Skip to main content
SpringerLink
Log in

Photosynthesis in Early Land Plants: Adapting to the Terrestrial Environment

  • Chapter
  • First Online:
Photosynthesis in Bryophytes and Early Land Plants

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 37))

Summary

The embryophytic land plants evolved from charophycean green algae, one of the three clades of green algae which are important components of the microflora of present-day terrestrial habitats. The earliest embryophytes are recognised in the fossil record from their characteristic spores, with little evidence as to their vegetative structure. These earliest embryophytes presumably resemble the extant terrestrial green algae in being desiccation tolerant and poikilohydric. Only the embrophytes subsequently developed the homoiohydry which characterised the organism which today contribute most of the biomass and primary productivity on land, and allowed many of the organisms to become desiccation intolerant in the vegetative phase. Pre-Carboniferous land plant fossils have very few examples of bryophytes other than spores: exceptions are the Middle Devonian Metzgeriothallus and the Upper Devonian Pallaviciniites. Many of the other fossils are recognisable as polysporangiophytes, including vascular plants. Homoiohydry in some of these plants is shown by the occurrence of cuticle and stomata, although there is no fossil evidence bearing on desiccation tolerance/intolerance. In addition to the embryophytes there are many other fossils, e.g. Pachytheca, Parka, Protosalvinia, Prototaxites and Spongiophyton, which are probably photosynthetic organisms, but are not readily classified: algae, bryophytes and lichens have been suggested, in addition to the possibility that some represent terrestrial fungi. The high atmospheric CO2 concentrations in the early Phanerozoic would have permitted higher rates of photosynthesis than occurs today on the basis of the surface area of the plant exposed to the gas phase because large concentration gradients from the atmosphere to the carboxylase driving diffusive entry of CO2 are possible. Relatively complex morphologies (several layers of photosynthetic structures) and/or anatomy (ventilation within the organisms using gas spaces) are required if the light-harvesting capacity is to be matched by the CO2 assimilation capacity.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

CAM:

Crassulacean Acid Metabolism;

CCM:

CO2 concentrating mechanism;

δ13C:

quantitative measure of the stable carbon isotope ratio relative to the standard carbon in the VPDB (Vienna Peee Dee Belemnite). δ13C = {[(13C/12C)sample/(13C/12C)standard] – 1} × 1,000;

Ga:

109 years;

Ma:

106 years;

Rubisco:

Ribulose Bisphosphate Carboxylase-Oxygenase

References

  • Abbott GD, Ewbank G, Edwards D, Wang G-Y (1998) Molecular characterization of some enigmatic Lower Devonian fossils. Geochim Cosmochim Acta 62:1407–1418

    CAS  Google Scholar 

  • Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685–695

    PubMed  Google Scholar 

  • Ayres E, van der Wal R, Sommerkorn M, Bardgett RD (2006) Direct uptake of soil nitrogen by mosses. Biol Lett 2:286–288

    CAS  PubMed  Google Scholar 

  • Baars C, Edwards D (2008) Effects of elevated atmospheric CO2 on spore capsules of the moss Leptobryum pyriforme. J Bryol 30:26–40

    Google Scholar 

  • Baars C, Jones TH, Edwards D (2008) Microcosm studies on the role of land plants in elevating carbon dioxide and chemical weathering. Glob Biogeochem Cycl 22(3):Art No. GB3019

    Google Scholar 

  • Becker B, Marin B (2009) Streptophyta algae and the origin of embryophytes. Ann Bot (Oxford, UK) 103:999–1004

    CAS  Google Scholar 

  • Beerling DJ (2005) Leaf evolution: gases, genes and geochemistry. Ann Bot (Oxford, UK) 96:3345–3352

    Google Scholar 

  • Beerling DJ, Franks PJ (2009) Evolution of stomatal function in ‘lower’ land plants. New Phytol 183:921–925

    PubMed  Google Scholar 

  • Beerling DJ, Fox A, Stevenson DS, Valdes PJ (2011) Enhanced chemistry-climate feedbacks in past greenhouse worlds. Proc Natl Acad Sci USA 108:9770–9775. www.pnas.org/cgi/101073/pnas.1102409108

  • Bell G, Mooers AO (1997) Size and complexity among multicellular organisms. Biol J Linn Soc 60:345–363

    Google Scholar 

  • Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the earth system, past and present. Curr Opin Plant Biol 13:233–240

    PubMed  Google Scholar 

  • Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. Biol Lett 7:574–577

    PubMed  Google Scholar 

  • Bidartondo MI, Duckett JG (2010) Conservative ecological and evolutionary patterns in liverwort-fungal symbioses. Proc R Soc Lond Ser B 277:485–492

    Google Scholar 

  • Blank CE, Sánchez-Baracaldo P (2010) Timing of morphological and ecological innovations in the cyanobacteria – a key to understanding the rise of atmospheric oxygen. Geobiology 8:1–23

    CAS  PubMed  Google Scholar 

  • Bomfleur B, Krings M, Kerp H (2010) Thalloid organisms and the fossil record. New perspectives from the Transantarctic Mountains. Plant Signal Behav 5:293–295

    PubMed  Google Scholar 

  • Bowman JL (2011) Stomata: active portals for flourishing on land. Curr Biol 21:R540–R541

    CAS  PubMed  Google Scholar 

  • Boyce CK (2008) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34:179–194

    Google Scholar 

  • Boyce CK (2010) The evolution of plant development in a palaeontological context. Curr Opin Plant Biol 13:102–107

    PubMed  Google Scholar 

  • Boyce CK, Hotton CL (2010) Prototaxites was not a taphonomic artefact. Am J Bot 97:1073

    PubMed  Google Scholar 

  • Boyce CK, Hotton CL, Fogel ML, Cody GD, Hazen RM, Knoll AH, Hueber FM (2007) Devonian landscape heterogeneity recorded by a giant fungus. Geology 35:399–401

    CAS  Google Scholar 

  • Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585. doi:10.1126/science.1197985

    CAS  PubMed  Google Scholar 

  • Brodribb TJ, Field TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898

    CAS  PubMed  Google Scholar 

  • Brodribb TJ, McAdam SAM, Jordan GJ, Field TS (2010) Evolution of stomatal responsiveness of water-use efficiency among land plants. New Phytol 183:839–847

    Google Scholar 

  • Brown RC, Lemmon BE (2011) Spores before sporophytes: hypothesizing the origin of sporogenesis at the algal-plant transition. New Phytol 192:266–301. doi:10.1111/j.1469-8137.03709.x

    Google Scholar 

  • Budke JM, Goffinet B, Jones CS (2011) A hundred-year-old question: is the moss calyptra covered by a cuticle? A case study of Funaria hygrometrica. Ann Bot (Oxford, UK) 107:1279–1286

    Google Scholar 

  • Butterfield NJ (2000) Bangiomorpha n. gen. n. sp.: implications for the evolution of sex, unicellularity, and the Mesoproterozoic/Neoproterozic radiation of eukaryotes. Paleobiology 26:386–404

    Google Scholar 

  • Butterfield NJ (2004) A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implication for the evolution of Proterozoic eukaryotes and the Cambrian explosion. Paleobiology 30:231–252

    Google Scholar 

  • Butterfield NJ (2007) Macroevolution and macroecology through deep time. Palaeontology 50:41–55

    Google Scholar 

  • Butterfield NJ, Knoll AH, Swett K (1988) Exceptional preservation of fossils in an upper Proterozoic shale. Nature 334:424–427

    CAS  PubMed  Google Scholar 

  • Butterfield NJ, Knoll AH, Swett K (1990) A bangiophyte red alga from the Proterozoic of Arctic Canada. Science 250:104–107

    CAS  PubMed  Google Scholar 

  • Caisova L, Marin B, Sausen N, Pröschold T, Melkonian M (2011) Polyphyly of Chaetophora and Stigeoclonium within the Chaetophorales (Chlorophyceae), revealed by sequence comparison on nuclear-encoded SSU rRNA genes. J Phycol 47:164–177. doi:10.1111/j.1529-8817.2010.00949.x

    Google Scholar 

  • Cardon ZG, Gray DW, Lewis LA (2008) The green algal underground: evolutionary secrets of desert cells. BioScience 58:114–122

    Google Scholar 

  • Chang Y, Graham SW (2011) Inferring the higher-order phylogeny of mosses (Bryophyta) and relatives using a large, multigene plastid data set. Am J Bot 98:839–849

    PubMed  Google Scholar 

  • Channing A, Edwards D (2009) Yellowstone hot spring environments and the palaeo-ecophysiology of Rhynie Chert plants: towards a synthesis. Plant Ecol Divers 2:111–143

    Google Scholar 

  • Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behaviour conserved across 400 million years of land plant evolution. Curr Biol 21:1025–1029

    CAS  PubMed  Google Scholar 

  • Clarke JT, Warnock RCM, Donoghue PCJ (2011) Establishing a time-scale for plant evolution. New Phytol 192:266–301. doi:10.1111/j.1469-8137.2011.03794.x

    PubMed  Google Scholar 

  • Cockell CS, Kaltenegger L, Raven JA (2009) Cryptic photosynthesis – extrasolar planetary oxygen without a surface biological signature. Astrobiology 9:623–636. doi:10.1089/ast.2008.0273

    PubMed  Google Scholar 

  • Cole KH, Sheath RG (1990) Biology of the red algae. Cambridge University Press, Cambridge/New York

    Google Scholar 

  • Csintalan Z, Takáks Z, Proctor MCF, Nagy Z, Tiuba Z (2000) Early morning photosynthesis in the moss Tortula ruralis following summer dew fall in the Hungarian dry sandy grassland. Plant Ecol 151:51–54

    Google Scholar 

  • Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov V (2010) A new extreme environment for aerobic phototrophs: biological soil crusts. In: Hallenbrock PC (ed) Recent advances in phototrophic prokaryotes. Advances in experimental medicine and biology, vol 657. Springer, Berlin, pp 3–14

    Google Scholar 

  • Derenne S, Metzger P, van Berber PF, Galletier JP, Sinninghe Damsté JS, De Leeuw JW, Berkaloff C (1992) Similar morphological and chemical variations of Gloecapsomorpha prisca in Ordovician sediments and cultures of Botryococcus braunii as a response to changes in salinity. Org Geochem 19:299–313

    CAS  Google Scholar 

  • Derry LA (2006) Fungi, weathering, and the emergence of animals. Science 311:1386–1387

    CAS  PubMed  Google Scholar 

  • Doi M, Shimazaki K (2008) The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiol 147:922–930

    CAS  PubMed  Google Scholar 

  • Doi M, Wada M, Shimazaki K (2008) The stomata of the fern Adiantum capillus-veneris lack stomatal responses to blue light. Plant Cell Physiol 47:748–755

    Google Scholar 

  • Duckett JG, Pressel S, P’ng KMY, Renzaglia KS (2009) Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum. New Phytol 183:1053–1063

    CAS  PubMed  Google Scholar 

  • Duckett JG, Pressel S, P’ng KMY, Renzaglia KS (2010) The Sphagnum air-gun mechanism resurrected? Not with a closer look. New Phytol 185:89–891

    Google Scholar 

  • Edwards D (1996) New insights into early land ecosystems: a glimpse of a lilliputian world. Rev Palaeobot Palynol 90:159–174

    Google Scholar 

  • Edwards D (2000) The role of Mid-Palaeozoic mesofossils in the detection of early bryophytes. Philos Trans R Soc B 355:733–754

    CAS  Google Scholar 

  • Edwards D (2003) Xylem in early tracheophytes. Plant Cell Environ 26:57–72

    Google Scholar 

  • Edwards D (2004) Embryophytic sporophytes in the Rhynie and Windyfield cherts. Trans R Soc Edinb Earth Sci 94:397–410

    Google Scholar 

  • Edwards D, Axe L (2012) Evidence for a fungal affinity for Nematasketum Burgess and Edwards, a close ally of Prototaxites Dawson. Bot J Linn Soc 168:1–18

    Google Scholar 

  • Edwards D, Abbott GD, Raven JA (1996) Cuticles in early land plants: a palaeoecophysiological evaluation. In: Kierstens G (ed) Plant cuticles. Bios Scientific Publishers, Oxford, pp 1–31

    Google Scholar 

  • Edwards D, Kerp H, Hass H (1997) Stomata in early land plants: an anatomical and ecophysiological approach. J Exp Bot 49:255–278

    CAS  Google Scholar 

  • Edwards D, Axe L, Duckett JG (2003) Diversity of conducting cells in early land plants and comparisons with extant bryophytes. Bot J Linn Soc 141:297–347

    Google Scholar 

  • Edwards D, Richardson JB, Axe L, Davies KL (2012) A new group of Early Devonian plants with valvate sporangia containing sculptured permanent dyads. Bot J Linn Soc 168:229–257

    Google Scholar 

  • Emiliani G, Fondi M, Fani R, Gribaldo S (2009) A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol Direct 4:7. doi:10.1186/1745-6150-4-7

    PubMed  Google Scholar 

  • Espiñeira JM, Uzal EO, Ros LVG, Carrión JS, Merino F, Barceló AR (2011) Distribution of lignin monomers and the evolution of lignification among lower plants. Plant Biol 13:59–68

    PubMed  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    CAS  Google Scholar 

  • Fletcher BJ, Beerling DJ, Chaloner WG (2004) Stable carbon isotopes and the metabolism of the terrestrial Devonian organism Spongiophyton. Geobiology 2:107–119

    Google Scholar 

  • Fritsch FE (1945) Studies in the comparative morphology of the algae. IV. Algae and archegoniate plants. Ann Bot (Oxford, UK) New Series 9:1–30

    Google Scholar 

  • Gadd GM, Raven JA (2010) Geomicrobiology of eukaryotic microorganisms. Geomicrobiol J 27:491–519

    CAS  Google Scholar 

  • Gensel PG (2008) The earliest land plants. Annu Rev Ecol Evol Syst 39:439–477

    Google Scholar 

  • Gensel PG, Chaloner WG, Forbes WH (1991) Spongiophyton from the late Lower Devonian of New Bruswick and Quebec, Canada. Palaeontology 34:149–168

    Google Scholar 

  • Gerrienne P, Gomez P (2011) Early evolution of life cycles in embryophytes: a focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity. J Syst Evol 49:1–16

    Google Scholar 

  • Gerrienne P, Gensel PG, Strullu-Derienne C, Lardeux H, Steemans P, Prestianni C (2011) A simple type of wood in two early Devonian plants. Science 333:837

    CAS  PubMed  Google Scholar 

  • Graham LE, Wilcox L (2000) Algae. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Graham LE, Cook ME, Hanson DT, Pigg KB, Graham JM (2010a) Structural, physiological, and stable isotope evidence that the enigmatic Palaeozoic fossil Prototaxites formed from rolled liverwort mats. Am J Bot 97:1079–1086

    PubMed  Google Scholar 

  • Graham LE, Cook ME, Hanson DT, Pigg KB, Graham JM (2010b) Rolled liverwort mat can explain major Prototaxites features: response to commentaries. Am J Bot 97:1079–1086

    PubMed  Google Scholar 

  • Graur D, Martin W (2003) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet 20:80–86

    Google Scholar 

  • Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1245

    CAS  PubMed  Google Scholar 

  • Grebe M (2011) Unveiling the Casparian strip. Nature 473:294–295

    CAS  PubMed  Google Scholar 

  • Griffiths H, Maxwell K, Richardson D, Robe W (2006) Turning the land green: inferring photosynthetic physiology and diffusive limitations in early bryophytes. In: Hemsley A, Poole I (eds) The evolution of plant physiology. Elsevier Academic Press, Kew, pp 33–6

    Google Scholar 

  • Guillou L (2011) Characterization of the Parmales: much more than resolution of a taxonomic enigma. J Phycol 47:2–4

    Google Scholar 

  • Gupta S, Agrawal SC (2004) Vegetative survival and reproduction under submerged and air-exposed conditions and vegetative survival as affected by salts, pesticides and metals in aerial green alga Trentepohlia aura. Folia Microbiol 49:37–40

    CAS  Google Scholar 

  • Hamerlynck EP, Csintalen Z, Nagy Z, Tuba Zm Goodin D, Henebry GM (2002) Ecophysiological consequences of contrasting microenvironments on the desiccation tolerant moss Tortula ruralis. Oecologia 131:498–505

    Google Scholar 

  • Hanson D, Andrews TJ, Badger MR (2002) Variability of the pyrenoid-based CO2-concentrating mechanism in hornworts (Anthocerophyta). Funct Plant Biol 28:407–416

    Google Scholar 

  • Hao S, Xue J, Guo D, Wang D (2010) Earliest rooting system and root:shoot ratio from a new Zosterophyllum plant. New Phytol 185:217–225

    PubMed  Google Scholar 

  • Hartung W (2010) The evidence of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37:806–812

    CAS  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    CAS  PubMed  Google Scholar 

  • Hemsley AR (1989) The ultrastructure of the Devonian plant Parka decipiens. Anns Bot (Oxford, UK 64:359–367

    Google Scholar 

  • Hernick LV, Landing E, Bartowski KE (2008) Earth’s oldest liverworts – Metzgeriothallus sharonae sp. nov. from the Middle Devonian (Givetian) of eastern New York, USA. Rev Palaeobot Palynol 148:154–162

    Google Scholar 

  • Hietz P, Wanek W, Popp M (1999) Stable isotope composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect. Plant Cell Environ 22:1435–1443

    Google Scholar 

  • Hillier RD, Edwards D, Morrisey LP (2008) Sedimentological evidence for rooting structures in the Early Devonian Anglo-Welsh Border (UK), with speculation on their producers. Palaeogeogr Palaeoclimatol Palaeoecol 270:366–380

    Google Scholar 

  • Hobbie EA, Boyce CK (2010) Carbon sources for the Paleozoic giant fungus Prototaxites inferred from modern analogues. Proc R Soc Lond Ser B 277:2149–2156

    CAS  Google Scholar 

  • Hoffmann L (1989) Algae of terrestrial habitats. Bot Rev 55:77–105

    Google Scholar 

  • Hueber FM (1961) Hepaticites devonicus, a new fossil liverwort from the Devonian of New York. Ann Mo Bot Gard 48:125–132

    Google Scholar 

  • Hueber FM (2001) Rotted wood-alga-fungus: the history and life of Prototaxites Dawson. Rev Palaeobot Palynol 116:125–158

    Google Scholar 

  • Ichiniomiya M, Yochikowa S, Kamiya M, Ohki K, Takaichi S, Kuwater A (2011) Isolation and characterization of Parmales (Heterokonta/Heterokontophyta/Stramenopiles) from the Oyashi region, Western North Pacific. J Phycol 47:144–151

    Google Scholar 

  • Javaneau EJ, Knoll AH, Walter MR (2003) Recognizing and interpreting the fossils of early eukaryotes. Orig Life Evol Biosph 33:75–94

    Google Scholar 

  • Jones MR, Leith ID, Fowler D, Raven JA, Sutton MA, Nemiz E, Cape JN, Sheppard LJ, Smith RI, Theobald MR (2007a) Concentration-dependent NH3 deposition processes for mixed moorland semi-natural vegetation. Atmos Environ 41:2049–2060

    CAS  Google Scholar 

  • Jones MR, Leith ID, Fowler D, Raven JA, Sutton MA, Nemiz E, Cape JN, Sheppard LJ, Smith RI (2007b) Concentration-dependent NH3 deposition processes for stomatal and non-stomatal moorland species. Atmos Environ 41:8980–8994

    CAS  Google Scholar 

  • Karatygin IV, Snigirevskaya NS, Vikulin SV (2009) The most ancient terrestrial lichen Winfrenatia reticulata: a new find and new interpretation. Palaeont J 43:107–114

    Google Scholar 

  • Karsten U, Lütz C, Holzinger A (2010) Ecophysiological performance of the aeroterrestrial green alga Klebsormidium crenulatum (Charophyceae, Streptophyta) isolated from an alpine soil crust with an emphasis on desiccation stress. J Phycol 56:1187–1197

    Google Scholar 

  • Kennedy M, Droser M, Mayer LM, Pevear D, Mrofka D (2006) Late Precambrian oxygenation; inception of the clay mineral factory. Science 311:1446–1449

    CAS  PubMed  Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39

    CAS  Google Scholar 

  • Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud P-F, Pan A, Quatrano RS (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327:546

    CAS  PubMed  Google Scholar 

  • Konrad W, Roth-Nebelsick A, Kerp H, Hass H (2000) Transpiration and assimilation of Early Devonian land plants with axially symmetric telomes – simulations at the tissue level. J Theor Biol 206:91–107

    CAS  PubMed  Google Scholar 

  • Kotyk ME, Basinger JF, Gensel PG, Freitas TF (2002) Morphologically complex plant macrofossils from the late Silurian of Arctic Canada. Am J Bot 89:1004–1013

    PubMed  Google Scholar 

  • Lang WH (1937) On the plant-remains from the Downtonian of England and Wales. Philos Trans R Soc B 227:245–291

    Google Scholar 

  • Lenton TM, Watson AJ (2004) Biotic enhancement of weathering, atmospheric oxygen and carbon dioxide in the Neoproterozoic. Geophys Res Lett 31:L05202. doi:10.1029/2003GL018802

    Google Scholar 

  • Lenton TM, Crouch MJC, Johnson MT, Pires N, Nolan (2012) Enhanced weathering by the first land plants caused Late Ordovician global change. Nat Geosci 5:86–89

    CAS  Google Scholar 

  • Lewis LA (2007) Chlorophyta on land. Independent lineages of green eukaryotes from arid lands. N: algae and cyanobacteria in extreme environments. Cellular origin, life in extreme habitats and astrobiology, vol 11, Part 6. Springer, Berlin, pp 569–582

    Google Scholar 

  • Lewis LA, Lewis PO (2005) Unearthing the molecular phylodiversity of desert green algae (Chlorophyta). Syst Biol 54:936–947

    PubMed  Google Scholar 

  • Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556

    PubMed  Google Scholar 

  • Ligrone R, Caraf A, Duckett JG, Renzaglia KS, Ruel K (2008) Immunocytochemical detection of lignin-related epitopes in cell walls in bryophytes and the charalean alga Nitella. Plant Syst Evol 270:257–272. doi:10.1007/s00606-007-0617-z

    CAS  Google Scholar 

  • Lüttge U, Büdel B (2009) Resurrection kinetics of photosynthesis in desiccation-tolerant terrestrial green algae (Chlorophyta) on tree bark. Plant Biol 12:437–444

    Google Scholar 

  • Maberly SC, Madsen TV (1990) The contribution of air and water to the carbon balance of Fucus spiralis L. Mar Ecol Progr Ser 62:175–183

    Google Scholar 

  • Marconi M, Giordano M, Raven JA (2011) Impact of taxonomy, geography and depth on δ13C and δ15N variation in a large collection of macroalgae. J Phycol 47:1025–1035. doi:10.1111/j.1529-8817.2011.01045.x

    Google Scholar 

  • Marischal M, Proctor MCF (2004) Are bryophytes shade plants? Photosynthetic light response and proportions of chlorophyll a and total carotenoids. Ann Bot (Oxford, UK) 94:593–603

    Google Scholar 

  • Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somerville C, Ralph J (2009) Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Curr Biol 19:169–175

    CAS  PubMed  Google Scholar 

  • McAllister CA, Bergman DC (2011) Sequence and formation of basic helix-loop-helix proteins required for stomatal development in Arabidopsis are deeply conserved in land plants. Evol Dev 13:182–189

    Google Scholar 

  • Meyer M, Seibt U, Griffiths H (2008) To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms. Philos Trans R Soc B 363:2767–2778

    CAS  Google Scholar 

  • Morris JL, Richardson JB, Edwards D (2011) Lower Devonian plant and spore assemblages from the Lower Old Red Sandstone strata of Tredomen Quarry, South Wales. Rev Palaeobot Palynol 185:183–208

    Google Scholar 

  • Nobel PS (1977) Internal leaf area and cellular CO2 resistance. Photosynthetic implications of variations with growth conditions and plant species. Physiol Plant 40:137–144

    CAS  Google Scholar 

  • Oliver MJ, Velter J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799

    PubMed  Google Scholar 

  • Oliver MJ, Guo L, Alexander DC, Ryals JA, Wore BWM, Cushman JC (2011) A sister group contract using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23:1231–1248

    CAS  PubMed  Google Scholar 

  • Org B-L, Lim M, Wee Y-C (1992) Effects of desiccation and illumination on photosynthesis and pigmentation of an edaphic population of Trentepohlia odorata (Chlorophyta). J Phycol 28:768–772

    Google Scholar 

  • Paffrey LW, Lahr DJG, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA 108:13624–13629

    Google Scholar 

  • Pannewitz S, Green TAG, Maysek K, Schensog M, Seppelt R, Sancho LG, Türk R, Schoetter B (2005) Photosynthetic responses of three common mosses from continental Antarctica. Antarct Sci 17:341–352

    Google Scholar 

  • Pittermann J (2010) The evolution of water transport in plants: an integrated approach. Geobiology 8:112–139

    CAS  PubMed  Google Scholar 

  • Popper ZA, Michel G, Hervé C, Domozych DS, Willats WGT, Tuohy MG, Kloareg B, Stengel D (2011) Evolution of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590

    CAS  PubMed  Google Scholar 

  • Proctor MCF (2005) Why do Polytrichaceae have lamellae? J Bryol 27:221–229

    Google Scholar 

  • Proctor MCF (2010) Trait correlation in bryophytes: exploring an alternative world. New Phytol 185:1–3

    PubMed  Google Scholar 

  • Proctor MCF, Tuba Z (2002) Poikilohydry and homoiohydry: antithesis or spectrum of possibilities? New Phytol 156:327–349

    Google Scholar 

  • Proctor MCF, Raven JA, Rice SK (1992) Stable carbon isotope discrimination measurements in Sphagnum and other bryophytes: physiological and ecological implications. J Bryol 17:193–202

    Google Scholar 

  • Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007) Dessication-tolerance in bryophytes: a review. Bryologist 110:595–621

    CAS  Google Scholar 

  • Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455:1101–1104

    CAS  PubMed  Google Scholar 

  • Raven JA (1977) The evolution of vascular land plants in relation to supracellular transport processes. Advances in Botanical Research 5:153–219, Academic Press, London

    CAS  Google Scholar 

  • Raven JA (1984) Physiological correlates of the morphology of early vascular plants. Bot J Linn Soc 88:105–126

    Google Scholar 

  • Raven JA (1993a) Energy and nutrient acquisition by autotrophic symbioses and their asymbiotic ancestors. Symbiosis 14:33–60

    Google Scholar 

  • Raven JA (1993b) The evolution of vascular land plants in relation to quantitative functioning of dead water-conducting cells and stomata. Biol Rev Camb Philos Soc 68:337–363

    Google Scholar 

  • Raven JA (1994a) Physiological aspects of the functioning of vascular tissue in early vascular plants. Bot J Scotl 47:49–64

    Google Scholar 

  • Raven JA (1994b) The significance of the distance from photosynthesising cells to vascular tissue in extant and early vascular plants. Bot J Scotl 47:65–82

    Google Scholar 

  • Raven JA (1995) The early evolution of land plants: aquatic ancestors and atmospheric interactions. Botan J Scotl 47:151–175

    Google Scholar 

  • Raven JA (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Ann Bot (Oxford, UK) 78:137–142

    Google Scholar 

  • Raven JA (1997a) The role of marine biota in the evolution of terrestrial biota: gases and genes. Biogeochemistry 39:139–164

    Google Scholar 

  • Raven JA (1997b) Multiple origins of plasmodesmata. Eur J Phycol 32:95–101

    Google Scholar 

  • Raven JA (1999a) The minimum size of seeds and spores in relation to the ontogeny of homoiohydry. Funct Ecol 13:5–14

    Google Scholar 

  • Raven JA (1999b) The size of cells and organisms in relation to the evolution of embryophytes. Plant Biol 1:2–12

    Google Scholar 

  • Raven JA (2002a) Putting the fight in bryophytes. New Phytol 156:321–326

    Google Scholar 

  • Raven JA (2002b) Tansley review: selection pressures on stomatal evolution. New Phytol 153:371–386

    CAS  Google Scholar 

  • Raven JA (2003) Long-distance transport in non-vascular plants. Plant Cell Environ 26:73–85

    Google Scholar 

  • Raven JA (2005) The evolution of plasmodesmata. In: Oparka K (ed) Plasmodesmata. Blackwell Publishers, Oxford, pp 33–52

    Google Scholar 

  • Raven JA, Andrews M (2010) Evolution of tree nutrition. Tree Physiol (Oxford, UK) 30:1050–71

    Google Scholar 

  • Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52:381–401

    CAS  PubMed  Google Scholar 

  • Raven JA, Edwards D (2004) Physiological evolution of lower embryophytes: adaptations to the terrestrial environment. In: Hemsley AR, Poole I (eds) The evolution of plant physiology: from whole plants to ecosystems, Linnean Society symposium series 21. Elsevier Academic Press, London, pp 17–41

    Google Scholar 

  • Raven JA, Griffiths H, Smith EC, Vaughn KC (1998) New perspectives in the biophysics and physiology of bryophytes. In: Bates JW, Ashton NW, Duckett JG (eds) Bryology for the twenty-first century. Proceedings of the centenary symposium of the British Bryological Society. Maney Publishing and The British Bryological Society, Leeds, pp 261–275

    Google Scholar 

  • Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredricksen J, Dunton KH (2002a) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378

    CAS  Google Scholar 

  • Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Clayton MN, Vanderklift M, Fredriksen S, Dunton KH (2002b) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot (Oxford, UK) 90:525–536

    CAS  Google Scholar 

  • Renzaglia KS, Duff RJ, Nickrent DI, Garbury DI (2000) Vegetative and reproductive innovations for a unified phylogeny. Philos Trans R Soc B 355:769–793

    CAS  Google Scholar 

  • Rice SK (2000) Variation in carbon isotope discrimination within and among Sphagnum species in a temperate wetland. Oecologia 123:1–8

    Google Scholar 

  • Rice SK, Giles L (1996) The influence of water content and leaf anatomy on carbon isotope discrimination and photosynthesis in Sphagnum. Plant Cell Environ 19:118–124

    CAS  Google Scholar 

  • Rice SK, Aclander L, Hansen DT (2008) Do bryophyte shoot systems function like vascular plant leaves or canopies? Functional trait relationship in Sphagnum mosses (Sphagnaceae). Am J Bot 95:1366–1374

    PubMed  Google Scholar 

  • Rindi F, Lam DW, López-Bautista JM (2009a) Phylogenetic relationships and species circumscription in Trentepohlia and Printzina (Trentepohliales, Chlorophyta). Mol Phylogenet Evol 52:329–339

    CAS  PubMed  Google Scholar 

  • Rindi F, Allali HA, Lam DW, López-Bautista JM (2009b) An overview of the biodiversity and biogeography of terrestrial green algae. In: Rescigno V et al (eds) Biodiversity hotspots. Nova Science Publishers, New York, pp 1–25

    Google Scholar 

  • Romankiw LA, Hatcher PG, Roen JB (2007) Evidence of land plant affinities for the Devonian fossil Protosalvinia (Foerstia). Lethaia 21:417–423

    Google Scholar 

  • Ropello D, De Rybel B, Tendon VD, Püster A, Alassimone J, Vermeer JEM, Yamazaki M, Stierhof Y-D, Beeckman T, Geldner M (2011) A novel protein family mediates Casparian strip formation in the endodermis. Nature 473:380–383

    Google Scholar 

  • Roth-Nebelsick A (2001) Heat transfer of rhyniophytic plant axes. Rev Palaeobot Palynol 116:112–139

    Google Scholar 

  • Roth-Nebelsick A (2005) Reconstructing atmospheric carbon dioxide with stomata: possibilities and limitations of a botanical CO2 sensor. Trees Struct Funct 19:251–265

    Google Scholar 

  • Roth-Nebelsick A, Konrad W (2005) Assimilation and transpiration capabilities of rhyniophytic plants from the Lower Devonian and their implications for palaeoatmospheric CO2 concentrations. Palaeogeogr Palaeoclimatol Palaeoecol 202:153–178

    Google Scholar 

  • Roth-Nebelsick A, Grimm G, Mosbrugger V, Hass H, Kerp H (2000) Morphometric analysis of Rhynia and Asteroxylon: testing functional aspects of early land plant evolution. Palaeobiology 26:406–418

    Google Scholar 

  • Rubinstein CV, Gerrienne P, de la Puente GS, Astini RA, Steemans P (2010) Early middle Ordovician evidence for land plants in Argentina (Eastern Antarctica). New Phytol 188:365–369

    CAS  PubMed  Google Scholar 

  • Rugg DA, Norton TA (1987) Pelvetia canaliculata, a high-shore seaweed that shuns the sea. In: Crawford RMM (ed) Plant life in aquatic and amphibious habitats. Blackwell, Oxford, pp 347–358

    Google Scholar 

  • Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, Hetherington AM (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21:1030–1035

    CAS  PubMed  Google Scholar 

  • Sánchez-Baracaldo P, Hayes PK, Blank CE (2005) Morphological and habitat evolution in the Cyanobacteria using a compartmentalization approach. Geobiology 3:145–165

    Google Scholar 

  • Sanders WS (2004) The intertidal marine lichen formed by the pyrenomycete fungus Verrucaria tavaresiae (Ascomytina) and the brown alga Petroderma maculiforme (Phaeophyceae) thallus organisation and symbiont interaction. Am J Bot 91:511–522

    PubMed  Google Scholar 

  • Sarkar P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot 60:3615–3635

    CAS  PubMed  Google Scholar 

  • Senousy HH, Beakes GW, Hack E (2004) Phylogenetic placement of Botryococcus braunii (Trebouxiophyceae) and Botryococcus sudatis isolate UTEX 2629 (Chlorophyceae). J Phycol 40:412–423

    CAS  Google Scholar 

  • Shaw AJ, Szövény P, Shaw B (2011) Bryophyte diversity and evolution: windows into the early evolution of land plants. Am J Bot 98:352–369

    PubMed  Google Scholar 

  • Shields GA (2007) A normalised seawater strontium isotope curve: possible implications for Neoproterozoic-Cambrian weathering rates and the further oxygenation of the Earth. eEarth 3:35–42

    Google Scholar 

  • Smith BN, Epstein E (1971) Two categories of 13C/12C ratios for high plants. Plant Physiol 47:380–384

    CAS  PubMed  Google Scholar 

  • Smith EC, Griffiths H (1996a) The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes. Planta 198:6–16

    CAS  Google Scholar 

  • Smith EC, Griffiths H (1996b) A pyrenoid-based carbon concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta 200:203–212

    CAS  Google Scholar 

  • Smith EC, Griffiths H (2000) The role of carbonic anhydrase in photosynthesis and the activity of the carbon concentrating mechanisms in bryophytes of the class Anthocerotae. New Phytol 145:29–37

    CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Souffreau C, Vanormelingen P, Verleyen E, Sabbe K, Wyverman W (2010) Tolerance of benthic diatoms from temperate aquatic and terrestrial habitats to experimental desiccation and temperature stress. Phycologia 49:309–324

    Google Scholar 

  • Souffreau C, Vanormelingen P, Sabbe K, Vyverman W (2013) Tolerance of resting cells of freshwater and terrestrial benthic diatoms to experimental -desiccation and freezing is habitat-dependent. Phycologia 52:246–255

    Google Scholar 

  • Sperry JS (2003) Evolution of water transport and xylem structure. Int J Plant Sci 164:S115–S127

    Google Scholar 

  • Stein WE, Mannolini F, VanAller Hernick L, Landing E, Berry CM (2007) Giant cladoxylopsid trees resolve the enigma of the earth’s earliest tree stumps at Gilboa. Nature 446:904–907

    CAS  PubMed  Google Scholar 

  • Stein WE, Berry CM, VanAller Hernick L, Mannolini F (2012) Surprisingly complex community discovered in mid-Devonian fossils forest at Gilboa. Nature 483:78–81

    CAS  PubMed  Google Scholar 

  • Strother PK (2010) Thalloid carbonaceous incrustations and the asynchronous evolution of embryophyte characters during the Paleozoic. Int J Coal Geol 83:154–161

    CAS  Google Scholar 

  • Strother PK, Battison L, Brasier MD, Wellman CH (2011) Earth’s earliest non-marine eukaryotes. Nature 473:505–509. doi:10.1038/nature09943

    CAS  PubMed  Google Scholar 

  • Surif MB (1989) Physiology of photosynthesis in relation to the taxonomy of the Phaeophyta. PhD Thesis, University of Dundee

    Google Scholar 

  • Surif MB, Raven JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic aspects. Oecologia 78:97–105

    Google Scholar 

  • Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82:68–80

    Google Scholar 

  • Taylor TN, Hass H, Remy W, Kerp H (1995) The oldest fossil lichen. Nature 378:244

    CAS  Google Scholar 

  • Taylor TN, Taylor EL, Krings M (2009) Paleobotany: the biology and evolution of fossil plants, 2nd edn. Academic, Amsterdam

    Google Scholar 

  • Taylor TN, Taylor EL, Decorbeix A-L, Schwenderer A, Serbet R, Escapa I, Krings M (2010) The enigmatic Devonian fossil Prototaxites is not a rolled-up liverwort mat. (comment on paper by Graham et al.). Am J Bot 97:268–275

    Google Scholar 

  • Taylor WA, Gensel PG, Wellman CH (2011) Wall ultrastructure in three species of dispersed spore Emphanisporites from the Early Devonian. Rev Palaeobot Palynol 163:264–280

    Google Scholar 

  • Teyssèdre B (2006) Are the green algae (Phylum Viridiplantae) two billion years old? Carnets de Geologie 2006(3):1–15

    Google Scholar 

  • Tomescu AMF, Rothwell GW (2006) Wetlands before tracheophytes: thalloid terrestrial communities of the Early Silurian Passage Creek biota (Virginia). Geol Soc Am Spec Pap 399:41–56

    Google Scholar 

  • Tomescu AMF, Rothwell GW, Honegger R (2006) Cyanobacterial macrophytes in an Early Silurian (Llandovery) continental biota: Passage Creek, lower Massanuten Sandstone, Virginia, USA. Lethaia 39:329–338

    Google Scholar 

  • Tomescu AMF, Pratt LM, Rothwell GW, Strother PK, Nadon GC (2009) Carbon isotopes support the presence of extensive land floras pre-dating the origin of vascular plants. Palaeogeogr Palaeoclimatol Palaeoecol 283:45–59

    Google Scholar 

  • Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: molecular phylogenetic and palaeontological perspectives. Proc Natl Acad Sci USA 103:5442–5447

    CAS  PubMed  Google Scholar 

  • Tschernak E (1941) Untersuchungen über die Beziehungen von Pilze und Alge in Flechtenthallus. Ost Bot Z 90:233–307

    Google Scholar 

  • Turmel M, Brouard J-S, Gagron C, Otis C, Lemieux C (2008) Deep division in the Chlorophyceae (Chlorophyta) revealed by chloroplast phylogeny analyses. J Phycol 44:739–750

    CAS  Google Scholar 

  • Turnbull JD, Robinson SA (2009) Desiccation protects two Antarctic mosses from ultraviolet-B induced DNA damage. Funct Plant Biol 36:214–221

    CAS  Google Scholar 

  • Tymms MJ, Ganff DF (1979) Proline accumulation during water stress in resurrection plants. J Exp Bot 30:165–168

    CAS  Google Scholar 

  • Van den Hoek C, Mann BG, Jahns HM (1995) Algae. An introduction to phylogeny. Cambridge University Press, Cambridge

    Google Scholar 

  • Waite M, Sack L (2010) How does moss photosynthesis relate to leaf and canopy structure? Trait relationships for 10 Hawaiian species of contrasting light habitats. New Phytol 185:156–172

    CAS  PubMed  Google Scholar 

  • Waite M, Sack L (2011) Does global stoichiometric theory apply to bryophytes? Tests across an elevation x soil age ecosystem matrix on Mauna Loa, Hawaii. J Ecol 99:122–134

    Google Scholar 

  • Wang XQ, Yang PF, Liu Z, Liu WZ, Hu Y, Chen H, Kuang TY, Reis ZM, Shen SH, He YK (2009) Exploring the mechanism of Physcomitrella patens desiccation tolerance through a proteomic strategy. Plant Physiol 149:1739–1750

    CAS  PubMed  Google Scholar 

  • Watkins JE, Rundell PW, Cardelús CL (2007a) The influence of life forms on carbon and nitrogen relationship in tropical rainforest ferns. Oecologia 153:225–232

    PubMed  Google Scholar 

  • Watkins JE, Mack MC, Sinclair TR, Mulkey SS (2007b) Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytol 176:708–717

    PubMed  Google Scholar 

  • Wellman CH (2010) The invasion of the land by plants: when and where? New Phytol 188:306–309

    PubMed  Google Scholar 

  • Wellman CH, Osterloff PL, Mohluddin U (2003) Fragments of the earliest land plants. Nature 425:282–285

    CAS  PubMed  Google Scholar 

  • Weng J-K, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–295

    CAS  PubMed  Google Scholar 

  • Williams TG, Flanagan LB (1996) Effect of changes in water content on photosynthesis, transpiration and discrimination against (CO2)-C-13 and (COO)-18O-16O in Sphagnum and Pleurozium. Oecologia 108:38–46

    Google Scholar 

  • Williams TG, Flanagan IB (1998) Measuring and modelling environmental influences on photosynthetic gas exchange in Sphagnum and Pleurozium. Plant Cell Environ 21:555–564

    CAS  Google Scholar 

  • Wilson JP, Fischer WW (2011) Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport in vascular plants. Geobiology 9:121–130

    CAS  PubMed  Google Scholar 

  • Wilson D, Stock WD, Hedderson F (2001) Historical nitrogen content of bryophyte tissue as an indicator of increased nitrogen deposition in Cape Metrapolitan Area, South Africa. Environ Pollut 157:938–945

    Google Scholar 

  • Winter K, Smith JAC (eds) (1996) Crassulacean acid metabolism. Biochemistry, Ecophysiology and Evolution. Springer, Berlin, pp xxxii–449

    Google Scholar 

  • Woodward FI (1998) Do plants really need stomata? J Exp Bot 49:471–480

    Google Scholar 

  • Wu MY, Zhao YL, Tong JN, Yang RD (2011) New macroalgal fossils of the Kaili Biota in Guizhou Province, China. Sci China Earth Sci 54:93–100

    Google Scholar 

  • Xu ZL (2001) New discoveries of phaeophycean fossils in the Early Cambrian, Haikou, Kunming, Yunnan, Southwest China. Acta Botanica Sinica 43:1072–1076

    Google Scholar 

  • Yang R-D, Mao J-R, Zhang W-H, Jiang L-J, Gao H (2004) Bryophyte-like fossil (Parafunaria sinensis) from Early-Middle Cambrian Kaili Formation of Guizhou Province, China. J Integr Plant Biol 46:180–185

    Google Scholar 

  • Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020

    CAS  PubMed  Google Scholar 

  • Yuan X, Chen Z, Xiao S, Zhou C, Hua H (2011) An early Ediacaran assemblage of morphologically differentiated eukaryotes. Nature 470:390–393

    CAS  PubMed  Google Scholar 

  • Zhang Z, Metzger P, Sachs JP (2007) Biomarker evidence for the co-occurrence of three races (A, B and C) of Botryococcus braunii in El Junco Lake, Galápagos. Organic Geochem 38:1459–1478

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the editors for helpful comments. The University of Dundee is a registered Scottish charity, No SC015096

Author information

Authors and Affiliations

  1. Division of Plant Sciences, University of Dundee at the James Hutton Institute, The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK

    John A. Raven

  2. School of Plant Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    John A. Raven

  3. School of Earth and Ocean Sciences, Cardiff University, Park Place, Cardiff, CF10 3AT, UK

    Dianne Edwards

Authors
  1. John A. Raven
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dianne Edwards
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John A. Raven .

Editor information

Editors and Affiliations

  1. Department of Biology, University of New Mexico, Albuquerque, New Mexico, USA

    David T. Hanson

  2. Department of Biological Sciences, Union College, Schenectady, New York, USA

    Steven K. Rice

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Raven, J.A., Edwards, D. (2014). Photosynthesis in Early Land Plants: Adapting to the Terrestrial Environment. In: Hanson, D., Rice, S. (eds) Photosynthesis in Bryophytes and Early Land Plants. Advances in Photosynthesis and Respiration, vol 37. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6988-5_3

Download citation

Publish with us

Policies and ethics

Search

Navigation