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Keywords:

  • atmosphere;
  • biodiversity;
  • colonization;
  • evolution;
  • fossil plants;
  • mycorrhizal symbiosis;
  • nitrogen-fixing symbiosis;
  • phylogenetic models

25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010

  1. Top of page
  2. 25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010
  3. How can we be sure of the exact date of land-plant arrival?
  4. How did plants equip themselves for survival on land?
  5. The big picture: interplay between land plants, geology, the atmosphere and ecosystems
  6. What does the future hold?
  7. References

The huge diversity of land plants we see on earth today underpins our atmosphere, our environment and our society. But how and when did they get here, and what will happen to them, and to us, in the future?

The 25th New Phytologist/Colston Research Symposium ‘Colonization of the terrestrial environment’ (http://www.newphytologist.org/colonization/default.htm) brought together scientists from diverse backgrounds – geology, atmospheric science, palaeobotany, plant physiology, molecular, genetic and evo-devo – to discuss this key event in Earth’s history.

‘...land plants (otherwise known as “land survival devices for cyanobacteria”!) could not have evolved without interplay between organisms (bacteria and algae), rocks and the atmosphere.’

Plants made the transition from water to land just under half a billion years ago (Fig. 1a). Land plants (Embryophytes) form a monophyletic group of multicellular green organisms; their sister group is the Charophycean green algae, composed of freshwater and terrestrial unicellular and multicellular algae. Together, the Embryophytes and the Charophyte algae constitute the Streptophyte clade. The Streptophytes are, in turn, a sister group to the Chlorophytes, an algal lineage comprising unicellular and multicellular/complex forms, which are found in freshwater, marine and terrestrial environments (Lewis & McCourt, 2004).

image

Figure 1.  Timescales and concepts. (a) Geological time from 4600 million years ago (Ma) to the present (0 Ma). The six periods of the Paleozoic era are Cambrian–Permian (543–248 Ma). Key innovations in plant evolution are depicted: 1, oldest discovered filamentous red algae (c. 2100 Ma); 2, first land-plant (liverwort) evolution (c. 470 Ma); 3, Cooksonia fossils (c. 425 Ma); 4, evolution of deep-rooting structures in the Devonian; 5, evolution of flowering plants. (b) Interplay among land plants, geology and the atmosphere.

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How can we be sure of the exact date of land-plant arrival?

  1. Top of page
  2. 25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010
  3. How can we be sure of the exact date of land-plant arrival?
  4. How did plants equip themselves for survival on land?
  5. The big picture: interplay between land plants, geology, the atmosphere and ecosystems
  6. What does the future hold?
  7. References

The fossil record pinpoints the mid-Ordovician period (472–461 million yr ago (Ma)) for the earliest appearance of land plants (Fig. 1a). Multicellular fossil plants of the genus Cooksonia have been identified in Silurian rocks (c. 425 million years (Myr) old; Fig. 1a). However, putative cryptospores from the first land plants have recently been discovered in Ordovician rocks up to 470 Myr old (Rubinstein et al., 2010; Wellman, 2010; Fig. 1a), a key finding that was even reported by the British Broadcasting Corporation (BBC) (Walker, 2010). Molecular phylogenetics using gene sequences from extant land plants has also been used to estimate land-plant evolution. Such models have suggested a range of dates for land-plant emergence, which do not always tie in with the fossil record (e.g. Zimmer et al., 2007 suggest a moss/seed plant split 496 Ma, in the early Ordovician). How can we reconcile these differences? A combination of increased fossil data and new phylogenetic models based on larger amounts of genomic data are likely to be the key.

An apparent gap in the fossil record was highlighted, possibly resulting from soft tissues not fossilizing well compared with spores. For this reason, the fossil record of early bryophyte species is limited to spore material. Fossils from the Devonian era delivered more elaborate structures, such as vasculature, leaf venation patterns and stomata, and identified early plant–insect interactions (Paul Kenrick, The Natural History Museum, UK; Kevin Boyce, University of Chicago, IL, USA; Conrad Labandeira, National Museum of Natural History, Smithsonian Institution, DC, USA). One organism that engendered much debate was Cooksonia, represented in fossil records worldwide. It is depicted as a branched, stick-like, leafless land plant with some spore-dispersal mechanisms that resemble those of Bryophytes. It was argued that Cooksonia may have been too small to fulfil all the functions of vascular land plants –‘In fact, was it even photosynthetic at all?’ (Kevin Boyce, University of Chicago, IL, USA).

Access to sequenced genomes of plant species representative of different evolutionary grades will greatly improve our understanding of the most formative episodes of plant phylogeny. Ralph Quatrano (Washington University, MO, USA) and Jody Banks (Purdue University, IN, USA) introduced Physcomitrella patens (a bryophyte) and Selaginella moellendorfii (a lycophyte), respectively, for which genome sequencing has recently been completed. Both plants are ideally positioned to help answer fundamental questions about the evolution of important biological processes, for example acquisition of desiccation tolerance by land plants (Ralph Quatrano), the establishment of elaborate rooting structures for anchorage and nutrient acquisition (Liam Dolan, University of Oxford, UK) and the development of leaves for efficient photosynthesis (Jane Langdale, University of Oxford, UK).

How did plants equip themselves for survival on land?

  1. Top of page
  2. 25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010
  3. How can we be sure of the exact date of land-plant arrival?
  4. How did plants equip themselves for survival on land?
  5. The big picture: interplay between land plants, geology, the atmosphere and ecosystems
  6. What does the future hold?
  7. References

Interactions with mycorrhizal fungi were crucial for plants to successfully colonize dry land, as hypothesized 35 yr ago (Pirozynski & Malloch, 1975). Fossil evidence shows that symbiotic soil fungi co-evolved with land plants before sophisticated rooting systems were developed. Even the most basal groups of rootless liverworts have associations with mycorrhizal fungi. David Beerling (University of Sheffield, UK) showed that associations such as these increase plant fitness, particularly in the high-CO2 atmosphere present during early land plant evolution (Humphreys et al., 2010). Arbuscular mycorrhizal (AM) symbiosis is particularly critical to improve phosphate uptake from the soil. Jonathan Leake (University of Sheffield, UK) showed a close correlation between phosphorus uptake, mycorrhizal hyphal length and plant size. He argued that the evolution of these plant–fungal associations played a crucial role in shaping terrestrial ecosystems and helping plants inhabit low-nutrient environments. Importantly, although mycorrhizal fungi evolved under conditions of relatively high CO2, the early-evolving mycorrhizas of liverworts increased reproductive fitness under both high- and low-CO2 conditions.

The signalling pathway controlling plant–AM symbiosis (sym genes) seems to be conserved in all Embryophytes (Wang et al., 2010), suggesting that the genes involved in mycorrhizal symbiosis were present in the common ancestor of all land plants. The ancient AM symbiosis pathway has probably been recruited and adapted for a later-evolving intracellular symbiosis with bacteria (Parniske, 2008). Allan Downie (John Innes Centre, UK) highlighted this and discussed the importance of nitrogen-fixing symbiosis during land plant evolution.

John Raven (University of Dundee, UK) described the nutritional and morphological innovations that accompanied plants’ evolution on dry land. Data from the fossil record suggests that the Silurian was the period where cuticle, xylem, stomata and intracellular gas spaces first arose. These attributes were undoubtedly crucial for plants to withstand dry environments and enhance desiccation tolerance. The new transpiration faculties also allowed better regulation of CO2 uptake.

The big picture: interplay between land plants, geology, the atmosphere and ecosystems

  1. Top of page
  2. 25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010
  3. How can we be sure of the exact date of land-plant arrival?
  4. How did plants equip themselves for survival on land?
  5. The big picture: interplay between land plants, geology, the atmosphere and ecosystems
  6. What does the future hold?
  7. References

A significant proportion of the meeting focused on how interactions between plants, soil/rocks and the atmosphere have shaped present-day life on earth (Fig. 1b).

Euan Nisbet (University of London, UK) discussed the interplay among living organisms, geology and the atmosphere. The evolution of photosynthesis remade the earth’s atmosphere as a ‘biological construction’. Ancient photosynthesizers were anoxygenic and methanogenic: the evolution of cyanobacterial photosynthesis (and hence the eventual creation of atmospheric oxygen) initiated a series of events that shaped the planet as we know it today. The carbon signature of the oldest rocks (in Greenland) suggests that biological activity was present from 3.8 billion yr ago (Nisbet & Sleep, 2001). As formation of soil from rocks requires biological activity, land plants (otherwise known as ‘land survival devices for cyanobacteria’!) could not have evolved without interplay between organisms (bacteria and algae), rocks and the atmosphere. In turn, land plants now interact with bacteria and algae to shape our current atmosphere (Nisbet & Nisbet, 2008).

Connections between atmospheric events and plant and animal evolution were highlighted by Emma Hammarlund (University of Southern Denmark, Denmark) who described how the oxidation states of iron and molybdenum in deep-sea sediments could be used to calculate the amount of oxygen present in the atmosphere in the past. The data suggested that two large increases in oxygen occurred: the first at 550 Ma (before the Cambrian explosion) and the second (a larger increase than the first) at 400 Ma. The dates for both increases correlate with the data available on stomatal density in fossil plants, and the second, larger, rise corresponds to an increase in the diversity of vascular plants. Could this increase in biomass have caused the second increase in atmospheric oxygen? The increase in oxygen that occurred 400 Ma may have enabled the evolution of large fish in the oceans (Dahl et al., 2010).

In addition to discussing mycorrhizas, Jonathan Leake (University of Sheffield, UK) described how the evolution of land plants has influenced both the soil and the atmosphere, and vice versa. In addition to the soil providing nutrients for the plant, root architecture in turn influences the soil, both mechanically and via release of chemicals, such as calcium, from rocks upon phosphate uptake.

Liam Dolan (University of Oxford, UK) described the evolution of deep-rooting systems in the Devonian (417–354 Ma), which enhanced the silicate weathering of soil (Berner & Kothavala, 2001; Raven & Edwards, 2001). This may have contributed to the drop in atmospheric CO2 concentration (and hence in global temperatures) associated with subsequent glaciation during the early Carboniferous period.

The evolution of angiosperms (Fig. 1a) has had profound effects on ecosystems and climate. Kevin Boyce (University of Chicago, IL, USA) elucidated how the evolution of the complex branching vascular systems in angiosperms resulted in these plants having a transpiration rate four times higher than that of earlier-evolving plants such as ferns. This adaptation is likely a prerequisite for the establishment of rainforests, as climate models excluding angiosperms show the ‘tropics’ as drier and more seasonal. Therefore, the evolution of angiosperms has had profound effects on the water cycle (Boyce & Lee, 2010). Kevin suggested that ‘modern’ ecology was not applicable to plant communities before the advent of angiosperms: for example, the large forests of the Carboniferous could not have been capable of the types of environmental ‘buffering’ carried out by extant angiosperm forests.

What does the future hold?

  1. Top of page
  2. 25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010
  3. How can we be sure of the exact date of land-plant arrival?
  4. How did plants equip themselves for survival on land?
  5. The big picture: interplay between land plants, geology, the atmosphere and ecosystems
  6. What does the future hold?
  7. References

Plant diversity and the carbon cycle, with particular reference to the future, was the subject of a talk by Ian Woodward (University of Sheffield, UK). Contrary to ‘popular’ thinking, current species diversity models (that relate species diversity to net primary productivity in a nonlinear manner) suggest that by 2050 a climate with increasing temperature and higher CO2 concentrations will increase overall biodiversity as ‘alien’ species redistribute into new environments (Woodward & Kelly, 2008). This resulted in a discussion on whether the potential loss of a few species of alpines as their cooler niche habitats disappeared was of primary concern! A decrease in plant diversity and biomass in the Amazon basin is predicted, as a result of reduced rainfall (Meir & Woodward, 2010). Even if human activity somehow stabilized the current CO2 concentrations, the temperature would continue to rise as a result of the past CO2 increases. In this situation, models predict a decrease in biodiversity everywhere apart from in very high and in very cold places (Woodward & Kelly, 2008). However, these models do not take into account the effect of human impact on biodiversity, which is much more detrimental in the short-term.

The objectives of the 25th New Phytologist/Colston Research Society Symposium were to ‘bring together cutting-edge plant scientists, geochemists and palaeontologists to discuss the most recent advances in this area’ and to ‘set the scientific agenda in this area for the next five years’. Both objectives were successfully achieved. The diversity of researchers present ensured animated debate and stimulated new collaborations.

The meeting particularly highlighted the importance of using genomic and ‘evo-devo’ studies on emerging model systems, including early-evolving land plants and algae. It also emphasized the use of mathematical modelling to interpret the past and predict the future. In the coming years, the new dialogue between the disciplines will ensure that we truly begin to understand the mechanisms by which plants colonized the terrestrial environment, and how land plants dictated our past and will shape our future. Only then can we fully address the challenges of how changes in the atmosphere, climate and biodiversity will affect our future societies.

References

  1. Top of page
  2. 25th New Phytologist/Colston Research Society Symposium – Colonization of the terrestrial environment, Bristol, UK, September 2010
  3. How can we be sure of the exact date of land-plant arrival?
  4. How did plants equip themselves for survival on land?
  5. The big picture: interplay between land plants, geology, the atmosphere and ecosystems
  6. What does the future hold?
  7. References