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Making Eden

Page 31

by David Beerling


  trace of their former diversity; see Schneider, H. et al. (2004) Ferns diversified in the shadow of angiosperms. Nature, 428, 553–7.

  79. Stromberg, C.A.E. (2011) Evolution of grasses and grassland ecosystems. Annual Review of Earth and Planetary Sciences, 39, 517–44.

  80. The metabolism of C plants gives them the edge over their C grassy cousins in warm, 4

  3

  open, arid regions, and it is here where they tend to be most common, with a plentiful supply of sunlight powering their energy-demanding photosynthetic way of life. See Edwards, E.J. & Smith S.A. (2010) Phylogenetic analyses reveal the shady history of C 4

  grasses. Proceedings of the National Academy of Sciences, USA, 107, 2532–7.

  81. Edwards, E.J. et al. (2010) The origin of C grasslands: integrating evolutionary and eco-4

  system science. Science, 328, 587–91.

  82. Sage, R.F. et al. (2011) The C plant lineages of planet Earth. Journal of Experimental Botany, 4

  62, 3155–69.

  83. Sage, R.F. (2016) A portrait of the C photosynthetic family on the 50th anniversary of 4

  its discovery: species number, evolutionary lineages, and Hall of Fame. Journal of Experimental Botany, 67, 4039–56.

  84. Spriggs, E.L., Christin, P.-A. & Edwards, E. J. (2014) C photosynthesis promoted spe-4

  cies diversification during the Miocene grassland expansion. PLoS ONE, 9 (5), e97722.

  85. Arakaki, M. et al. (2011) Contemporaneous and recent radiations of the world’s major succulent lineages. Proceedings of the National Academy of Sciences, USA, 108, 8379–84.

  86. Amis, M. (2002) The War Against Cliché. Vintage, London.

  3. Genomes decoded

  1. Miller, W. et al. (2008) Sequencing the nuclear genome of the extinct woolly mammoth. Nature, 456, 387–90.

  2. Green, R. E. et al. (2010) A draft sequence of the Neanderthal genome. Science, 328, 710–22.

  3. Frank, L. (2011) My Beautiful Genome. Exposing Our Genetic Future, One Quirk at a Time. One World, Oxford. Back in the days of the human genome project, whole genome

  sequencing required large teams of scientists and billions of dollars. Subsequent technological and computing advances have made it fast and cheap to sequence and

  analyse genomes. Many individuals have had their genomes sequenced for informa-

  tion regarding heritage as well as to obtain information regarding their likelihood of certain diseases. Before long, we may all have our genome sequences stored on our laptops or smart phones, and personalized approaches to medicine will be the ‘new normal’ for healthcare, Frank points out.

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  4. Hidalgo, O. et al. (2017) Is there an upper limit to genome size? Trends in Plant Science, 7, 567–73.

  5. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796–815.

  6. Rensing, S.A. (2017) Why we need more non-seed plant models. New Phytologist, 216, 355–60.

  7. Derelle, E. et al. (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proceedings of the National Academy of Sciences, USA, 103, 11647–52.

  8. Archibald, J.M. (2006) Genome complexity in a lean, mean photosynthetic machine.

  Proceedings of the National Academy of Sciences, USA, 103, 11433–4.

  9. Worden, A.Z. et al. (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science, 324, 268–72.

  10. The larger genome of Micromonas relative to Ostreococcus includes a richer set of genes for transporting nutrients into the cell across cellular membranes, and for dealing with toxicity caused by heavy metals and reactive oxygen species. A clear advantage of the extended metabolic repertoire of Micromonas is that it copes with a wide range of environmental conditions, and this sees it occupy a global distribution throughout the world’s oceans compared to the more restricted range of Ostreococcus; see Worden et al.

  (2009) above.

  11. See Derelle et al. (2006).

  12. See Derelle et al. (2006).

  13. Merchant, S.S. et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science, 318, 245–51.

  14. Hodges, M.E. et al. (2012) The evolution of land plant cilia. New Phytologist, 195, 526–40.

  15. General review is given in Ainsworth, C. (2007) Tails of the unexpected. Nature, 448, 638–41.

  16. Li, J.B. et al. (2004) Comparative and basal genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell, 117, 541–52.

  17. See Knoll, A.H. (2011) The multiple origins of complex multicellularity. Annual Reviews of Earth and Planetary Science, 39, 217–39.

  18. Kirk, D.L. (1998) Volvox. Molecular and genetic origins of multicellularity and cellular differentiation. Cambridge University Press, Cambridge. See also: Kirk, D.L. (2010) Volvox.

  Current Biology, 14, R599–600.

  19. Multicellular Volvox is a physically larger organism than Chlamydomonas, but even so it is still dwarfed by the record-holding giant unicellular sub-tropical green alga by the name of Acetabularia, which is a whopping 20–40mm in diameter (Mandoli, D.F. (1998) Whatever happened to Acetabularia? Bringing the once classic model system into the age of molecular genetics. International Reviews in Cytology, 182, 1–67).

  20. Prochnik, S. E. et al. (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science, 329, 223–6.

  21. Nishii, I. & Miller, S.M. (2010) Volvox: simple steps to developmental complexity?

  Current Opinion in Plant Biology, 13, 646–53.

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  22. Herron, M.D. et al. (2009) Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences, USA, 106, 3254–8.

  23. Stebbins, G.L. & Hill, G.C.J. (1980) Did multicellular plants invade the land? American Naturalist, 115, 343. Harholt, J., Moestrup, O. & Ulvskov, P. (2016) Why plants were terrestrial from the beginning. Trends in Plant Science, 21, 96–101. de Vries, J. et al. (2016) Streptophyte terrestrialization in light of plastid evolution. Trends in Plant Science, 21, 467–76.

  24. Hori, K. et al. (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications, 5, doi:10.1038/ncomms4978.

  25. Nishiyama, T. et al. (2018) The Chara genome: secondary complexity and implications for plant terrestrialization. Cell, 174(2), 448–64.

  26. Ju, C. et al. (2015) Conservation of ethylene as a plant hormone over 450 million years of evolution. Nature Plants, 1, doi:10.1038/NPLANTS.2014.4.

  27. Timme, R.E. & Delwiche, C.F. (2010) Uncovering the evolutionary origin of plant molecular processes: comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biology, 10, 96.

  28. Buschmann, H. & Zachgo, S. (2016) The evolution of cell division: from Streptophyte algae to land plants. Trends in Plant Science, 21, 872–83.

  29. Rensing, S.A. et al. (2008) The Physcomitrella genome reveals evolutionary insights in the conquest of land by plants. Science, 319, 64–9.

  30. Bowman, J.L. et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell, 171, 287–304. See also the commentary: Delwiche, C.F., Goodman, C.A. & Chang, C. (2017) Land plant model systems branch out. Cell, 171, 265–6.

  31. Chang, C., Bowman, J.L. & Meyerowitz, E.M. (2016) Field guide to plant model systems.

  Cell, 167, 325–39.

  32. Banks, J.A. et al. (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular land plants. Science, 332, 960–2. For the evolutionary history of Selaginella, see Banks, J.A. (2009) Selaginella and 400 million years of separation.

  Annual Reviews of Plant Biology, 60, 223–38.

  33. Banks et al. (2011).


  34. Chang, C., Bowman, J.L. & Meyerowitz, E. Field guide to plant model systems. Cell, 167, 325–30.

  35. Xu, B. et al. (2014) Contribution of NAC transcription factors to plant adaption to land.

  Science, 343, 1505–8.

  36. Robinson, J.M. (1990) Lignin, land plants, and fungi: biological evolution affecting Phanerozoic oxygen balance. Geology, 18, 607–10.

  37. Floudas, D. et al. (2012) Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science, 336, 1715–19. See also the commentary by Hittinger, C.T. (2012) Endless rots most beautiful. Science, 336, 1649–50.

  38. Hibbett, D. et al. (2016) Climate, decay, and the death of coal forests. Current Biology, 26, R563–7.

  39. Nelson, M.P. et al. (2016) Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proceedings of the National Academy of Sciences, USA, 113, 2442–7.

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  Nevertheless, whatever the dating for white rot fungi, their arrival on the evolutionary stage must have changed the rates of terrestrial carbon cycle processes.

  40. Weng, J.K. & Chapple, C. (2010) The origin and synthesis of lignin. New Phytologist, 187, 273–85.

  41. Niklas, K.J., Cobb, E.D. & Matas, J. (2017) The evolution of hydrophobic cell wall biopolymers: from algae to angiosperms. Journal of Experimental Botany, 68, 5261–9.

  42. Renault, H. et al. (2017) A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nature Communications, 8, doi:10.1038/ncomms14713.

  43. See discussion in Weng & Chapple (2010).

  44. Emiliani, G. et al. (2009) A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biology Direct, 4, 7.

  45. The current paradigm we have been rehearsing invokes lignin evolution in green plants as providing stems with mechanical rigidity for allowing shoots to grow upright.

  But very low levels of lignin were discovered in the cell walls of an intertidal red alga.

  We have already seen that red algae and vascular plants diverged over a billion years ago. One possibility is that the origin of the genes for lignin synthesis considerably pre-dated the origin of land plants. Another explanation is this represents another example of convergent evolution. Both may be a bit of a stretch. See Martone, P.T. et al.

  (2009) Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Current Biology, 19, 169–75.

  46. Weng, J.K. et al. (2008) Independent origins of syringyl lignin in vascular plants.

  Proceedings of the National Academy of Sciences, USA, 105, 7887–92.

  47. A comprehensive treatment of the topic is given in: Conway Morris, S. (2003) Life’s solution: Inevitable Humans in a Lonely Universe. Cambridge University Press, Cambridge.

  48. Melzer, S. et al. (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics, 40, 1489–92.

  49. Kim, S.C. et al. (1996) A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiations. Proceedings of the National Academy of Sciences, USA, 93, 7743–8.

  50. St Helena is one of the most desolate places on Earth. Lying 1200 miles south of the West African coast in the middle of the vast South Atlantic, it originally formed over a period of 7 million years about 14 million years ago. Eastwood, A., Gibby, M. & Cronk, Q.C.B. (2004) Evolution of St Helena arborescent Astereae (Asteraceae): relationships of the genera Commidendrum and Melanodendron. Botanical Journal of the Linnean Society, 144, 69–83.

  51. Crowther, T.W. et al. (2015) Mapping tree density at the global scale. Nature, 525, 201–5.

  52. Tuskan, G.A. et al. (2006) The genome of black cottonwood, Populus tricharpa (Torr. & Gray). Science, 313, 1596–1604.

  53. Myburg, A.A. et al. (2014) The genome of Eucalyptus grandis. Nature, 510, 356–62.

  54. See, for example, Lang, D. et al. (2010) Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biology and Evolution, 2, 488–503. Wilhelmsson, P.K.I. et al. (2017) Comprehensive genome-wide classification reveals that many plant-specific transcription factors evolved in streptophyte algae. Genome Biology and Evolution, 9, 3384–97.

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  55. Soltis, D.E., Visger, C.J. & Soltis, P.S. (2014) The polyploidy revolution then . . . and now: Stebbins revisited. American Journal of Botany, 101, 1057–78.

  56. Van de Peer, Y., Mizrachi, E. & Marchal, K. (2017) The evolutionary significance of polyploidy. Nature Reviews Genetics, 18, 411–24.

  57. Van de Peer, Y. (2004) Computational approaches to unveiling ancient genome duplications. Nature Reviews Genetics, 5, 752–63.

  58. Rensing, S.A. (2014) Gene duplication as a driver of plant morphogenetic evolution.

  Current Opinion in Plant Biology, 17, 43–8.

  59. Maere, S. et al. (2005) Modeling gene and genome duplications in eukaryotes.

  Proceedings of the National Academy of Sciences, USA, 102, 5454–9.

  60. Ibarra-Laclette, E. et al. (2013) Architecture and evolution of a minute plant genome.

  Nature, 498, 94–8.

  61. Guan, R. et al. (2016) Draft genome of the living fossil Ginkgo biloba. GigaScience, 5, doi: 10.1186/s13742-016-0154-1.

  62. Jiao, Y. et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature, 473, 97–100. See also the commentary by Van de Peer, Y. (2011) A mystery unveiled. Genome Biology, 12, 113. Further evidence of ancient whole genome duplications in conifers is reported here: Li, Z. et al. (2015) Early genome duplications in conifers and other seed plants. Science Advances, 1, e1501084.

  63. Ruprecht, C. et al. (2017) Revisiting ancestral polyploidy in plants. Science Advances, 3, e1603195.

  64. Coen, E.S. & Meyerowitz, E.M. (1991) The war of the whorls: genetic interactions controlling flower development. Nature, 353, 31–7.

  65. For reviews, see Soltis, P.S. & Soltis, D.E. (2016) Ancient WGD events as drivers of key innovations in angiosperms. Current Opinion on Plant Biology, 30, 159–65. Chanderbali, A.S. et al. (2016) Evolving ideas on the origin and evolution of flowers in the genomic era. Genetics, 202, 1255–65.

  66. Sanders, M.R. & Bowman, J.L. (2016) Genetic Analysis: An Integrated Approach. Global Edition. Pearson Education Limited, England.

  67. Friis, E.M. et al. (2006) Cretaceous angiosperm flowers: innovations and evolution in plant reproduction. Palaeogeography, Palaeoecology, Palaeoclimatology, 232, 251–93. See also: Herendeen, P.S. et al. (2017) Palaeobotanical redux: revisiting the age of the angiosperms. Nature Plants, 3, doi: 10.1038/nplants.2017.15.

  68. Van de Peer, Y. et al. (2009) The evolutionary significance of ancient genome duplications. Nature Reviews Genetics, 10, 725–32.

  69. Tank, D.C. et al. (2015) Progressive radiations and the pulse of angiosperm diversification. New Phytologist, 207, 454–67.

  70. Jao, Y. et al. (2014) Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots. Plant Cell, 26, 2792–802.

  71. Estep, M.C. et al. (2014) Allopolyploidy, diversification, and the Miocene grassland expansion. Proceedings of the National Academy of Sciences, USA, 111, 15149–54.

  72. Salse, J. et al. (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell, 20, 11–24.

  See also Eckardt, N.A. (2008) Grass genome evolution. Plant Cell, 20, 3–4.

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  73. See Haberer, G. et al. (2016) The big five of the monocot genomes. Current Opinion in Plant Biology, 30, 33–40.

  74. Edger, P.P. et al. (2015) The butterfly plant arms-race escalated by gene and genome duplications. Proceedings of the National Academy of Sciences, USA, 112, 8362–6.

  75. Ehrlich, P. & Raven, P.H. (1964) Butterflies and plants: a study in coevo
lution. Evolution, 18, 586–608.

  76. Ohno, S. (1970) Evolution by Gene Duplication. Springer-Verlag, New York.

  77. Dehal, P. & Boore, J. L. (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology, 3, e314.

  78. Van de Peer et al. (2009).

  79. Zhou, X. et al. (2010) Phylogenetic detection of numerous gene duplications shared by animals, fungi and plants. Genome Biology, 11, R38.

  80. Beutler, E. (2002) Susumu Ohno 1928–2000. Biographical Memoirs, National Academy of Sciences, 81, 1–13.

  81. Fawcett, J.A. et al. (2009) Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event. Proceedings of the National Academy of Sciences, USA, 106, 5737–42. See also the commentary by Soltis, D.E. & Burleigh, J.G. (2009) Surviving the K-T mass extinction: new perspectives of poly-ploidization in angiosperms. Proceedings of the National Academy of Sciences, USA, 106, 5455–6.

  82. Vanneste, K. et al. (2014) Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary. Genome Research, 24, 1334–47. An update is provided by Lohaus, R. & Van de Peer, Y. (2016) Of dups and dinos: evolution at the K/Pg boundary. Current Opinion in Plant Biology, 30, 62–9.

  83. See Li et al. (2015).

  84. As set out in my earlier book: Beerling, D.J. (2007) The Emerald Planet. How Plants Changed Earth’s History. Oxford University Press, Oxford.

  4. Ancient genes, new plants

  1. Carpenter, H. (2000) J.R.R. Tolkien: A Biography. Houghton Mifflin, London.

  2. Miller, A.J. et al. (2015) Expanding the role of botanical gardens in the future of food.

  Nature Plants, 1, http://dx.doi.org/10.1038/nplants.2015.78

  3. Kenrick, P. & Crane, P.R. (1997) The origin and early evolution of plants on land. Nature, 389, 33–9; Bateman, R.M. et al. (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annual Reviews in Ecology and Systematics, 29 , 263–92.

  4. See Kenrick, P. & Davis, P. (2004) Fossil Plants. The Natural History Museum, London.

 

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