Sporophytes of polysporangiate land plants from the early Silurian period may have been photosynthetically autonomous

Abstract

The colonization of land by vascular plants is an extremely important phase in Earth’s life history. This key evolutionary process is thought to have begun during the Middle Cambrian1 period and culminated in the Silurian/Early Devonian period (interval about 509–393 million years ago (Ma)), and is documented primarily by microfossils (that is, by dispersed spores, phytodebris including fragments of algae, tissues, sporangia and cuticles), tubes and rare megafossils2. A newly recognized fossil cooksonioid plant with in situ spores from the Barrandian area, Czech Republic, is of the highest importance because it represents extremely ancient megafossil evidence of land plant diploid generation: sporophytes (~432 Ma). The robust size of this plant places it among the largest known early polysporangiate land plants and it is probable that it attained adequate size for both aeration and effective photosynthetic competence. This would mean not only that sporophytes were photosynthetically autonomous but also that the they might have been able to sustain a relatively gametophyte-independent existence.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: C.barrandei sp. nov., Loděnice, Špičatý vrch-Barrandovy Jámy, coll. J. Barrande, National Museum, Prague, Czech Republic.
Fig. 2: Comparison of Cooksonia species based on the thickness of the axes.

References

  1. 1.

    Morris, J. L. et al. The timescale of early land plant evolution. Proc. Natl Acad. Sci. USA 115, 2274–2283 (2018).

    Article  Google Scholar 

  2. 2.

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

    Article  Google Scholar 

  3. 3.

    Rubinstein, C. V., Gerrienne, P., de la Punte, G. S., Astini, R. A. & Steemans, P. Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytol. 188, 365–369 (2010).

    CAS  Article  PubMed  Google Scholar 

  4. 4.

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

    CAS  Article  Google Scholar 

  5. 5.

    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  PubMed  Google Scholar 

  6. 6.

    Morris, J. L., Edwards, D., Richardson, J. B., Axe, L. & Davies, K. L. New plant taxa from the Lower Devonian (Lochkovian) of the Welsh Borderland, with a hypothesis on the relationship between hilate and trilete spore producers. Rev. Palaeobot. Palynol. 167, 51–81 (2011).

    Article  Google Scholar 

  7. 7.

    Edwards, D., Feehan, J. & Smith, D. G. A late Wenlock flora from Co. Tipperary, Ireland. Bot. J. Linn. Soc. 86, 19–36 (1983).

    Article  Google Scholar 

  8. 8.

    Taylor, T. N., Taylor, E. L. & Krings, M. Palaeobotany, the Biology and Evolution of Fossil Plants 2nd edn (Elsevier, Amsterdam, 2009).

  9. 9.

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

    Article  Google Scholar 

  10. 10.

    Edwards, D. & Kenrick, P. The early evolution of land plants, from fossils to genomics: a commentary on Lang (1937) ‘on the plant-remains from the Downtonian of England and Wales’. Phil. Trans. R. Soc. B 370, 20140343 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Edwards, D., Banks, H. P., Ciurca, S. J. & Laub, S. R. New Silurian cooksonias from dolostones of north-eastern North America. Bot. J. Linn. Soc. 146, 399–413 (2004).

    Article  Google Scholar 

  12. 12.

    Daber, R. Cooksonia—one of the most ancient psilophytes—widely distributed, but rare. Botanique (Nagpur) 2, 35–40 (1971).

    Google Scholar 

  13. 13.

    Yurina, A. L. The Devonian flora of central Kazakhstan. Mat. Geol. Centr. Kazakh. 8, 14–19 (1969).

    Google Scholar 

  14. 14.

    Gonez, P. & Gerrienne, P. A new definition and a lectotypification of the genus Cooksonia Lang 1937. Int. J. Plant Sci. 171, 199–215 (2010).

    Article  Google Scholar 

  15. 15.

    Edwards, D. Cells and tissues in the vegetative sporophytes of early land plants. New Phytol. 125, 225–247 (1993).

    Article  Google Scholar 

  16. 16.

    Lang, W. H. On the plant-remains from the Dowtonian of England and Wales. Phil. Trans. R. Soc. Lond. B 227, 245–291 (1937).

    Article  Google Scholar 

  17. 17.

    Gonez, P. & Gerrienne, P. Aberlemnia caledonica gen. et comb. nov., a new name for Cooksonia caledonica Edwards 1970. Rev. Palaeobot. Palynol. 163, 64–72 (2010).

    Article  Google Scholar 

  18. 18.

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

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Cox, C. J., Li, B., Foster, P. G., Embley, T. M. & Civáň, P. Conflicting phylogenies for early land plants are caused by composition biases among synonymous substitutions. Syst. Biol. 63, 272–279 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Wickett, N. J. et al. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl Acad. Sci. USA 111, 4859–4868 (2014).

    Article  Google Scholar 

  21. 21.

    Harrison, J. Development and genetics in the evolution of land plant body plans. Phil. Trans. R. Soc. B 372, 20150490 (2016).

    Article  Google Scholar 

  22. 22.

    Thomas, R. J., Stanton, D. S., Longendorfer, D. H. & Farr, M. E. Physiological evaluation of the nutritional autonomy of a hornwort sporophyte. Bot. Gaz. 139, 306–311 (1978).

    CAS  Article  Google Scholar 

  23. 23.

    Proctor, M. C. F. 14C experiments on the nutrition of liverwort sporophytes: Pellia epiphylla, Cephalozia bicuspidata and Lophocolea heterophylla. J. Bryol. 12, 279–285 (1982).

    Article  Google Scholar 

  24. 24.

    Li, F. W., Villarreal, J. C. & Szövényi, P. Hornworts: an overlooked window into carbon-concentrating mechanisms. Trends Plant Sci. 22, 275–277 (2017).

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Čelakovský, L. Ueber die verschiedenen Formen und die Bedeutung des Generationswechsels der Pflanzen. Sitz. Königl. Böhm. Ges. Wiss. Prag. 1874, 21–61 (1874).

    Google Scholar 

  26. 26.

    Bower, F. O. On antithetic as distinct from homologous alternation of generations in plants. Ann. Bot. 4, 374–440 (1890).

    Google Scholar 

  27. 27.

    Stebbins, G. L. & Hill, G. J. C. Did multicellular plants invade the land? Am. Nat. 115, 342–353 (1980).

    Article  Google Scholar 

  28. 28.

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge financial support from the Grant Agency of Czech Republic, First vascular land plants and palynomorphs from the Silurian–Lower Devonian of the Barrandian area, Czech Republic (GAČR 17-102333S). Part of this contribution was also supported by the Research Program of the Institute of Geology AS CR, v.v.i. (RVO67985831). Work in this field by V.Ž. was supported by the EU-PLANTORIGINS-ITN project 238640. Special thanks to D. Edwards, School of Earth and Ocean Sciences, Cardiff University, UK, for valuable discussions.

Author information

Affiliations

Authors

Contributions

M.L., J.K., V.Ž. and J.B. conceived the study. M.L., J.B. and P.Š. performed the laboratory work and analysed the data. J.K., M.L., V.Ž. and J.B. wrote the manuscript.

Corresponding authors

Correspondence to Jiří Kvaček or Viktor Žárský.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Material, Supplementary References, Supplementary Figures 1–4 and Supplementary Table 1.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Libertín, M., Kvaček, J., Bek, J. et al. Sporophytes of polysporangiate land plants from the early Silurian period may have been photosynthetically autonomous. Nature Plants 4, 269–271 (2018). https://doi.org/10.1038/s41477-018-0140-y

Download citation

Further reading