Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The origin of a land flora

Abstract

The origin of a land flora fundamentally shifted the course of evolution of life on earth, facilitating terrestrialization of other eukaryotic lineages and altering the planet’s geology, from changing atmospheric and hydrological cycles to transforming continental erosion processes. Despite algal lineages inhabiting the terrestrial environment for a considerable preceding period, they failed to evolve complex multicellularity necessary to conquer the land. About 470 million years ago, one lineage of charophycean alga evolved complex multicellularity via developmental innovations in both haploid and diploid generations and became land plants (embryophytes), which rapidly diversified to dominate most terrestrial habitats. Genome sequences have provided unprecedented insights into the genetic and genomic bases for embryophyte origins, with some embryophyte-specific genes being associated with the evolution of key developmental or physiological attributes, such as meristems, rhizoids and the ability to form mycorrhizal associations. However, based on the fossil record, the evolution of the defining feature of embryophytes, the embryo, and consequently the sporangium that provided a reproductive advantage, may have been most critical in their rise to dominance. The long timeframe and singularity of a land flora were perhaps due to the stepwise assembly of a large constellation of genetic innovations required to conquer the terrestrial environment.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The progressive assembly of the embryophyte genetic toolkit.
Fig. 2: Evolution of embryophyte phytohormone signalling pathways.
Fig. 3: Extant embryophyte relationships and life cycle diversity.
Fig. 4: Geological distribution of fossils affiliated with early embryophyte evolution.
Fig. 5: Speculation on attributes of the ancestral embryophyte.

Similar content being viewed by others

References

  1. Delwiche, C. F. & Cooper, E. D. The evolutionary origin of a terrestrial flora. Curr. Biol. 25, R899–R910 (2015).

    Article  CAS  Google Scholar 

  2. Hofmeister, W. F. B. On the Germination, Development, and Fructification of the Higher Cryptogamia, and on the Fructification of the Coniferae (Ray Society, 1862).

  3. Graham, L. E. The origin of the life-cycle of land plants. Am. Sci. 73, 178–186 (1985).

    Google Scholar 

  4. Brown, R. C. & Lemmon, B. E. Spores before sporophytes- hypothesizing the origin of sporogenesis at the algal–plant transition. New Phytol. 190, 875–881 (2011).

    Article  Google Scholar 

  5. Bower, F. O. On antithetic as distinct from homologous alternation of generations in plants. Ann. Bot. 4, 347–370 (1890).

    Article  Google Scholar 

  6. Bower, F. O. Origin of a Land Flora: A Theory Based on the Facts of Alternation (MacMillan and Co., 1908).

  7. Kenrick, P. Changing expressions: a hypothesis for the origin of the vascular plant life cycle. Phil. Trans. R. Soc. B 373, 20170149 (2018).

    Article  Google Scholar 

  8. Gensel, P. G., Glasspool, I., Gastaldo, R. A., Libertin, M. & Kvaček, J. in Nature through Time Springer Textbooks in Earth Sciences, Geography and Environment (eds Martinetto, E. et al.) 367–398 (Springer, 2020).

  9. Tanabe, Y. et al. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc. Natl Acad. Sci. USA 102, 2436–2441 (2005).

    Article  CAS  Google Scholar 

  10. Floyd, S. K., Zalewski, C. S. & Bowman, J. L. Evolution of class III homeodomain-leucine zipper genes in streptophytes. Genetics 173, 373–388 (2006).

    Article  CAS  Google Scholar 

  11. Cheng, S. et al. Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179, 1057–1067 (2019).

    Article  CAS  Google Scholar 

  12. Hori, K. et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5, 3978 (2014).

    Article  CAS  Google Scholar 

  13. Jiao, C. et al. The genome of the charophyte alga Penium margaritaceum bears footprints of the evolutionary origins of land plants. Cell 181, 1097–1111 (2020).

    Article  CAS  Google Scholar 

  14. Liang, Z. et al. Mesostigma viride genome and transcriptome provide insights into the origin and evolution of Streptophyta. Adv. Sci. 7, 1901850 (2019).

    Article  Google Scholar 

  15. Nishiyama, T. et al. The Chara genome- secondary complexity and implications for plant terrestrialization. Cell 174, 448–464 (2018).

    Article  CAS  Google Scholar 

  16. Timme, R. E., Bachvaroff, T. R. & Delwiche, C. F. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696 (2012).

    Article  CAS  Google Scholar 

  17. Wang, S. et al. Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nat. Plants 6, 95–106 (2019).

    Article  Google Scholar 

  18. Cooper, E. & Delwiche, C. Green algal transcriptomes for phylogenetics and comparative genomics. figshare https://doi.org/10.6084/m9.figshare.1604778 (2016).

  19. Bowman, J. L. et al. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171, 287–304 (2017).

    Article  CAS  Google Scholar 

  20. Zhang, J. et al. The hornwort genome and early land plant evolution. Nat. Plants 6, 107–118 (2020).

    Article  CAS  Google Scholar 

  21. Rensing, S. A. et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64–69 (2008).

    Article  CAS  Google Scholar 

  22. Li, F.-W. et al. Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. Nat. Plants 6, 259–272 (2020).

    Article  CAS  Google Scholar 

  23. Banks, J. A. et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960–963 (2011).

    Article  CAS  Google Scholar 

  24. Cannell, N. et al. Multiple metabolic innovations and losses are associated with major transitions in land plant evolution. Curr. Biol. 30, 1783–1800 (2020).

    Article  CAS  Google Scholar 

  25. Catarino, B., Hetherington, A. J., Emms, D. M., Kelly, S. & Dolan, L. The stepwise increase in the number of transcription factor families in the Precambrian predated the diversification of plants on land. Mol. Biol. Evol. 33, 2815–2819 (2016).

    Article  CAS  Google Scholar 

  26. Wilhelmsson, P. K. I., Mühlich, C., Ullrich, K. K. & Rensing, S. A. Comprehensive genome-wide classification reveals that many plant-specific transcription factors evolved in streptophyte algae. Genome Biol. Evol. 9, 3384–3397 (2017).

    Article  CAS  Google Scholar 

  27. Jin, J. et al. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 45, D1040–D1045 (2017).

    Article  CAS  Google Scholar 

  28. Lehti-Shiu, M. D. & Shiu, S. H. Diversity, classification and function of the plant protein kinase superfamily. Phil. Trans. R. Soc. B 367, 2619–2639 (2012).

    Article  CAS  Google Scholar 

  29. Whitewoods, C. D. et al. CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr. Biol. 28, 2365–2376 (2018).

    Article  CAS  Google Scholar 

  30. Furumizu, C. & Sawa, S. Insight into early diversification of leucine‑rich repeat receptor‑like kinases provided by the sequenced moss and hornwort genomes. Plant Mol. Biol. 107, 337–353 (2021).

    Article  CAS  Google Scholar 

  31. Furumizu, C. et al. The sequenced genomes of nonflowering land plants reveal the innovative evolutionary history of peptide signaling. Plant Cell 33, 2915–2934 (2021).

    Article  Google Scholar 

  32. Bowman, J. L., Flores-Sandoval, E. & Kato, H. On the evolutionary origins of land plant auxin biology. Cold Spring Harb. Perspect. Biol. 13, a040048 (2021).

    Article  CAS  Google Scholar 

  33. Skokan, R. et al. PIN-driven auxin transport emerged early in streptophyte evolution. Nat. Plants 5, 1114–1119 (2019).

    Article  CAS  Google Scholar 

  34. Flores-Sandoval, E. et al. Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. New Phytol. 218, 1612–1630 (2018).

    Article  CAS  Google Scholar 

  35. Mutte, S. K. et al. Origin and evolution of the nuclear auxin response system. eLife 7, e33399 (2018).

    Article  Google Scholar 

  36. Martin-Arevalillo, R. et al. Evolution of the Auxin Response Factors from charophyte ancestors. PLoS Genet. 15, e1008400 (2019).

    Article  CAS  Google Scholar 

  37. Flores-Sandoval, E., Eklund, D. M. & Bowman, J. L. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort Marchantia polymorpha. PLoS Genet. 11, e1005207 (2015).

    Article  Google Scholar 

  38. Kato, H. et al. Auxin-mediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha. PLoS Genet. 11, e1005084 (2015).

    Article  Google Scholar 

  39. Kato, H. et al. The roles of the sole activator-type auxin response factor in pattern formation of Marchantia polymorpha. Plant Cell Physiol. 58, 1642–1651 (2017).

    Article  CAS  Google Scholar 

  40. Lavy, M. et al. Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife 5, e13325 (2016).

    Article  Google Scholar 

  41. Prigge, M. J., Lavy, M., Ashton, N. W. & Estelle, M. Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr. Biol. 20, 1907–1912 (2010).

    Article  CAS  Google Scholar 

  42. Kato, H. et al. Design principles of a minimal auxin response system. Nat. Plants 6, 473–482 (2020).

    Article  CAS  Google Scholar 

  43. Bennett, T. & Leyser, O. in Auxin and Its Role in Plant Development (eds Zažímalová, E. et al.) 3–19 (Springer, 2014).

  44. Stewart, J. L. & Nemhauser, J. L. Do trees grow on money? Auxin as the currency of the cellular economy. Cold Spring Harb. Perspect. Biol. 2, a001420 (2010).

    Article  Google Scholar 

  45. Ohtaka, K., Hori, K., Kanno, Y., Seo, M. & Ohta, H. Primitive auxin response without TIR1 and Aux/IAA in the charophyte alga Klebsormidium nitens. Plant Physiol. 174, 1621–1632 (2017).

    Article  CAS  Google Scholar 

  46. Eklund, D. M. et al. Auxin produced by the indole-3-pyruvate pathway regulates development and gemmae dormancy in the liverwort Marchantia polymorpha. Plant Cell 27, 1650–1669 (2015).

    Article  CAS  Google Scholar 

  47. Delaux, P.-M. & Schornack, S. Plant evolution driven by interactions with symbiotic and pathogenic microbes. Science 371, eaba6605 (2021).

    Article  CAS  Google Scholar 

  48. Monte, I. et al. A single JAZ repressor controls the jasmonate pathway in Marchantia polymorpha. Mol. Plant 12, 185–198 (2019).

    Article  CAS  Google Scholar 

  49. Monte, I. et al. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat. Chem. Biol. 14, 480–488 (2018).

    Article  CAS  Google Scholar 

  50. Peñuelas, M. et al. Jasmonate-related MYC transcription factors are functionally conserved in Marchantia polymorpha. Plant Cell 31, 2491–2509 (2019).

    Article  Google Scholar 

  51. Monte, I. et al. An ancient COI1-independent function for reactive electrophilic oxylipins in thermotolerance. Curr. Biol. 30, 962–971 (2020).

    Article  CAS  Google Scholar 

  52. Takezawa, D., Komatsu, K. & Sakata, Y. ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J. Plant Res. 124, 437–453 (2011).

    Article  CAS  Google Scholar 

  53. de Vries, J., Curtis, B. A., Gould, S. B. & Archibald, J. M. Embryophyte stress signaling evolved in the algal progenitors of land plants. Proc. Natl Acad. Sci. USA 115, E3471–E3480 (2018).

    Article  Google Scholar 

  54. Sun, Y. et al. A ligand-independent origin of abscisic acid perception. Proc. Natl Acad. Sci. USA 116, 24892–24899 (2019).

    Article  CAS  Google Scholar 

  55. Ju, C. et al. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants 1, 14004 (2015).

    Article  CAS  Google Scholar 

  56. Li, D. et al. Ethylene-independent functions of the ethylene precursor ACC in Marchantia polymorpha. Nat. Plants 6, 1335–1344 (2020).

    Article  CAS  Google Scholar 

  57. Katayose, A., Kanda, A., Kubo, Y., Takahashi, T. & Motose, H. Distinct functions of ethylene and ACC in the basal land plant Marchantia polymorpha. Plant Cell Physiol. 62, 858–871 (2021).

    Article  CAS  Google Scholar 

  58. Rashotte, A. M. The evolution of cytokinin signaling and its role in development before Angiosperms. Semin. Cell Dev. Biol. 109, 31–38 (2021).

    Article  CAS  Google Scholar 

  59. Wheeldon, C. D. & Bennett, T. There and back again: an evolutionary perspective on long-distance coordination of plant growth and development. Semin. Cell Dev. Biol. 109, 55–67 (2021).

    Article  CAS  Google Scholar 

  60. Hernández-García, J. et al. Coordination between growth and stress responses by DELLA in the liverwort Marchantia polymorpha. Curr. Biol. 31, 3678–3686 (2021).

    Article  Google Scholar 

  61. Hernández-García, J., Briones-Moreno, A. & Blázquez, M. A. Origin and evolution of gibberellin signaling and metabolism in plants. Semin. Cell Dev. Biol. 109, 46–54 (2021).

    Article  Google Scholar 

  62. Mecchia, M. A. et al. The BES1/BZR1-family transcription factor MpBES1 regulates cell division and differentiation in Marchantia polymorpha. Curr. Biol. 31, 4860–4869 (2021).

    Article  CAS  Google Scholar 

  63. de Vries, S. et al. The evolution of the phenylpropanoid pathway entailed pronounced radiations and divergences of enzyme families. Plant J. 107, 975–1002 (2021).

    Article  Google Scholar 

  64. Albert, N. W. et al. Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. New Phytol. 218, 554–566 (2018).

    Article  CAS  Google Scholar 

  65. Berland, H. et al. Auronidins are a previously unreported class of flavonoid pigments that challenges when anthocyanin biosynthesis evolved in plants. Proc. Natl Acad. Sci. USA 116, 20232–20239 (2019).

    Article  CAS  Google Scholar 

  66. Davies, K. M. et al. The evolution of flavonoid biosynthesis- a bryophyte perspective. Front. Plant Sci. 11, 7 (2020).

    Article  Google Scholar 

  67. Renault, H. et al. A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nat. Commun. 8, 14713 (2017).

    Article  Google Scholar 

  68. Kriegshauser, L. et al. Function of the HYDROXYCINNAMOYL-CoA:SHIKIMATE HYDROXYCINNAMOYL TRANSFERASE is evolutionarily conserved in embryophytes. Plant Cell 33, 1472–1491 (2021).

    Article  Google Scholar 

  69. Kong, L. et al. Evolution of cuticle biosynthetic machinery. Plant Physiol. 184, 1998–2010 (2020).

    Article  CAS  Google Scholar 

  70. Xu, B. et al. The land plant-specific MIXTA-MYB lineage is implicated in the early evolution of the plant cuticle and the colonization of land. New Phytol. 229, 2324–2338 (2021).

    Article  CAS  Google Scholar 

  71. Strullu-Derrien, C., Selosse, M.-A., Kenrick, P. & Martin, F. M. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytol. 220, 1012–1030 (2018).

    Article  Google Scholar 

  72. Delaux, P.-M. et al. Algal ancestor of land plants was preadapted for symbiosis. Proc. Natl Acad. Sci. USA 112, 13390–13395 (2015).

    Article  CAS  Google Scholar 

  73. Kodama, K. et al. An ancestral function of strigolactones as symbiotic rhizosphere signals. Nat. Commun. 13, 3974 (2022).

    Article  CAS  Google Scholar 

  74. Radhakrishnan, G. V. et al. An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages. Nat. Plants 6, 280–289 (2020).

    Article  Google Scholar 

  75. Bowman, J. L., Briginshaw, L. N. & Florent, S. N. Evolution and co-option of developmental regulatory networks in early land plants. Curr. Top. Dev. Biol. 131, 35–53 (2019).

    Article  Google Scholar 

  76. Ligrone, R., Duckett, J. G. & Renzaglia, K. S. Major transitions in the evolution of early land plants: a bryological perspective. Ann. Bot. 109, 851–871 (2012).

    Article  Google Scholar 

  77. Kenrick, P. How plant life cycles first evolved. Science 358, 1538–1539 (2017).

    Article  CAS  Google Scholar 

  78. Mishler, B. D. & Churchill, S. P. Transition to a land flora: phylogenetic relationships of the green algae and bryophytes. Cladistics 1, 305–328 (1985).

    Article  Google Scholar 

  79. Kenrick, P. & Crane, P. R. The Origin and Early Diversification of Land Plants: A Cladistic Study (Smithsonian Institution Press, 1997).

  80. Qiu, Y. L. et al. The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl Acad. Sci. USA 103, 15511–15516 (2006).

    Article  CAS  Google Scholar 

  81. Nishiyama, T. et al. Chloroplast phylogeny indicates that bryophytes are monophyletic. Mol. Biol. Evol. 21, 1813–1819 (2004).

    Article  CAS  Google Scholar 

  82. Puttick, M. N. et al. The interrelationships of land plants and the nature of the ancestral embryophyte. Curr. Biol. 28, 733–745 (2018).

    Article  CAS  Google Scholar 

  83. Wickett, N. J. et al. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl Acad. Sci. USA 111, E4859–E4868 (2014).

    Article  CAS  Google Scholar 

  84. de Sousa, F., Foster, P. G., Donoghue, P. C. J., Schneider, H. & Cox, C. J. Nuclear protein phylogenies support the monophyly of the three bryophyte groups (Bryophyta Schimp). New Phytol. 222, 565–575 (2019).

    Article  Google Scholar 

  85. Bell, D. et al. Organellomic data sets confirm a cryptic consensus on (unrooted) land-plant relationships and provide new insights into bryophyte molecular evolution. Am. J. Bot. 107, 91–115 (2019).

    Article  Google Scholar 

  86. Bowman, J. L., Sakakibara, K., Furumizu, C. & Dierschke, T. Evolution in the cycles of life. Annu. Rev. Genet. 50, 133–154 (2016).

    Article  CAS  Google Scholar 

  87. Haig, D. Homologous versus antithetic alternation of generations and the origin of sporophytes. Bot. Rev. 74, 395–418 (2008).

    Article  Google Scholar 

  88. Schuster, R. M. The Hepaticae and Anthocerotae of North America Vol. I (Columbia Univ. Press, 1966).

  89. Dierschke, T. et al. Gamete expression of TALE class HD genes activates the diploid sporophyte program in Marchantia polymorpha. eLife 10, e57088 (2021).

    Article  CAS  Google Scholar 

  90. Horst, N. A. et al. A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction. Nat. Plants 2, 15209 (2016).

    Article  CAS  Google Scholar 

  91. Sakakibara, K. et al. KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science 339, 1067–1070 (2013).

    Article  CAS  Google Scholar 

  92. Sakakibara, K., Nishiyama, T., Deguchi, H. & Hasebe, M. Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol. Dev. 10, 555–566 (2008).

    Article  CAS  Google Scholar 

  93. Hisanaga, T. et al. Deep evolutionary origin of gamete-directed zygote activation by KNOX/ BELL transcription factors in green plants. eLife 10, e57090 (2021).

    Article  CAS  Google Scholar 

  94. Lee, J.-H., Lin, H., Joo, S. & Goodenough, U. Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133, 829–840 (2008).

    Article  CAS  Google Scholar 

  95. Joo, S. et al. Gene regulatory networks for the haploid-to-diploid transition of Chlamydomonas reinhardtii. Plant Physiol. 175, 314–332 (2017).

    Article  CAS  Google Scholar 

  96. Furumizu, C., Alvarez, J. P., Sakakibara, K. & Bowman, J. L. Antagonistic Roles for KNOX1 and KNOX2genes in patterning the land plant body plan following an ancient gene duplication. PLoS Genet. 11, e1004980 (2015).

    Article  Google Scholar 

  97. Hay, A. & Tsiantis, M. KNOX genes: versatile regulators of plant development and diversity. Development 137, 3153–3165 (2010).

    Article  CAS  Google Scholar 

  98. Wang, S. et al. The Class II KNOX genes KNAT3 and KNAT7 work cooperatively to influence deposition of secondary cell walls that provide mechanical support to Arabidopsis stems. Plant J. 101, 293–309 (2020).

    Article  CAS  Google Scholar 

  99. Ortiz-Ramírez, C. et al. GLUTAMATE RECEPTOR-LIKE channels are essential for chemotaxis and reproduction in mosses. Nature 549, 91–95 (2017).

    Article  Google Scholar 

  100. Mosquna, A. et al. Regulation of stem cell maintenance by the polycomb protein FIE has been conserved during land plant evolution. Development 136, 2433–2444 (2009).

    Article  CAS  Google Scholar 

  101. Okano, Y. et al. A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc. Natl Acad. Sci. USA 106, 16321–16326 (2009).

    Article  CAS  Google Scholar 

  102. Pereman, I. et al. The polycomb group protein CLF emerges as a specific tri-methylase of H3K27 regulating gene expression and development in Physcomitrella patens. Biochim. Biophys. Acta 1859, 860–870 (2016).

    Article  CAS  Google Scholar 

  103. Khanday, I., Skinner, D., Yang, B., Mercier, R. & Sundaresan, V. A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565, 91–95 (2019).

    Article  CAS  Google Scholar 

  104. Knauth, L. P. & Kennedy, M. J. The late Precambrian greening of the Earth. Nature 460, 728–732 (2009).

    Article  CAS  Google Scholar 

  105. Kremer, B., Kaźmierczak, J. & Środoń, J. Cyanobacterial-algal crusts from Late Ediacaran paleosols of the East European Craton. Precambrian Res. 305, 236–246 (2018).

    Article  CAS  Google Scholar 

  106. Wellman, C. H. & Strother, P. K. The terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence. Palaeontology 58, 601–627 (2015).

    Article  Google Scholar 

  107. Berbee, M. L. et al. Genomic and fossil windows into the secret lives of the most ancient fungi. Nat. Rev. Microbiol. 18, 717–730 (2020).

    Article  CAS  Google Scholar 

  108. Strother, P. K. & Beck, J. H. in Pollen and Spores (eds Harley, M. M. et al.) 413–424 (The Royal Botanic Gardens Kew, 2000).

  109. Richardson, J. B. in Subsurface Palynostratigraphy of Northeastern Libya (eds El Amauti, A. et al.) 89–109 (Garyounis Univ. Publ., 1988).

  110. Richardson, J. B., Ford, J. H. & Parker, F. Miospores, correlation and age of some Scottish Lower Old Red Sandstone sediments from the Strathmore region (Fife and Angus). J. Micropalaeontol. 3, 25 (1984).

    Article  Google Scholar 

  111. Edwards, D., Morris, J. L., Richardson, J. B. & Kenrick, P. Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytol. 202, 50–78 (2014).

    Article  Google Scholar 

  112. Strother, P. K. & Taylor, W. A. in Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor (eds Krings, M. et al.) 3–20 (Elsevier, 2018).

  113. Wellman, C. H. The invasion of the land by plants: when and where? New Phytol. 188, 306–309 (2010).

    Article  Google Scholar 

  114. Edwards, D. et al. Piecing together the eophytes – a new group of ancient plants containing cryptospores. New Phytol. 233, 1440–1455 (2022).

    Article  CAS  Google Scholar 

  115. Strother, P. K. & Foster, C. A fossil record of land plant origins from charophyte algae. Science 373, 792–796 (2021).

    Article  CAS  Google Scholar 

  116. Strother, P. K., Wood, G. D., taylor, W. A. & Beck, J. H. Middle Cambrian cryptospores and the origin of land plants. Mem. Assoc. Australas. Palaeontol. 29, 99–113 (2004).

    Google Scholar 

  117. Taylor, W. A. & Strother, P. K. Ultrastructure of some Cambrian palynomorphs from the Bright Angel Shale, Arizona, USA. Rev. Palaeobot. Palynol. 151, 41–50 (2008).

    Article  Google Scholar 

  118. Taylor, W. A., Strother, P. K., Vecoli, M. & Al-Hajri, S. I. Wall ultrastructure of the oldest embryophytic spores: implications for early land plant evolution. Rev. Micropaléontol. 60, 281–288 (2017).

    Article  Google Scholar 

  119. Strother, P. K. Systematics and evolutionary significance of some new cryptospores from the Cambrian of eastern Tennessee, USA. Rev. Palaeobot. Palynol. 227, 28–41 (2016).

    Article  Google Scholar 

  120. Steemans, P., Lepot, K., Marshall, C. P., Le Herisse, A. & Javaux, E. J. FTIR characterisation of the chemical composition of Silurian miospores (cryptospores and trilete spores) from Gotland, Sweden. Rev. Palaeobot. Palynol. 162, 577–590 (2010).

    Article  Google Scholar 

  121. Wellman, C. H., Osterloff, P. L. & Mohiuddin, U. Hepatic characters in the earliest land plants. Nature 425, 282–285 (2003).

    Article  CAS  Google Scholar 

  122. Gray, J. The microfossil record of early land plants - advances in understanding of early terrestrialization, 1970–1984. Phil. Trans. R. Soc. B 309, 167–195 (1985).

    Google Scholar 

  123. Wellman, C. H. & Gray, J. The microfossil record of early land plants. Phil. Trans. R. Soc. B 355, 717–731 (2000).

    Article  CAS  Google Scholar 

  124. Wellman, C. H. Cryptospores from the type area of the caradoc series in southern Britain. Special Pap. Paleontol. 55, 103–136 (1996).

    Google Scholar 

  125. Steemans, P. Miospore evolution from the Ordovician to the Silurian. Rev. Palaeobot. Palynol. 113, 189–196 (2000).

    Article  CAS  Google Scholar 

  126. Morris, J. L. et al. The timescale of early land plant evolution. Proc. Natl Acad. Sci. USA 115, E2274–E2283 (2018).

    Article  CAS  Google Scholar 

  127. Hedges, S. B., Tao, Q., Walker, M. & Kumar, S. Accurate timetrees require accurate calibrations. Proc. Natl Acad. Sci. USA 115, E9510–E9511 (2018).

    Article  CAS  Google Scholar 

  128. Suvorov, A. et al. Widespread introgression across a phylogeny of 155 Drosophila genomes. Curr. Biol. 32, 111–123 (2022).

    Article  CAS  Google Scholar 

  129. Edwards, D., Morrisa, J. L., Axe, L. & Duckett, J. G. Picking up the pieces: new charcoalified plant mesofossils (eophytes) from a Lower Devonian Lagerstӓtte in the Welsh Borderland, UK. Rev. Palaeobot. Palynol. 297, 104567 (2022).

    Article  Google Scholar 

  130. Edwards, D. et al. Earliest record of transfer cells in Lower Devonian plants. New Phytol. 233, 1456–1465 (2022).

    Article  CAS  Google Scholar 

  131. Strother, P. K. Thalloid carbonaceous incrustations and the asynchronous evolution of embryophyte characters during the Early Paleozoic. Int. J. Coal Geol. 83, 154–161 (2010).

    Article  CAS  Google Scholar 

  132. Tomescu, A. M. F., Pratt, L. M., Rothwell, G. W., Strother, P. K. & Nadon, G. C. Carbon isotopes support the presence of extensive land floras pre-dating the origin of vascular plants. Palaeogeogr. Palaeoclimatol. Palaeoecol. 283, 46–59 (2009).

    Article  Google Scholar 

  133. Tomescu, A. M. F. & Rothwell, G. W. Wetlands before tracheophytes: thalloid terrestrial communities of the Early Silurian Passage Creek biota (Virginia). Geol. Soc. Am. Spec. Pap. 399, 41–56 (2006).

    Google Scholar 

  134. Libertín, M., Kvaček, J., Bek, J., Žárský, V. & Štorch, P. Sporophytes of polysporangiate land plants from the early Silurian period may have been photosynthetically autonomous. Nat. Plants 4, 269–271 (2018).

    Article  Google Scholar 

  135. Lang, W. H. On the plant-remains from the Downtonian of England and Wales. Phil. Trans. R. Soc. Lond. B 544, 245–291 (1937).

    Google Scholar 

  136. Gerrienne, P. et al. An exceptional specimen of the early land plant Cooksonia paranensis, and a hypothesis on the life cycle of the earliest eutracheophytes. Rev. Palaeobot. Palynol. 142, 123–130 (2006).

    Article  Google Scholar 

  137. Kotyk, M. E., Basinger, J. F., Gensel, P. G. & de Freitas, T. A. Morphologically complex plant macrofossils from the Late Silurian of Arctic Canada. Am. J. Bot. 89, 1004–1013 (2002).

    Article  Google Scholar 

  138. Matsunaga, K. K. S. & Tomescu, A. M. F. An organismal concept for Sengelia radicans gen. et sp. nov. – morphology and natural history of an Early Devonian lycophyte. Ann. Bot. 119, 1097–1113 (2017).

    Article  Google Scholar 

  139. Noetinger, S., Bippus, A. C. & Tomescu, A. M. F. Palynology of a short sequence of the Lower Devonian Beartooth Butte Formation at Cottonwood Canyon (Wyoming): age, depositional environments and plant diversity. Pap. Palaeontol. 7, 2183–2204 (2021).

    Article  Google Scholar 

  140. Gensel, P. G. The earliest land plants. Annu. Rev. Ecol. Evol. Syst. 39, 349–377 (2008).

    Article  Google Scholar 

  141. Hetherington, A. J. & Dolan, L. Stepwise and independent origins of roots among land plants. Nature 561, 235–238 (2018).

    Article  CAS  Google Scholar 

  142. Bateman, R. M. et al. Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu. Rev. Ecol. Syst. 29, 263–292 (1998).

    Article  Google Scholar 

  143. Kerp, H., Trewin, N. H. & Hass, H. New gametophytes from the Early Devonian Rhynie Chert. Trans. R. Soc. Edinb. Earth Sci. 94, 411–428 (2004).

    Article  Google Scholar 

  144. Remy, W., Gensel, P. G. & Hass, H. The gametophyte generation of some Early Devonian land plants. Int. J. Plant Sci. 154, 35–58 (1993).

    Article  Google Scholar 

  145. Taylor, T. N., Kerp, H. & Hass, H. Life history biology of early land plants: deciphering the gametophyte phase. Proc. Natl Acad. Sci. USA 102, 5892–5897 (2005).

    Article  CAS  Google Scholar 

  146. Gerrienne, P. & Gonez, P. 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 (2011).

    Article  Google Scholar 

  147. Remy, W., Taylor, T. N., Hass, H. & Kerp, H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl Acad. Sci. USA 91, 11841–11843 (1994).

    Article  CAS  Google Scholar 

  148. Strullu-Derrien, C. et al. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. New Phytol. 203, 964–979 (2014).

    Article  Google Scholar 

  149. Tomescu, A. M. F., Bomfleur, B., Bippus, A. C. & Savoretti, M. A. in Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor (eds Krings, M. et al.) 375–416 (Elsevier, 2018).

  150. Andrews, H. N. Jr. Notes on Belgian specimens of Sporogonites. Palaeobotanist 7, 85–89 (1960).

    Google Scholar 

  151. Gess, R. W. & Prestianni, C. An early Devonian flora from the Baviaanskloof Formation (Table Mountain Group) of South Africa. Sci. Rep. 11, 11859 (2021).

    Article  Google Scholar 

  152. Oostendorp, C. The Bryophytes of Paleozoic and the Mesozoic. Bryophyt. Bibl. 34, 1–110 (1987).

    Google Scholar 

  153. Hernick, L. V., Landing, E. & Bartowski, K. E. Earth’s oldest liverworts - Metzgeriothallus sharonae sp. nov. from the Middle Devonian (Givetian) of eastern New York, USA. Rev. Palaeobot. Palynol. 148, 154–162 (2008).

    Article  Google Scholar 

  154. Drinnan, A. N. & Chambers, T. C. Flora of the Lower Cretaceous Koonwarra Fossil Bed (Korumburra Group), South Gippsland, Victoria. Mem. Assoc. Australas. Palaeontol. 3, 1–77 (1986).

    Google Scholar 

  155. Hübers, M. & Kepr, H. Oldest known mosses discovered in Mississippian (late Visean) strata of Germany. Geology 40, 755–758 (2012).

    Article  Google Scholar 

  156. Taylor, W. A., Gensel, P. G. & Wellman, C. H. Wall ultrastructure in three species of the dispersed spore Emphanisporites from the Early Devonian. Rev. Palaeobot. Palynol. 163, 264–280 (2011).

    Article  Google Scholar 

  157. Graham, L. K. E. & Wilcox, L. W. The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Phil. Trans. R. Soc. B 355, 757–766 (2000).

    Article  CAS  Google Scholar 

  158. Hemsley, A. R. The origin of the land plant sporophyte: an interpolational scenario. Biol. Rev. 69, 263–273 (1994).

    Article  Google Scholar 

  159. Tomescu, A. M. F., Wyatt, S. E., Hasebe, M. & Rothwell, G. W. Early evolution of the vascular plant body plan — the missing mechanisms. Curr. Opin. Plant Biol. 17, 126–136 (2014).

    Article  Google Scholar 

  160. Ligrone, R., Duckett, J. G. & Renzaglia, K. S. The origin of the sporophyte shoot in land plants: a bryological perspective. Ann. Bot. 110, 935–941 (2012).

    Article  Google Scholar 

  161. Kato, M. & Akiyama, H. Interpolation hypothesis for origin of the vegetative sporophyte of land plants. Taxon 54, 443–450 (2005).

    Article  Google Scholar 

  162. Bowman, J. L. Walkabout on the long branches of plant evolution. Curr. Opin. Plant Biol. 16, 70–77 (2013).

    Article  Google Scholar 

  163. Ligrone, R. & Gambardella, R. in Advances in Bryology Vol. 3 (ed. Miller, N. G.) 225–274 (J. Cramer, 1988).

  164. Merced, A. & Renzaglia, K. S. Structure, function and evolution of stomata from a bryological perspective. Bryophyt. Divers. Evol. 39, 7–20 (2017).

    Article  Google Scholar 

  165. McAdam, S. A. M. et al. Stomata: the holey grail of plant evolution. Am. J. Bot. 108, 366–371 (2021).

    Article  Google Scholar 

  166. Clark, J. W. et al. The origin and evolution of stomata. Curr. Biol. 32, R539–R553 (2022).

    Article  CAS  Google Scholar 

  167. Donoghue, P. C. J., Harrison, J., Paps, J. & Schneider, H. The evolutionary emergence of land plants. Curr. Biol. 31, R1281–R1298 (2020).

    Article  Google Scholar 

  168. Haskell, G. Some evolutionary problems concerning the Bryophyta. Bryologist 52, 50–57 (1949).

    Article  Google Scholar 

  169. Scott, D. H. The Evolution of Plants (Williams and Norgate, 1911).

  170. Brodribb, T. J., Carriquí, M., Delzon, S., McAdam, S. A. M. & Holbrook, N. M. Advanced vascular function discovered in a widespread moss. Nat. Plants 6, 273–279 (2020).

    Article  CAS  Google Scholar 

  171. Woudenberg, S., Renema, J., Tomescu, A. M. F., Rybel, B. D. & Weijers, D. Deep origin and gradual evolution of transporting tissues: perspectives from across the land plants. Plant Physiol. https://doi.org/10.1093/plphys/kiac1304 (2022).

  172. Xu, B. et al. Contribution of NAC transcription factors to plant adaptation to land. Science 343, 1505–1508 (2014).

    Article  CAS  Google Scholar 

  173. Bowles, A. M. C., Paps, J. & Bechtold, U. Water-related innovations in land plants evolved by different patterns of gene cooption and novelty. New Phytol. 235, 732–742 (2022).

    Article  CAS  Google Scholar 

  174. Pincher, H. C. A genetical interpretation of alternation of generations. New Phytol. 36, 179–183 (1937).

    Article  Google Scholar 

  175. Allen, C. E. A chromosome difference correlated with sex differences in Sphærocarpos. Science 46, 466–467 (1917).

    Article  CAS  Google Scholar 

  176. Berrie, G. K. Cytology and phylogeny of liverworts. Evolution 17, 347–357 (1963).

    Google Scholar 

  177. Iwasaki, M. et al. Sex determination factor and sex chromosome evolution in a haploid system. Curr. Biol. 31, 5522–5532 (2021).

    Article  CAS  Google Scholar 

  178. Carey, S. B. et al. Gene-rich UV sex chromosomes harbor conserved regulators of sexual development. Sci. Adv. 7, eabh2488 (2021).

    Article  CAS  Google Scholar 

  179. Bateman, R. M. & DiMichele, W. A. Heterospory: the most iterative key innovation in the evolutionary history of the plant kingdom. Biol. Rev. 69, 345–417 (1994).

    Article  Google Scholar 

  180. Graham, L. E. & Gray, J. in Plants Invade the Land. Evolutionary and Environmental Perspectives (eds Gensel, P. G. & Edwards, D.) 140–158 (Columbia Univ. Press, 2001).

  181. Duckett, J. G. & Pressel, S. The evolution of the stomatal apparatus: intercellular spaces and sporophyte water relations in bryophytes—two ignored dimensions. Phil. Trans. R. Soc. Lond. B 373, 20160498 (2017).

    Article  Google Scholar 

  182. Sokoloff, D. D. & Remizowa, M. V. Diversity, development and evolution of archegonia in land plants. Bot. J. Linn. Soc. 195, 380–419 (2020).

    Article  Google Scholar 

  183. Mori, T., Kawai-Toyooka, H., Igawa, T. & Nozaki, H. Gamete dialogs in green lineages. Mol. Plant 8, 1442–1454 (2015).

    Article  CAS  Google Scholar 

  184. Koi, S. et al. An evolutionarily conserved plant RKD factor controls germ cell differentiation. Curr. Biol. 26, 1775–1781 (2016).

    Article  CAS  Google Scholar 

  185. Rövekamp, M., Bowman, J. L. & Grossniklaus, U. Marchantia MpRKD regulates the gametophyte–sporophyte transition by keeping egg cells quiescent in the absence of fertilization. Curr. Biol. 26, 1782–1789 (2016).

    Article  Google Scholar 

  186. Hater, F., Nakel, T. & Groß-Hardt, R. Reproductive multitasking: the female gametophyte. Annu. Rev. Plant Biol. 71, 517–546 (2020).

    Article  CAS  Google Scholar 

  187. Renzaglia, K. S., Duff, R. J., Nickrent, D. L. & Garbary, D. J. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Phil. Trans. R. Soc. B 355, 769–793 (2000).

    Article  CAS  Google Scholar 

  188. Higo, A. et al. Transcription factor DUO1 generated by neofunctionalization is associated with evolution of sperm differentiation in plants. Nat. Commun. 9, 5283 (2018).

    Article  CAS  Google Scholar 

  189. Yamaoka, S. et al. Generative cell specification requires transcription factors evolutionarily conserved in land plants. Curr. Biol. 28, 479–486 (2018).

    Article  CAS  Google Scholar 

  190. Tsuzuki, M. et al. An early arising role of the MicroRNA156-529-SPL module in reproductive development revealed by the liverwort Marchantia polymorpha. Curr. Biol. 29, 3307–3314 (2019).

    Article  CAS  Google Scholar 

  191. Hisanaga, T. et al. A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. EMBO J. 38, e100240 (2019).

    Article  Google Scholar 

  192. Lewis, L. A. in Algae and Cyanobacteria in Extreme Environments Vol. 11 (ed. Seckbach, J.) 569–582 (Springer, 2007).

  193. Holzinger, A. Abiotic stress tolerance of charophyte green algae: new challenges for omics techniques. Front. Plant Sci. 7, 678 (2016).

    Article  Google Scholar 

  194. Harholt, J., Moestrup, Ø. & Peter, U. Why plants were terrestrial from the beginning. Trends Plant Sci. 21, 96–101 (2016).

    Article  CAS  Google Scholar 

  195. Davies, K. M. et al. Evolution and function of red pigmentation in land plants. Ann. Bot. 130, 613–636 (2022).

    Article  Google Scholar 

  196. Kubo, H. et al. Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha. J. Plant Res. 131, 849–864 (2018).

    Article  CAS  Google Scholar 

  197. Lopez-Obando, M., Landberg, K., Sundberg, E. & Thelander, M. Dependence on clade II bHLH transcription factors for nursing of haploid products by tapetal-like cells is conserved between moss sporangia and angiosperm anthers. New Phytol. 235, 718–731 (2022).

    Article  CAS  Google Scholar 

  198. Zheng, X. et al. A study of male fertility control in Medicago truncatula uncovers an evolutionarily conserved recruitment of two tapetal bHLH subfamilies in plant sexual reproduction. New Phytol. 228, 1115–1133 (2020).

    Article  Google Scholar 

  199. Haig, D. Coleochaete and the origin of sporophytes. Am. J. Bot. 102, 417–422 (2015).

    Article  Google Scholar 

  200. Thelander, M., Landberg, K. & Sundberg, E. Minimal auxin sensing levels in vegetative moss stem cells revealed by a ratiometric reporter. New Phytol. 224, 775–788 (2019).

    Article  CAS  Google Scholar 

  201. Pernisová, M. & Vernoux, T. Auxin does the SAMba: auxin signaling in the Shoot Apical Meristem. Cold Spring Harb. Perspect. Biol. 13, a039925 (2021).

    Article  Google Scholar 

  202. Ishida, S. et al. Diminished auxin signaling triggers cellular reprogramming by inducing a regeneration factor in the liverwort Marchantia polymorpha. Plant Cell Physiol. 63, 384–400 (2022).

    Article  CAS  Google Scholar 

  203. Hirakawa, Y. et al. Induction of multichotomous branching by CLAVATA peptide in Marchantia polymorpha. Curr. Biol. 30, 3833–3840 (2020).

    Article  CAS  Google Scholar 

  204. Hirakawa, Y. et al. Control of haploid meristem activity by CLE peptide signaling in Marchantia polymorpha. PLoS Genet. 15, e1007997 (2019).

    Article  CAS  Google Scholar 

  205. Schlegel, J. et al. Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways. eLife 10, e70934 (2021).

    Article  CAS  Google Scholar 

  206. Hirakawa, Y. Evolution of meristem zonation by CLE gene duplication in land plants. Nat. Plants https://doi.org/10.1038/s41477-41022-01199-41477 (2022).

  207. Nemec-Venza, Z. et al. CLAVATA modulates auxin homeostasis and transport to regulate stem cell identity and plant shape in a moss. New Phytol. 234, 149–163 (2022).

    Article  CAS  Google Scholar 

  208. Moreno-Risueno, M. A. et al. Transcriptional control of tissue formation throughout root development. Science 350, 426–430 (2015).

    Article  CAS  Google Scholar 

  209. Aoyama, T. et al. AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139, 3120–3129 (2012).

    Article  CAS  Google Scholar 

  210. Scheres, B. & Krizek, B. A. Coordination of growth in root and shoot apices by AIL/PLT transcription factors. Curr. Opin. Plant Biol. 41, 95–101 (2018).

    Article  CAS  Google Scholar 

  211. Yip, H. K., Floyd, S. K., Sakakibara, K. & Bowman, J. L. Class III HD-Zip activity coordinates leaf development in Physcomitrella patens. Dev. Biol. 419, 184–197 (2016).

    Article  CAS  Google Scholar 

  212. Sakakibara, K. et al. WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. Development 141, 1660–1670 (2014).

    Article  CAS  Google Scholar 

  213. Honkanen, S. et al. The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr. Biol. 26, 3238–3244 (2016).

    Article  CAS  Google Scholar 

  214. Menand, B. et al. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316, 1477–1480 (2007).

    Article  CAS  Google Scholar 

  215. Proust, H. et al. RSL Class I genes controlled the development of epidermal structures in the common ancestor of land plants. Curr. Biol. 26, 93–99 (2016).

    Article  CAS  Google Scholar 

  216. Bonnot, C. et al. Neofunctionalisation of basic helixloophelix proteins occurred when embryophytes colonised the land. New Phytol. 223, 993–1008 (2019).

    Article  CAS  Google Scholar 

  217. Field, K. J., Pressel, S., Duckett, J. G., Rimington, W. R. & Bidartondo, M. I. Symbiotic options for the conquest of land. Trends Ecol. Evol. 30, 477–486 (2015).

    Article  Google Scholar 

  218. Duckett, J. G., Carafa, A. & Ligrone, R. 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 (2006).

    Article  Google Scholar 

  219. Rimington, W. R. et al. Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi. Proc. R. Soc. B 285, 20181600 (2018).

    Article  Google Scholar 

  220. Rimington, W. R., Pressel, S., Duckett, J. G., Field, K. J. & Bidartondo, M. I. Evolution and networks in ancient and widespread symbioses between Mucoromycotina and liverworts. Mycorrhiza 29, 551–565 (2019).

    Article  CAS  Google Scholar 

  221. Taylor, T. N., Remy, W., Hass, H. & Kerp, H. Fossil arbuscular mycorrhizae from the early Devonian. Mycologia 87, 560–573 (1995).

    Article  Google Scholar 

  222. Briginshaw, L. N., Flores-Sandoval, E., Dierschke, T., Alvarez, J. P. & Bowman, J. L. KANADI promotes thallus differentiation and FR-induced gametangiophore formation in the liverwort Marchantia. New Phytol. 234, 1377–1393 (2022).

    Article  CAS  Google Scholar 

  223. Schneider, S. C., García, A., Martín-Closas, C. & Chivas, A. The role of charophytes (Charales) in past and present environments: an overview. Aquat. Bot. 120, 2–6 (2015).

    Article  Google Scholar 

  224. Delwiche, C. F., Karol, K. G., Cimino, M. T. & Sytsma, K. J. Phylogeny of the genus Coleochaete (Coleochaetales, Charophyta) and related taxa inferred by analysis of the chloroplast gene rbcL. J. Phycol. 38, 394–403 (2002).

    Article  CAS  Google Scholar 

  225. Hall, J. D., Karol, K. G., McCourt, R. M. & Delwiche, C. F. Phylogeny of the conjugating green algae based on chloroplast and mitochondrial nucleotide sequence data. J. Phycol. 44, 467–477 (2008).

    Article  CAS  Google Scholar 

  226. Richardson, J. B. Lower Palaeozoic sporomorphs: their stratigraphical distribution and possible affinities. Phil. Trans. R. Soc. Lond. B 309, 201–205 (1985).

    Article  Google Scholar 

  227. Edwards, D., Duckett, J. G. & Richardson, J. B. Hepatic characters in the earliest land plants. Nature 374, 635–636 (1995).

    Article  CAS  Google Scholar 

  228. Taylor, W. A. Spores in earliest land plants. Nature 373, 391–392 (1995).

    Article  CAS  Google Scholar 

  229. Edwards, D., Wellman, C. H. & Axe, L. Tetrads in sporangia and spore masses from the upper Silurian and Lower Devonian of the Welsh Borderland. Bot. J. Linn. Soc. 130, 111–156 (1999).

    Article  Google Scholar 

  230. Strother, P. K., Traverse, A. & Vecoli, M. Cryptospores from the Hanadir Shale Member of the Qasim Formation, Ordovician (Darriwilian) of Saudi Arabia: taxonomy and systematics. Rev. Palaeobot. Palynol. 212, 97–110 (2015).

    Article  Google Scholar 

  231. Salamon, M. A. et al. Putative Late Ordovician land plants. New Phytol. 218, 1305–1309 (2018).

    Article  Google Scholar 

  232. Capel, E., Cleal, C. J., Gerrienne, P., Servais, T. & Cascales-Miñana, B. A factor analysis approach to modelling the early diversification of terrestrial vegetation. Palaeogeogr. Palaeoclimatol. Palaeoecol. 566, 110170 (2021).

    Article  Google Scholar 

  233. Halle, T. G. Notes on the Devonian genus Sporogonites. Sven. Bot. Tidskr. 30, 613–623 (1936).

    Google Scholar 

  234. Lang, W. H. & Cookson, I. C. On a flora, including vascular plants, associated with Monograptus, in rocks of Silurian age, from Victoria, Australia. Phil. Trans. R. Soc. Lond. 224, 421–449 (1935).

    Google Scholar 

  235. Smith, U. & Holloway, D. Baragwanathia longifolia, candidate for Victoria’s state fossil emblem in Museums Victoria Collections https://collections.museumsvictoria.com.au/articles/17145 (2022).

Download references

Acknowledgements

I thank P. Strother and P. Gensel for discussions that influenced some ideas presented; M. Tomescu for insightful comments; P. Strother and J. Ding for images and drawings; T. Yamato and members of my laboratory for comments and discussions; and the 262 days of lockdown in Melbourne that gave me plenty of time to think—any misinterpretations are my own. I apologize to the many authors who I have failed to cite due to space limitations. Research in my laboratory is supported by the Australian Research Council (DP200100225, DP210101423, CE200100015).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John L. Bowman.

Ethics declarations

Competing interests

The author declares no competing interests.

Peer review

Peer review information

Nature Plants thanks Stefan Rensing, Alexandru Tomescu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bowman, J.L. The origin of a land flora. Nat. Plants 8, 1352–1369 (2022). https://doi.org/10.1038/s41477-022-01283-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-022-01283-y

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing