Summary
Terrestrialization of planet Earth likely began more than a billion years ago with the colonization of land by bacteria, followed by eukaryotic algae much like those occupying modern soils and shallow freshwaters and the earliest embryophytes, close relatives of modern bryophytes. Colonization of land by algae and the first plants was prerequisite to the development of organic-rich soils that later supported more complex plant communities dominated by vascular plants, and the rise of land animals. Consequently, understanding terrestrialization sheds light on Earth’s early biological carbon cycling processes, which aids our understanding of global biogeochemistry in particular, and planetary science in general.
Comprehending the process and pattern of ancient terrestrialization requires both neontological and paleontological approaches. Molecular phylogenetics provides the necessary scaffold upon which terrestrialization processes can be analyzed by comparing the structures, physiologies, microbiomes, and genomes of earliest-branching lineages of modern liverworts and mosses to those of plants’ closest modern green algal relatives, the streptophyte algae (also known as charophyte algae or charophycean green algae). Such studies reveal that modern bryophytes inherited spore and body desiccation-resistance, degradation-resistant lignin-like phenolic cell wall polymers, and other physiological traits useful in terrestrial habitats from ancestral algae, indicating that such features were also traits of the earliest land plants.
Because modern algae and bryophytes possess degradation-resistant cells or tissues, artificially degrading them for comparison with enigmatic microscopic fossils has been a fruitful way to identify remains of early terrestrial photosynthesizers and thus illuminate terrestrialization patterns. Microfossils cited as evidence for terrestrial cyanobacteria occur beginning more than 1,000 million years ago in the Precambrian, as do probable remains of freshwater and terrestrial eukaryotic algae. Some microfossils obtained from 499 to 511 million year old deposits closely resemble the modern complex streptophyte alga Coleochaete when it has been cultivated subaerially, suggesting that streptophytes were able to photosynthesize on land by the Middle Cambrian. Other microfossils observed in Cambrian and early Middle Ordovician deposits may also be remains of land plants. Remains of early liverwort-like land plants are confidently known from 470 million year old mid-Ordovician deposits, as are possible fossils of early-divergent mosses. Microfossils and macrofossils that have been compared to modern liverwort and moss taxa occur in Silurian to Devonian deposits laid down before and during the first major diversification of the vascular plants in the Late Silurian to Early Devonian, 407–418 million years ago. Such evidence, together with molecular phylogenies and clock analyses, demonstrates that bryophytes and streptophyte algal relatives were the dominant eukaryotic photosynthesizers on land from about 500–400 million years ago, prior to and during the earliest stages of vascular plant evolution.
Because bryophytes and streptophyte algae produce degradation-resistant carbon that can be sequestered, thereby reducing atmospheric carbon dioxide levels, models suggest that they had significant impacts on Earth’s carbon cycle for at least 40 million years and perhaps more than 100 million years. We can thus predict that other Earth-like, habitable-zone planets may likewise experience long periods during which organisms equivalent to earthly terrestrial streptophyte algae and bryophytes impact planetary biogeochemistry.
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References
Adams DG, Duggan PS (2008) Cyanobacteria-bryophyte symbioses. J Exp Bot 59:1047–1058
Alboresi A, Caffarri S, Nogue F, Bassi R, Morosinotto T (2008) In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One 3:e2033
Arancibia-Avila P, Coleman JR, Russin WA, Wilcox LW, Graham LE (2000) Effects of pH on cell morphology and carbonic anhydrase activity and localization in bloom-forming Mougeotia (Chlorophyta, Charophyceae). Can J Bot 78:1206–1214
Arancibia-Avila PA, Coleman JR, Russin WA, Graham JM, Graham LE (2001) Carbonic anhydrase localization in charophycean green algae: ecological and evolutionary significance. Int J Plant Sci 162:127–135
Baraffe I, Chabrier G, Barman T (2010) The physical properties of extra-solar planets. Rep Prog Phys 73:1–30
Basile DV, Slade LL, Corpe WA (1969) An association between a bacterium and a liverwort, Scapania nemorosa. J Torrey Bot Soc 96:711–714
Basilier K (1980) Fixation and uptake of nitrogen in Sphagnum blue-green algal associations. Oikos 34:239–242
Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004
Berner RA (1997) The rise of land plants and their effect on weathering and CO2. Science 276:544–546
Bidartondo MI, Duckett JG (2010) Conservative ecological and evolutionary patterns in liverwort-fungal symbioses. Proc R Soc B Biol Sci 277:485–492
Bidartondo MI, Bruns TD, Weiss M, Sérgio C, Read DJ (2002) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proc R Soc Biol Sci Ser B 270:835–842
Bonfante P, Selosse M-A (2010) A glimpse into the past of land plants and of their mycorrhizal affairs: from fossils to evo-devo. New Phytol 186:267–270
Brasier MD (2009) Darwin’s lost world: the hidden history of animal life. Oxford University Press, Oxford
Brook AJ, Williamson DB (1998) The survival of desmids on the drying mud of a small lake. In: Round FE (ed) Algae and the aquatic environment. BioPress, Bristol, pp 185–196
Brown RC, Lemmon BE (2011) Spores before sporophytes: hypothesizing the origin of sporogenesis at the algal-plant transition. New Phytol 190:875–881
Büdel B, Darienko T, Deutschewitz K, Dojani S, Friedl T, Mohr KI, Salisch M, Reisser R, Weber B (2009) Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency. Microb Ecol 57:229–247
Chen Y, Dumont MG, McNamara NP, Chamberlain PM, Bodrossy L, Stralis-Pavese N, Murrell JC (2008) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PFLA analyses. Environ Microb 10:446–459
Clarke JT, Warnock RCM, Donoghue PCJ (2011) Establishing a time-scale for plant evolution. New Phytol 192:266–301
Cockell CS, McKay CP, Warren-Rhodes K, Horneck G (2008) Ultraviolet radiation-induced limitation to epilithic microbial growth in arid deserts – dosimetric experiments in the hyperarid core of the Atacama desert. J Photochem Photobiol B 90:79–87
Costa J-L, Paulsrud P, Rikkinen J, Lindblad P (2001) Genetic diversity of Nostoc symbionts endophytically associated with two bryophyte species. Appl Environ Microbiol 67:4393–4396
Crandall-Stotler BJ, Forrest L, Stotler RE (2005) Evolutionary trends in the simple thalloid liverworts (Marchantiophyta, Junnermanniopsida subclass Metzgeriidae). Taxon 54:299–316
Dedysh SN, Khmelenina VN, Suzina NE, Trotsenko YA, Semrau JD, Liesack W, Tiedje JM (2002) Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int J Syst Evol Microbiol 52:251–261
Dedysh SN, Pankratov TA, Belova SE, Kulichevskaya IS, Liesack W (2006) Phylogenetic analysis and in situ identification of bacteria community composition in an acidic Sphagnum peat bog. Appl Environ Microbiol 72:2110–2117
Delwiche CF, Graham LE, Thomson N (1989) Lignin-like compounds and sporopollenin in Coleochaete, an algal model for land plant ancestry. Science 245:399–401
Dombrovska O, Qiu Y-L (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 32:246–263
Duckett JG, Carafa A, Ligrone R (2006) A highly-differentiated glomeromycotean association with the mucilage-secreting, primitive antipodean liverwort Treubia (Treubiaceae): clues to the origins of mycorrhizas. Am J Bot 93:797–813
Edwards D, Wellman CH, Axe L (1999) Tetrads in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland. Bot J Linn Soc 130:111–115
Elster JD, Peter D, L’ubomir K, Lucia V, Katarina Š, Antonio BP (2008) Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia 63:843–851
Espiñeira JM, Uzal EN, Gómez Ros LV, Carrión JS, Merino F, Ros Barceló A, Pomar F (2010) Distribution of lignin monomers and the evolution of lignification among lower plants. Plant Biol 13:59–68
Finet C, Timme RE, Delwiche CF, Marlétaz F (2010) Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr Biol 20:1–6
Fisher MM, Wilcox LW (1996) Desmid-bacterial associations in Sphagnum-dominated Wisconsin peatlands. J Phycol 32:543–549
Fisher MM, Wilcox LW, Graham LE (1998) Molecular characterization of epiphytic bacterial communities on charophycean green algae. Appl Environ Microbiol 64:4384–4389
Flechtner VR, Johansen JR, Belnap J (2008) The biological soil crusts of the San Nicolas Island: enigmatic algae from a geographically isolated ecosystem. West N Am Nat 68:405–436
Forrest LL, Davis EC, Long DG, Crandall-Stotler BJ, Clark A, Hollingsworth ML (2006) Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. Bryologist 109:304–334
Gensel PG (2008) The earliest land plants. Annu Rev Ecol Evol Syst 39:459–477
Gensel PG, Johnson NG, Strother PK (1991) Early land plant debris (Hooker’s “waifs and strays”?). Palaios 5:520–547
Gentili F, Nilsson M-C, Zackrisson O, DeLuca TH, Sellstedt A (2005) Physiological and molecular diversity of feather moss associative N2-fixing cyanobacteria. J Exp Bot 56:3121–3127
Graham LE (1993) The origin of land plants. Wiley, New York
Graham LE, Gray J (2001) The origin, morphology and ecophysiology of early embryophytes: neontological and palaeontological perspectives. In: Gensel P, Edwards D (eds) Plants invade the land. Columbia University Press, New York, pp 140–156
Graham LE, Graham JM, Russin WA, Chesnick JM (1994) Occurrence and phylogenetic significance of glucose utilization by charophycean algae: glucose enhancement of growth in Coleochaete orbicularis. Am J Bot 81:423–432
Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci USA 97:4535–4540
Graham LE, Kodner RG, Fisher MM, Graham JM, Wilcox LW, Hackney JM, Obst J, Bilkey PC, Hanson DT, Cook ME (2004a) Early land plant adaptations to terrestrial stress: a focus on phenolics. In: Hemsley A, Poole I (eds) Evolution of plant physiology. Academic, New York, pp 155–170
Graham LE, Wilcox LW, Cook ME, Gensel PG (2004b) Resistant tissues of marchantioid liverworts resemble enigmatic Early Paleozoic microfossils. Proc Natl Acad Sci USA 101:11025–11029
Graham LE, Graham JM, Wilcox LW (2009) Algae. Benjamin Cummings/Pearson, San Francisco
Graham LE, Kim E, Arancibia-Avila P, Graham JM, Wilcox LW (2010a) Evolutionary and ecophysiological significance of sugar utilization by the peatmoss Sphagnum compactum (Sphagnaceae) and the common charophycean associates Cylindrocystis brebissonii and Mougeotia sp. (Zygnemataceae). Am J Bot 97:1485–1491
Graham LE, Cook ME, Hanson DT, Pigg KB, Graham JM (2010b) Structural, physiological, and stable carbon isotopic evidence that the enigmatic Paleozoic fossil Prototaxites formed from rolled liverwort mats. Am J Bot 97:1–8
Graham LE, Cook ME, Hanson DT, Pigg KB, Graham JM (2010c) Rolled liverwort mats explain major Prototaxites features: response to commentaries. Am J Bot 97:1079–1086
Graham LE, Arancibia-Avila P, Taylor WA, Strother PK, Cook ME (2012) Aeroterrestrial Coleochaete (Streptophyta, Coleochaetales) models early plant adaptation to land. Am J Bot 99:130–144
Gray J (1985) The microfossil record of early land plants: advances in understanding of early terrestrialization, 1970–1984. Philos Trans R Soc Lond B Biol Sci 309:167–195
Gray J, Massa D, Boucot AJ (1982) Caradocian microfossils from Libya. Geology 10:197–201
Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1255
Gunnison D, Alexander M (1975a) Resistance and susceptibility to decomposition by natural microbial communities. Limnol Oceanogr 20:64–70
Gunnison D, Alexander M (1975b) Basis for the resistance of several algae to microbial decomposition. Appl Microbiol Biotechnol 29:729–738
Hanson DT, Swanson S, Graham LE, Sharkey TD (1999) Evolutionary significance of isoprene emission from mosses. Am J Bot 86:634–639
Hedges SB, Battistuzzi U, Blair JE (2006) Chapter 7. Molecular timescale of evolution in the Proterozoic. In: Xiao S, Kaufman AJ (eds) Neoproterozoic geology and paleobiology. Springer, New York
Hernick LVA, 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
Holtzinger A, Tschaikner A, Remias D (2010) Cytoarchitecture of the desiccation-tolerant green alga Zygogonium erecitorum. Protoplasma 243:15–24
Horodyski RJ, Knauth LP (1994) Life on land in the Precambrian. Science 263:494–498
Houle D, Gauthier SB, Paquet S, Planas D, Warren A (2006) Identification of two genera of N2-fixing cyanobacteria growing on three feather moss species in boreal forests of Quebec-Canada. Can J Bot 84:1025–1029
Hu CX, Zhang DL, Huang ZB, Liu YD (2003) The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts. Plant Soil 257:97–111
Hueber FM (1961) Hepaticites devonicus a new fossil liverwort from the Devonian of New York. Ann Mo Bot Gard 48:125–131
Hughes KA, Lawley B (2003) A novel Antarctic microbial endolithic community within gypsum crusts. Environ Microbiol 5:555–565
Jaiswal P, Singh PK, Prasanna R (2008) Cyanobacterial bioactive molecules – an overview of their toxic properties. Can J Microbiol 54:701–717
Kaltenegger L, Selsis F, Fridlund M, Lammer H, Beichman C, Danchi W, Eiroa C, Henning T, Herbst T, Léger A, Liseau R, Lunine J, Paresca F, Penny A, Quirrenbach A, Röttgering H, Schneider J, Stam D, Tinetti G, White GJ (2010) Deciphering spectral fingerprints of habitable exoplanets. Astrobiology 10:89–102
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 46:1187–1197
Kennedy M, Droser M, Mayer LM, Pevear D, Mrofka D (2006) Late Precambrian oxygenation; inception of the clay mineral factory. Science 311:1446–1449
Kirilovsky D (2010) The photoactive orange carotenoid protein and photoprotection in cyanobacteria. In: Hallenbeck PC (ed) Recent advances in phototrophic prokaryotes. Springer, Philadelphia, pp 139–159
Knauth LP, Kennedy MJ (2009) The late Precambrian greening of the earth. Nature 460:728–732
Kodner RB, Graham LE (2001) High-temperature, acid-hydrolyzed remains of Polytrichum (Musci, Polytrichaceae) resemble enigmatic Silurian-Devonian tubular microfossils. Am J Bot 88:462–466
Koziol AG, Borza T, Ishida K-I, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816
Kroken SB, Graham LE, Cook ME (1996) Occurrence and evolutionary significance of resistant cell walls in charophytes and bryophytes. Am J Bot 83:1241–1254
Lakatos M, Bilger W, Büdel B (2001) Carotenoid composition of terrestrial cyanobacteria: response to natural light conditions in open rock habitats in Venezuela. Eur J Phycol 36:367–375
Leiming Y, Xunlai Y (2007) Radiation of Meso-Neoproterozoic and early Cambrian protists inferred from the microfossil record of China. Palaeogeogr Palaeoclimatol Palaeoecol 254:350–361
Leiming Y, Xunlai Y, Fanwei M, Jie H (2005) Protists of the Upper Mesoproterozoic Ruyang group in Shanxi Province, China. Precambrian Res 141:49–66
Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556
Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG (2007) Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am J Bot 94:1756–1777
Luo Z-X, Yuan CX, Meng Q-J, Ji Q (2011) A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476:442–445
Luttge U, Büdel B (2010) Resurrection kinetics of photosynthesis in desiccation-tolerant terrestrial green algae. Plant Biol 12:437–444
Mitchell EAD, Gilbert D, Buttler A, Amblard C, Grosvernier P, Gobat J-M (2003) Structure of microbial communities in Sphagnum peatlands and effect of atmospheric carbon dioxide enrichment. Microb Ecol 46:187–199
Nagao MK, Matsui K, Uemura M (2008) Klebsormidium flaccidum, a streptophyte algae green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ 31:872–875
Nilsson M, Rasmussen U, Bergman B (2006) Cyanobacterial chemotaxis to extracts of host and nonhost plants. FEMS Microbial Ecol 55:382–390
Opelt K, Chobot V, Hadacek F, Schönmann S, Eberl L, Berg G (2007) Investigations of the structure and function of bacterial communities associated with Sphagnum mosses. Environ Microbiol 9:2795–2809
Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10
Potts M (1999) Desiccation tolerance in cyanobacteria. Eur J Phycol 34:319–328
Prave AR (2002) Life on land in the Proterozoic: evidence from the Torridonian rocks of northwest Scotland. Geology 30:811–814
Pressel S, Ligrone R, Duckett JG, Davis EC (2008) A novel ascomycetous endophytic association in the rhizoids of the leafy liverwort family Schistochilaceae (Jungermanniidae, Hepaticopsida). Am J Bot 95:531–541
Qiu Y-L, Cho Y, Cox JC, Palmer JD (1998) The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394:671–674
Qiu Y-L, Li L, Bin W, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J, Estabrook GF, Hendry TA, Taylor DW, Testa CM, Ambros M, Crandall-Stotler B, Duff RJ, Stech M, Frey W, Quandt D, Davis CC (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516
Qiu Y-L, Li L, Wang B, Chen Z, Dombrovska O, Lee J, Kent L, Li R, Jobson RW, Hendry TA, Taylor DW, Testa CM, Ambros M (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168:691–708
Raghoebarsing AA, Smolders AJP, Schmid MC, Riipstra WIC, Wolters-Arts M, Derksen J, Jetten MSM, Schouten S, Damsté S, Lamers LPM, Roelofs JGM, Op den Camp HJM, Strous M (2005) Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436:1153–1156
Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond B Biol Sci 355:815–831
Redeker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921
Redeker D, Kodner R, Graham LE (2002) Palaeoglomus grayi from the Ordovician. Mycotaxon 84:33–37
Rikkinen J, Vertanen V (2008) Genetic diversity in cyanobacterial symbionts of thalloid bryophytes. J Exp Bot 59:1013–1021
Rubinstein CV, Gerrienne P, de la Puente GS, Astini RA, Steemans P (2010) Early Middle Ordovician evidence for land plants in Argentina (Eastern Gondwana). New Phytol 188:365–369
Russell J, Bulman S (2004) The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol 165:567–569
Sanderson MJ (2003) Molecular data from 27 proteins do not support a Precambrian origin of land plants. Am J Bot 90:954–956
Schlesinger WH, Pippen JS, Wallenstein MD, Hofmockel KS, Klepeis DM, Mahall BE (2003) Community composition and photosynthesis by photoautotrophs under quartz pebbles, southern Mohave desert. Ecology 84:3222–3231
Sinha RP, Häder D-P (2007) UV-protectants in cyanobacteria. Plant Sci 174:278–289
Škaloud P (2009) Species composition and diversity of aero-terrestrial algae and cyanobacteria of the Boreč Hill ventaroles. Fottea 9:65–80
Steemans P, Le Hérissé A, Melvin J, Miller MA, Paris F, Verniers J, Wellman CH (2009) Origin and radiation of the earliest vascular land plants. Science 324:353
Steemans P, Lepot K, Marshall CP, Le Hérissé A, Javaux EJ (2010) FTIR characterization of the chemical composition of Silurian miospores (cryptospores and trilete spores) from Gotland, Sweden. Rev Palaeobot Palynol 162:577–590
Strother PK, Al-Hajri S, Traverse A (1996) New evidence for land plants from the lower Middle Ordovician of Saudi Arabia. Geology 24:55–58
Strother PK, Battison L, Brasier MD, Wellman CH (2011) Earth’s earliest non-marine eukaryotes. Nature 473:505–509
Taylor WA (1995) Spores in earliest land plants. Nature 373:391–392
Taylor WA, Strother PK (2009) Ultrastructure, morphology, and topology of Cambrian palynomorphs from the Lone Rock Formation, Wisconsin, USA. Rev Palaeobot Palynol 153:296–309
Timme RE, Bachvaroff TR, Delwiche CF (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS One 7(1):e29696
Tomescu AMF, Rothwell GW, Honeggar R (2009) A new genus and species of filamentous microfossil of cyanobacterial affinity from Early Silurian fluvial environments (lower Massanutten Sandstone, Virginia, USA). Bot J Linn Soc 160:284–289
Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106:395–409
Turmel M, Pombert J-F, Charlebois P, Otis C, Lemieux C (2007) The green algal ancestry of land plants as revealed by the chloroplast genome. Int J Plant Sci 168:679–689
Villarreal JCA, Renzaglia KS (2006) Structure and development of Nostoc strands in Leiosporoceros dussii (Anthocerotophyta): a novel symbiosis in land plants. Am J Bot 93:693–705
Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363
Wang B, Yeun LH, Xue J-Y, Liu Y, Ané J-M, Qiu Y-L (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525
Warren-Rhodes KA, Rhodes KL, Boyle LN, Pointing SB, Chen Y, Liu S, Zhuo P, McKay CP (2007) Cyanobacterial ecology across environmental gradients and spatial scales in China’s hot and cold deserts. FEMS Microbiol Ecol 61:470–482
Wellman CH (2010) The invasion of the land by plants: when and where? New Phytol 188:306–309
Wellman CH, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285
West NJ, Adams DG (1997) Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single field site. Appl Environ Microbiol 63:4479–4484
Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Phillippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11:104–111
Wood AJ (2007) The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts, and mosses. Bryologist 110:163–177
Zackrisson O, DeLuca TH, Gentili F, Sellstedt A, Jäderlund A (2009) Nitrogen fixation in mixed Hylocomium splendens moss communities. Oecologia 160:309–319
Zhang Z (1982) Upper Proterozoic microfossils from the Summer Isles, NW Scotland. Palaeontology 25:443–460
Zimmer A, Lang D, Richardt S, Frank W, Reski R, Rensing SA (2007) Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol Genet Genom 278:393–402
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Sarah Friedrich provided assistance with illustrations. We thank Dr. James Graham and Christopher Cardona-Correa for helpful discussions. Grant support from the US National Science Foundation (NSF) and the United Kingdom Natural Environment Research Council (NERC) is much appreciated.
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Graham, L., Lewis, L.A., Taylor, W., Wellman, C., Cook, M. (2014). Early Terrestrialization: Transition from Algal to Bryophyte Grade. 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_2
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