Land Plants

  • Roberto Ligrone


Land plants (Embryophyta) appear in the fossil record from about 470 MYA. Phylogenomic analysis favours the Zygnematophyceae (Charophytes) as their closest algal relative. Early land plants probably inherited somatic desiccation tolerance (poikilohydry) from their charophycean ancestor. Major innovations underpinning plant terrestrialization include sporophyte interpolation in an ancestrally haplobiontic cycle and symbiotic association with mycorrhizal fungi. Poikilohydry and a unisporangiate sporophyte permanently dependent on the gametophyte are ancestral traits retained in extant bryophytes. The evolution of a branched, autonomous sporophyte led to the emergence of polysporangiophytes in Mid Silurian. Homeohydry (the control of water loss) and xylem (a lignified water-conducting tissue) gave polysporangiophytes access to a multitude of novel habitats and niches, driving a dramatic increase in the biological diversity and complexity of terrestrial ecosystems. Roots and leaves evolved multiple times during the Devonian. Seed evolution in Late Devonian severed ancestral dependence on liquid water for sexual reproduction. With the assistance of their fungal associates, land plants are powerful geochemical agents. Their diffusion caused a dramatic decline in carbon dioxide concentration and an unprecedented rise of oxygen. By reducing carbon dioxide level, land plants cooled the planet, creating the conditions for the establishment of the current climatic regime. Land plant cover increases local rainfall and is essential for long-term maintenance of climatic conditions favourable to life on continental masses.


  1. Aires T, Marbà N, Cunha RL, Kendrick GA, Walker DI, Serrão EA, Duarte CM, Arnaud-Haond S (2011) Evolutionary history of the seagrass genus Posidonia. Mar Ecol Prog Ser 421:117–130CrossRefGoogle Scholar
  2. Algeo TJ, Scheckler SE (1998) Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events. Philos Trans R Soc B 353:113–130CrossRefGoogle Scholar
  3. Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685–695PubMedCrossRefGoogle Scholar
  4. Ambrose BA (2013) The morphology and development of lycophytes. Annual Plant Reviews 45:91–114Google Scholar
  5. Bargel H et al (2006) Structure/function relationships of the plant cuticle and cuticular waxes: a smart material? Funct Plant Biol 33:893–910CrossRefGoogle Scholar
  6. Bateman RM et al (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292CrossRefGoogle Scholar
  7. Beerling DJ (2005) Leaf evolution: gases, genes and geochemistry. Ann Bot 96:345–352PubMedPubMedCentralCrossRefGoogle Scholar
  8. Beerling DJ (2007) The emerald planet, How plants changed Earth’s history. Oxford University Press, OxfordGoogle Scholar
  9. Beerling DJ, Fleming AJ (2007) Zimmermann’s telome theory of megaphyll leaf evolution: a molecular and cellular critique. Curr Opin Plant Biol 10:4–12PubMedCrossRefGoogle Scholar
  10. Beerling DJ, Royer DL (2011) Convergent Cenozoic CO2 history. Nat Geosci 4:418–420CrossRefGoogle Scholar
  11. Berner RA (2003a) The long-term carbon cycle, fossil fuels and atmospheric composition. Nature 426:323–326CrossRefGoogle Scholar
  12. Berner RA (2003b) The rise of trees and their effects on Paleozoic atmospheric CO2 and O2. Compt Rendus Geosci 335:1173–1177CrossRefGoogle Scholar
  13. Berner RA (2006) GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochim Cosmochim Acta 70:5653–5664CrossRefGoogle Scholar
  14. Berner RA, Kothavala Z (2001) GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. Am J Sci 301:182–204CrossRefGoogle Scholar
  15. Berner RA, VandenBrooks JM, Ward PD (2007) Oxygen and evolution. Science 316:557–558CrossRefGoogle Scholar
  16. Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the earth system, past and present. Curr Opin Plant Biol 13:233–240PubMedCrossRefGoogle Scholar
  17. Bidartondo MI (2005) The evolutionary ecology of myco-heterotrophy. New Phytol 167:335–352PubMedCrossRefGoogle Scholar
  18. Blackwell WH (2003) Two theories of origin of the land-plant sporophyte: which is left standing? Bot Rev 69:125–148CrossRefGoogle Scholar
  19. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. CrossRefPubMedGoogle Scholar
  20. Bowman JL (2013) Walkabout on the long branches of plant evolution. Curr Opin Plant Biol 16:70–77PubMedCrossRefGoogle Scholar
  21. Boyce CK, Knoll AH (2002) Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28:70–100CrossRefGoogle Scholar
  22. Boyce CK, Lee J-E (2011) Could land plant evolution have fed the marine revolution? Paleontol Res 15:100–105CrossRefGoogle Scholar
  23. Boyce CK et al (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Philos Trans R Soc B 276:1771–1776Google Scholar
  24. Brodersen CR, McElrone AJ (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Front Plant Sci 4:108. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Brodribb TJ (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Sci 177:245–251CrossRefGoogle Scholar
  26. Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175–183PubMedCrossRefGoogle Scholar
  27. Brodribb TJ et al (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytol 183:839–847PubMedCrossRefGoogle Scholar
  28. Brodribb TJ, Pittermann J, Coomes DA (2012) Elegance versus speed: examining the competition between conifer and angiosperm trees. Int J Plant Sci 173:673–694CrossRefGoogle Scholar
  29. Brundett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115CrossRefGoogle Scholar
  30. Brunkard JO, Zambryski PC (2016) Plasmodesmata enable multicellularity: new insights into their evolution, biogenesis, and functions in development and immunity. Curr Opin Plant Biol 35:76–83PubMedCrossRefGoogle Scholar
  31. Carlquist S (2012) How wood evolves: a new synthesis. Botany 90:901–940CrossRefGoogle Scholar
  32. Chater CC et al (2011) Regulatory mechanisms controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr Biol 21:1025–1029PubMedCrossRefGoogle Scholar
  33. Chater CC et al (2016) Origin and function of stomata in the moss Physcomitrella patens. Nat Plants 2:16179. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Chater CC et al (2017) Origins and evolution of stomatal development. Plant Physiol 174:624–638PubMedPubMedCentralCrossRefGoogle Scholar
  35. Civàň P et al (2014) Analyses of charophyte chloroplast genomes help characterize the ancestral chloroplast genome of land plants. Genome Biol Evol 6:897–911PubMedPubMedCentralCrossRefGoogle Scholar
  36. Clarke JT et al (2011) Establishing a time-scale for plant evolution. New Phytol 192:266–301PubMedCrossRefGoogle Scholar
  37. Cochard H et al (2010) The effects of sap ionic composition on xylem vulnerability to cavitation. J Exp Bot 61:275–285PubMedCrossRefGoogle Scholar
  38. Cook ME, Graham LE (1998) Structural similarities between surface layers of charophycean algae and bryophytes and the cuticle of vascular plants. Int J Plant Sci 159:780–787CrossRefGoogle Scholar
  39. Cox CJ et al (2014) Conflicting phylogenies for early and plants are caused by composition biases among synonymous substitutions. Syst Biol 63:272–279PubMedPubMedCentralCrossRefGoogle Scholar
  40. Crane PR, Kenrick P (1997) Diverted development of reproductive organs: a source of morphological innovation in land plants. Plant Syst Evol 206:161–174CrossRefGoogle Scholar
  41. de Vries J, Archibald M (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytol. PubMedCrossRefGoogle Scholar
  42. Delaux P-M (2017) Comparative phylogenomics of symbiotic associations. New Phytol 213:89–94PubMedCrossRefGoogle Scholar
  43. Delaux P-M et al (2014) Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 10:e1004487. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Delwiche CF, Cooper ED (2015) The evolutionary origin of a terrestrial flora. Curr Biol 25:R899–R910. CrossRefPubMedGoogle Scholar
  45. Diaz S et al (2016) The global spectrum of plant form and function. Nature 529:167–178PubMedCrossRefGoogle Scholar
  46. Domìnguez E et al (2010) Self-assembly of supramolecular lipid nanoparticles in the formation of plant biopolyester cutin. Mol BioSyst 6:948–950PubMedCrossRefGoogle Scholar
  47. Domozych DS, Popper ZA, Sørensen I (2017) Charophytes: evolutionary giants and emerging model organisms. Front Plant Sci 7:1470. CrossRefGoogle Scholar
  48. Doyle JA (2013) Phylogenetic analyses and morphological innovations in land plants. Annu Plant Rev 45:1–50Google Scholar
  49. Duckett JG, Pressel S (2017) The evolution of the stomatal apparatus: intercellular spaces and sporophyte water relations in bryophytes – two ignored dimensions. Philos Trans R Soc B 373:20160498. CrossRefGoogle Scholar
  50. Ehlers J, Gibbard PL (2007) The extent and chronology of Cenozoic global glaciation. Quat Int 164–165:6–20CrossRefGoogle Scholar
  51. Farrant JM, Moore JP (2011) Programming desiccation tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14:340–345PubMedCrossRefGoogle Scholar
  52. Fernàndez V et al (2016) Cuticle structure in relation to chemical composition: re-assessing the prevailing model. Front Plant Sci. 31
  53. Field KJ et al (2015) Symbiotic options for the conquest of land. Trends Ecol Evol 30:477–486PubMedCrossRefGoogle Scholar
  54. Fletcher BJ et al (2006) BRYOCARB: a process-based model of thallose liverwort carbon isotope fractionation in response to CO2, O2, light and temperature. Geochim Cosmochim Acta 70:5676–5691CrossRefGoogle Scholar
  55. Floyd SK, Bowman JL (2006) Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Curr Biol 16:1911–1917PubMedCrossRefGoogle Scholar
  56. Franks PJ, Beerling DJ (2009) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7:227–236PubMedCrossRefGoogle Scholar
  57. Goffinet B, Buck WR (2013) The evolution of body form in bryophytes. Annu Plant Rev 45:51–90Google Scholar
  58. Graham LKE, Wilcox LW (2000) The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Philos Trans R Soc Lond B 355:757–767CrossRefGoogle Scholar
  59. Graham LKE, Wilcox LW (2003) The occurrence and phylogenetic significance of putative placental transfer cells in the green alga Coleochaete. Am J Bot 70:113–120CrossRefGoogle Scholar
  60. Graham LKE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci U S A 97:4535–4540PubMedPubMedCentralCrossRefGoogle Scholar
  61. Graham LKE et al (2012) Aeroterrestrial Coleochaete (Streptophyta, Coleochaetales) models early adaptation to land. Am J Bot 88:1–15Google Scholar
  62. Graham LKE et al (2014) Early Terrestrialization: transition from algal to bryophyte grade. In: Hanson DT, Rice SK (eds) Photosynthesis in bryophytes and early land plants, Advances in photosynthesis and respiration, vol 37. Springer, Dordrecht, pp 9–28CrossRefGoogle Scholar
  63. Haig D (2008) Homologous versus antithetic alternation of generations and the origin of sporophytes. Bot Rev 74:395–418CrossRefGoogle Scholar
  64. Hao S et al (2010) Earliest rooting system and root: shoot ratio from a new Zosterophyllum plant. New Phytol 185:217–225PubMedCrossRefGoogle Scholar
  65. Harrison CJ (2017) Development and genetics in the evolution of land plant body plans. Philos Trans R Soc B 372:20150490. CrossRefGoogle Scholar
  66. Harrison CJ, Morris JL (2017) The origin and early evolution of vascular plant shoots and leaves. Philos Trans R Soc B 373:20160496. CrossRefGoogle Scholar
  67. Haworth M, Elliott-Kingston C, McElwain JC (2011) Stomatal control as a driver of plant evolution. J Exp Bot 62:2419–2423PubMedCrossRefGoogle Scholar
  68. Hetherington AJ, Dolan L (2017) Bilaterally symmetric axes with rhizoids composed the rooting structure of the common ancestor of vascular plants. Philos Trans R Soc Lond B 373:20170042. CrossRefGoogle Scholar
  69. Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front Plant Sci 4:327. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Honkanen S et al (2016) The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr Biol 26:3238–3244PubMedPubMedCentralCrossRefGoogle Scholar
  71. Humphreys CP et al (2010) Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat Commun 1:103. CrossRefPubMedGoogle Scholar
  72. Ishizaki K (2015) Development of schizogenous intercellular spaces in plants. Front Plant Sci 6:497. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419PubMedCrossRefGoogle Scholar
  74. Jeffree CE (2006) The fine structure of the plant cuticle. In: Riederer M, Müller C (eds) Biology of the plant cuticle. Blackwell, Oxford, pp 11–125CrossRefGoogle Scholar
  75. Jones VAS, Dolan L (2012) The evolution of root hairs and rhizoids. Ann Bot 110:205–212PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kenrick P (2017) How land plant life cycles first evolved. Science 358:1538–1539PubMedCrossRefGoogle Scholar
  77. Kenrick P, Crane PR (1991) Water-conducting cells in early fossil land plants: implications for the early evolution of tracheophytes. Bot Gaz 152:335–356CrossRefGoogle Scholar
  78. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39CrossRefGoogle Scholar
  79. Kenrick P, Strullu-Derrien C (2014) The origin and early evolution of roots. Plant Physiol 166:570–580PubMedPubMedCentralCrossRefGoogle Scholar
  80. Kenrick P et al (2012) A timeline for terrestrialization: consequences for the carbon cycle in the Paleozoic. Philos Trans R Soc B 367:519–536CrossRefGoogle Scholar
  81. Kerp H, Trewin NH, Hass H (2004) New gametophytes from the Early Devonian Rhynie Chert. Trans R Soc Edinb 94:411–428CrossRefGoogle Scholar
  82. Landerweert R et al (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol 16:248–254CrossRefGoogle Scholar
  83. Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytol 181:13–34PubMedCrossRefGoogle Scholar
  84. Leliaert F et al (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46CrossRefGoogle Scholar
  85. Lenton TM, Daines SJ (2016) Matworld - the biogeochemical effects of early life on land. New Phytol. PubMedCrossRefGoogle Scholar
  86. Lenton T, Watson A (2011) Revolutions that made the Earth. Oxford University Press, OxfordCrossRefGoogle Scholar
  87. Lenton TM et al (2012) First plants cooled the Ordovician. Nat Geosci 5:86–89CrossRefGoogle Scholar
  88. Ligrone R, Duckett JG, Renzaglia KS (2000) Conducting tissues and phyletic relationships of bryophytes. Philos Trans R Soc Lond B 355:815–831CrossRefGoogle Scholar
  89. Ligrone R et al (2008) Immunocytochemical detection of lignin-related epitopes in cell walls in bryophytes and the charalean alga Nitella. Plant Syst Evol 270:257–272CrossRefGoogle Scholar
  90. Ligrone R, Duckett JG, Renzaglia KS (2012) Major transitions in the evolution of early land plants: a bryological perspective. Ann Bot 109:851–871PubMedPubMedCentralCrossRefGoogle Scholar
  91. Liu Y et al (2014) Mitochondrial phylogenomics of early and plants: mitigating the effects of saturation, compositional heterogeneity, and codon-usage bias. Syst Biol 63:862–878PubMedCrossRefGoogle Scholar
  92. Lucas WJ et al (2013) The plant vascular system: evolution, development and function. J Integr Plant Biol 55:294–388PubMedCrossRefGoogle Scholar
  93. Mackenzie G et al (2015) Sporopollenin, the least known yet toughest natural biopolymer. Front Mater 2:66. CrossRefGoogle Scholar
  94. Magallòn S, Hilu KW (2009) Land plants (Embryophyta). In: Hedge SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 133–137Google Scholar
  95. Martin FM, Uroz S, Barker DG (2017) Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356(6340):eaad4501. CrossRefPubMedGoogle Scholar
  96. McAdam SAM, Brodribb TJ (2012) Stomatal innovation and the rise of seed plants. Ecol Lett 15:1–8CrossRefGoogle Scholar
  97. Merced A, Renzaglia KS (2017) Structure, function and evolution of stomata from a bryological perspective. Bry Div Evo 39:7–20Google Scholar
  98. Mills BJW, Batterman SA, Field KJ (2017) Nutrient acquisition by symbiotic fungi governs Paleozoic climate transition. Philos Trans R Soc Lond B 373:20160503. CrossRefGoogle Scholar
  99. Mitchell RL et al (2016) Mineral weathering and soil development in the earliest land plant ecosystems. Geology 44:1007–1010CrossRefGoogle Scholar
  100. Nardini A, Lo Gullo MA, Salleo S (2011a) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Sci 180:604–611PubMedCrossRefGoogle Scholar
  101. Nardini A, Salleo S, Jansen S (2011b) More than just a vulnerable pipeline: xylem physiology in the light of ion-mediated regulation of plant water transport. J Exp Bot 62:4701–4718PubMedCrossRefGoogle Scholar
  102. Nelsen MP et al (2016) Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proc Natl Acad Sci U S A 113:2442–2447PubMedPubMedCentralCrossRefGoogle Scholar
  103. Niklas KJ (2000) The evolution of plant body plans – a biomechanical perspective. Ann Bot 85:411–438CrossRefGoogle Scholar
  104. Niklas KJ, Kutschera U (2010) The evolution of the land plant life cycle. New Phytol 185:27–41PubMedCrossRefGoogle Scholar
  105. Ogden DE, Sleep NH (2012) Explosive eruption of coal and basalt and the end-Permian mass extinction. Proc Natl Acad Sci USA 109:59–62PubMedCrossRefGoogle Scholar
  106. Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100CrossRefGoogle Scholar
  107. Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats. Integr Comp Biol 45:788–799PubMedCrossRefGoogle Scholar
  108. Pires ND, Dolan L (2012) Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc B 367:508–518CrossRefGoogle Scholar
  109. Porada P et al (2016) High potential for weathering and climate effects of non-vascular vegetation in the Late Ordovician. Nat Commun 7:12113. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Pressel S, Goral T, Duckett JG (2014) Stomatal differentiation and abnormal stomata in hornworts. J Bryol 36:87–103CrossRefGoogle Scholar
  111. Proctor MCF (2000) The bryophyte paradox: tolerance of desiccation, evasion of drought. Plant Ecol 151:41–49CrossRefGoogle Scholar
  112. Proctor MCF et al (2007) Desiccation-tolerance in bryophytes: a review. Bryologist 110:595–621CrossRefGoogle Scholar
  113. Proust H et al (2016) RSL class I genes controlled the development of epidermal structures in the common ancestor of land plants. Curr Biol 26:93–99PubMedPubMedCentralCrossRefGoogle Scholar
  114. Puttick MN et al (2018) The interrelationships of land plants and the nature of the ancestral embryophyte. Curr Biol 28:1–13CrossRefGoogle Scholar
  115. Qiu Y-L (2008) Phylogeny and evolution of charophytic algae and land plants. J Syst Evol 46:287–306Google Scholar
  116. Qiu Y-L et al (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516PubMedCrossRefGoogle Scholar
  117. Qiu Y-L, Taylor AB, McManus HA (2012) Evolution of the life cycle in land plants. J Syst Evol 50:171–194CrossRefGoogle Scholar
  118. Quirk J et al (2012) Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering. Biol Lett 8:1006–1011PubMedPubMedCentralCrossRefGoogle Scholar
  119. Rascio N, La Rocca N (2005) Resurrection plants: the puzzle of surviving extreme vegetative desiccation. Crit Rev Plant Sci 24:209–225CrossRefGoogle Scholar
  120. Raven JA (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Ann Bot 78:137–142CrossRefGoogle Scholar
  121. Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386CrossRefGoogle Scholar
  122. Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52:381–401PubMedCrossRefGoogle Scholar
  123. Read DJ et al (2000) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond B 355:815–831CrossRefGoogle Scholar
  124. Renner S (2009) Gymnosperms. In: Hedge SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 157–160Google Scholar
  125. Rensing SA (2018) Plant evolution: phylogenetic relationships between the earliest land plants. Curr Biol 28:R210–R213. CrossRefPubMedGoogle Scholar
  126. Renzaglia KS et al. (2017) Hornwort stomata: architecture and fate shared with 400-million-year-old fossil plants without leaves. Plant Physiology 174:788–797PubMedPubMedCentralCrossRefGoogle Scholar
  127. Rippin M, Becker B, Holzginer A (2017) Enhanced desiccation tolerance in mature cultures of the streptophytic green alga Zygnema circumcarinatum revealed by transcriptomics. Plant Cell Physiol 58:2067–2084PubMedPubMedCentralCrossRefGoogle Scholar
  128. Roberts AW et al (2004) Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements. Protoplasma 224:217–229PubMedCrossRefGoogle Scholar
  129. Roland JC (1978) Cell wall differentiation and stages involved with intercellular gas space opening. J Cell Sci 32:325–336PubMedGoogle Scholar
  130. Royer DL et al (2004) CO2 as a primary driver of Phanerozoic climate. GSA Today 14:4–10.<4:CAAPDO>2.0.CO;2 CrossRefGoogle Scholar
  131. Ruhfel BR et al (2014) From algae to angiosperms: inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol Biol 14:23. CrossRefPubMedPubMedCentralGoogle Scholar
  132. Sakakibara K et al (2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella but do function in sporophyte development. Evol Dev 10:555–566PubMedCrossRefGoogle Scholar
  133. Sakakibara K et al (2013) KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science 339:1067–1070PubMedCrossRefGoogle Scholar
  134. Schneider H (2013) Evolutionary morphology of ferns (Monilophytes). Annu Plant Rev 45:115–140Google Scholar
  135. Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553PubMedCrossRefGoogle Scholar
  136. Smith R (2011) Lost world. Nature 479:287–289PubMedCrossRefGoogle Scholar
  137. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  138. Sperry JS (2010) Hydraulics of vascular water transport. In: Wojtaszek P (ed) Mechanical integration of plant cells and plants, vol 9. Springer, pp 303–327Google Scholar
  139. Strullu-Derrien C, Paul Kenrick P, Marc-André Selosse MA (2016) Origins of the mycorrhizal symbioses. In: Martin F (ed) Molecular mycorrhizal symbiosis. Wiley, New York, pp 1–20Google Scholar
  140. Taboada-Diego A et al (2014) Hollow pollen shells to enhance drug delivery. Pharmaceutics 6:80–96CrossRefGoogle Scholar
  141. Tam THY, Catarino B, Dolan L (2015) Conserved regulatory mechanism controls the development of cells with rooting functions in land plants. In: Proceedings of the National Academy of Sciences USA E3959-E3968. CrossRefGoogle Scholar
  142. Taylor TN, Kerp H, Hass H (2005) Life history biology of early land plants: deciphering the gametophyte phase. Proc Natl Acad Sci U S A 102:5892–5897PubMedPubMedCentralCrossRefGoogle Scholar
  143. Taylor TN, Taylor EL, Krings M (2009) Paleobotany. The biology and evolution of fossil plants. Academic, LondonGoogle Scholar
  144. Taylor LL et al (2009) Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7:171–191PubMedCrossRefGoogle Scholar
  145. Taylor LL et al (2012) Evaluating the effects of terrestrial ecosystems, climate and carbon dioxide on weathering over geological time: a global-scale process-based approach. Philos Trans R Soc Lond B 367:565–582CrossRefGoogle Scholar
  146. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263PubMedCrossRefGoogle Scholar
  147. Terrer C et al (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74PubMedCrossRefGoogle Scholar
  148. Tomescu AMF (2008) Microphylls, megaphylls and the evolution of leaf development. Trends Plant Sci 14:5–12PubMedCrossRefGoogle Scholar
  149. Tomescu AMF et al (2009) Carbon isotopes support the presence of extensive land floras pre-dating the origin of vascular plants. Palaeogeogr Palaeoclimatol Palaeoecol 283:46–59CrossRefGoogle Scholar
  150. Tomescu AMF et al (2018) Why are bryophytes so rare in the fossil record? A spotlight on taphonomy and fossil preservation. In: Krings M et al (eds) Transformative paleobotany. Academic, London, pp 375–416. CrossRefGoogle Scholar
  151. Tuomela M et al (2000) Biodegradation of lignin in a compost environment: a review. Bioresour Technol 72:169–183CrossRefGoogle Scholar
  152. van der Heijden M et al (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423PubMedCrossRefGoogle Scholar
  153. Venturas MD, Sperry JS, Hacke UG (2017) Plant xylem hydraulics: what we understand, current research, and future challenges. J Integr Plant Biol 59:356–389PubMedCrossRefGoogle Scholar
  154. Voesenek LA et al (2006) How plants cope with complete submergence. New Phytol 170:213–226PubMedCrossRefGoogle Scholar
  155. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363PubMedCrossRefGoogle Scholar
  156. Wang B et al (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 186:514–525PubMedCrossRefGoogle Scholar
  157. Wang Y et al (2013) Plant cell wall lignification and monolignol metabolism. Front Plant Sci 4:220. CrossRefPubMedPubMedCentralGoogle Scholar
  158. Watkins JE et al (2007) Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytol 176:708–717PubMedCrossRefGoogle Scholar
  159. Wellman CH, Strother PK (2015) The terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence. Paleontology 58:601–627CrossRefGoogle Scholar
  160. Wellman CH, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285PubMedCrossRefGoogle Scholar
  161. Weng J-K, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285CrossRefGoogle Scholar
  162. Wickett NJ, Goffinet B (2008) Origin and relationships of the myco-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Bot J Linn Soc 156:1–12CrossRefGoogle Scholar
  163. Wickett NJ et al (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci USA 111:E4859–E4868PubMedCrossRefGoogle Scholar
  164. Willis KJ, McElwain JC (2014) The evolution of plants. Oxford University press, OxfordGoogle Scholar
  165. Wood AJ (2007) The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts, and mosses. Bryologist 110:163–177CrossRefGoogle Scholar
  166. Yeats TH, Rose JKC (2013) The formation and function of plant cuticles. Plant Physiol 163:5–20PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Roberto Ligrone
    • 1
  1. 1.Department of Environmental, Biological and Pharmaceutical Sciences and TechnologiesUniversity of Campania “Luigi Vanvitelli”CasertaItaly

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