferns also
show an ABA stomatal closure response, see Cai et al. (2017) and also Hõrak, H., Kollist, H. & Merilo, E. (2017) Fern stomatal responses to ABA and CO depend on species and growth conditions. Plant 2
Physiology, 174, 672–9.
61. Merced, A. & Renzaglia, K. (2014) Developmental changes in guard cell wall structure and pectin composition in the moss Funaria: implications for function and evolution of stomata. Annals of Botany, 114, 1001–10.
62. Haig, D. (2013) Filial mistletoes: the functional morphology of moss sporophytes.
Annals of Botany, 111, 337–45.
63. Merced, A. & Renzaglia, K.S. (2013) Moss stomata in highly elaborated Oedipodium (Oedipodiaceae) and highly reduced Ephemerum (Pottiaceae) sporophytes are remarkably similar. American Journal of Botany, 100, 2318–27.
64. See Chater et al. (2016).
65. See Keeley, J.E., Osmond, C.B. & Raven, J.A. (1984) Stylites, a vascular land plant without stomata, absorbs CO via its roots. Nature, 310, 694–5.
2
66. Beer, C. et al. (2010) Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science, 329, 834–8.
226 a EndnotEs
67. McKown, A.D., Cochard, H. & Sack, L. (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution.
American Naturalist, 175, 447–60.
68. Beerling, D.J. & Franks, P.J. (2010) The hidden cost of transpiration. Nature, 464, 495–6.
69. Franks, P.J. & Beerling, D.J. (2009) Maximum leaf conductance driven by atmospheric CO effects on stomatal size and density over geologic time. Proceedings of the National 2
Academy of Sciences, USA, 106, 10343–7.
70. Brodribb, T.J. et al. (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist, 165, 839–46. Sack, L. & Holbrook, N.M. (2006) Leaf Hydraulics. Annual Review of Plant Physiology and Molecular Biology, 57, 361–81.
71. For further discussion see also Brodribb, T.J. & Feild, T.S. (2009) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters, 13, 175–83.