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.

Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales

Nature volume 450, pages 549–552 (2007)Cite this article

Abstract

Over the past 25 years the discovery and study of Cretaceous plant mesofossils has yielded diverse and exquisitely preserved fossil flowers that have revolutionized our knowledge of early angiosperms1, but remains of other seed plants in the same mesofossil assemblages2,3 have so far received little attention. These fossils, typically only a few millimetres long, have often been charred in natural fires and preserve both three-dimensional morphology and cellular detail. Here we use phase-contrast-enhanced synchrotron-radiation X-ray tomographic microscopy to clarify the structure of small charcoalified gymnosperm seeds from the Early Cretaceous of Portugal and North America. The new information links these seeds to Gnetales (including Erdtmanithecales, a putatively closely related fossil group2), and to Bennettitales—important extinct Mesozoic seed plants with cycad-like leaves and flower-like reproductive structures. The results suggest that the distinctive seed architecture of Gnetales, Erdtmanithecales and Bennettitales defines a clade containing these taxa. This has significant consequences for hypotheses of seed plant phylogeny by providing support for key elements of the controversial anthophyte hypothesis, which links angiosperms, Bennettitales and Gnetales.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Early Cretaceous (Barremian–Aptian) seed from Catefica, Portugal, with affinities to Gnetales and Bennettitales.
Figure 2: Early Cretaceous (mid-Albian) seed from the Puddledock locality, USA, with affinities to Gnetales and Bennettitales.
Figure 3: The phylogenetic relationships among ‘anthophytes’.

References

  1. Friis, E. M., Pedersen, K. R. & Crane, P. R. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 251–293 (2006)

    Article  Google Scholar 

  2. Pedersen, K. R., Crane, P. R. & Friis, E. M. Pollen organs and seeds with Eucommiidites pollen. Grana 28, 279–294 (1989)

    Article  Google Scholar 

  3. Rydin, C., Pedersen, K. R., Crane, P. R. & Friis, E. M. Former diversity of Ephedra (Gnetales): evidence from Early Cretaceous seeds from Portugal and North America. Ann. Bot. (Lond.) 98, 123–140 (2006)

    Article  Google Scholar 

  4. Doyle, J. A. Seed ferns and the origin of angiosperms. J. Torrey Bot. Soc. 133, 169–209 (2006)

    Article  Google Scholar 

  5. Hilton, J. & Bateman, R. M. Pteridosperms are the backbone of seed-plant phylogeny. J. Torrey Bot. Soc. 133, 119–168 (2006)

    Article  Google Scholar 

  6. Bateman, R. M., Hilton, J. & Rudall, P. J. Morphological and molecular phylogenetic context of the angiosperms: contrasting the ‘top-down’ and ‘bottom-up’ approaches used to infer the likely characteristics of the first flowers. J. Exp. Bot. 57, 3471–3503 (2006)

    Article  CAS  Google Scholar 

  7. Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006)

    Article  ADS  CAS  Google Scholar 

  8. Tafforeau, P. et al. Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl. Phys. A 83, 195–202 (2006)

    Article  ADS  CAS  Google Scholar 

  9. Tafforeau, P., Bentaleb, I., Jaeger, J. J. & Martin, C. Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: Potential implications for palaeoenvironmental isotopic studies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 246, 206–227 (2007)

    Article  Google Scholar 

  10. Friis, E. M., Pedersen, K. R. & Crane, P. R. Angiosperm floral structures from the Early Cretaceous of Portugal. Plant Syst. Evol. 8 (suppl.). 31–49 (1994)

    Google Scholar 

  11. Thoday, M. G. The female Inflorescence and ovules of Gnetum africanum, with notes on Gnetum scandens . Ann. Bot. (Lond.) 25, 1101–1135 (1911)

    Article  Google Scholar 

  12. Berridge, E. M. On some points of resemblance between Gnetalean and Bennettitean seeds. New Phytol. 10, 140–144 (1911)

    Article  Google Scholar 

  13. Pearson, H. H. W. Gnetales (Cambridge Univ. Press, Cambridge, 1929)

    Google Scholar 

  14. Martens, P. Handbuch der Pflanzenanatomie, vol. 12, pt 2:Les gnétophytes (eds Zimmermann, W., Carlquist, S., Ozenda, P. & Wulff, H. D.) (Gebrüder Borntraeger, Berlin, Stuttgart, 1971)

    Google Scholar 

  15. Yang, Y., Geng, B.-Y., Dilcher, D. L., Chen, Z.-D. & Lott, T. A. Morphology and affinities of an Early Cretaceous Ephedra (Ephedraceae) from China. Am. J. Bot. 92, 231–241 (2005)

    Article  Google Scholar 

  16. Harris, T. M. The fossil flora of Scoresby Sound East Greenland. Part 3: Caytoniales and Bennettitales. Medd. Grønl. 85, 1–133 (1932)

    Google Scholar 

  17. Pedersen, K. R., Crane, P. R. & Friis, E. M. Morphology and phylogenetic significance of Vardekloeftia Harris (Bennettitales). Rev. Palaeobot. Palynol. 60, 7–24 (1989)

    Article  Google Scholar 

  18. Stopes, M. C. New Bennettitean cones from the British Cretaceous. Phil. Trans. R Soc. B 208, 389–440 (1918)

    Article  ADS  Google Scholar 

  19. Rothwell, G. W. & Stockey, R. A. Anatomically preserved Cycadeoidea (Cycadeoidaceae), with a reevaluation of systematic characters for the seed cones of Bennettitales. Am. J. Bot. 89, 1447–1458 (2002)

    Article  Google Scholar 

  20. Crane, P. R. Phylogenetic analysis of seed plants and the origin of angiosperms. Ann. Mo. Bot. Gard. 72, 716–793 (1985)

    Article  Google Scholar 

  21. Lignier, O. Végétaux fossiles de Normandie. Structure et affinités du Bennettites morierei Sap. & Mar. (sp.) 1–78 (E. Lanier, Caen, 1894)

    Google Scholar 

  22. Doyle, J. A., Donoghue, M. J. & Zimmer, E. A. Integration of morphological and ribosomal RNA data on the origin of angiosperms. Ann. Mo. Bot. Gard. 81, 419–450 (1994)

    Article  Google Scholar 

  23. Arber, E. A. N. & Parkin, J. On the origin of angiosperms. J. Linn. Soc. Bot. 38, 29–80 (1907)

    Article  Google Scholar 

  24. Burleigh, J. G. & Mathews, S. Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. Am. J. Bot. 91, 1599–1613 (2004)

    Article  CAS  Google Scholar 

  25. Groso, A., Abela, R. & Stampanoni, M. Implementation of a fast method for high resolution phase contrast tomography. Opt. Express 14, 8103–8110 (2006)

    Article  ADS  CAS  Google Scholar 

  26. Bronnikov, A. V. Reconstruction formulas in phase-contrast tomography. Opt. Commun. 171, 239–244 (1999)

    Article  ADS  CAS  Google Scholar 

  27. Cloetens, P. et al. Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation X rays. Appl. Phys. Lett. 75, 2912–2914 (1999)

    Article  ADS  CAS  Google Scholar 

  28. Weitkamp, T. et al. X-ray phase imaging with a grating interferometer. Opt. Express 13, 6296–6304 (2005)

    Article  ADS  Google Scholar 

  29. Bronnikov, A. V. Theory of quantitative phase-contrast computed tomography. J. Opt. Soc. Am. A 19, 472–480 (2002)

    Article  ADS  Google Scholar 

  30. Gureyev, T. E., Paganin, D. M., Myers, G. R., Nesterets, Y. I. & Wilkins, S. W. Phase-and-amplitude computer tomography. Appl. Phys. Lett. 89, 034102–1–034102-3 (2006)

    Article  ADS  Google Scholar 

Download references

Acknowledgements

We thank F. Marone of the Swiss Light Source for valuable help in setting up the software on the cluster, and T. Huldtgren and N. J. Gostling for help with data analyses. We also thank the Natural History Museum, London, for the loan of petrified specimens, J.-P. Rioult for information on the Lignier fossils, and J. Hilton for helpful suggestions. This study was funded by the Swiss Light Source (P.C.J.D. and S.B.), European Union FP6, as well as by grants from the Swedish Research Council (E.M.F.), the Carlsberg Foundations (K.R.P. and E.M.F.) and the National Science Foundation (P.R.C.).

Author information

Authors and Affiliations

  1. Departments of Palaeobotany and Palaeozoology, Swedish Museum of Natural History, SE-104 05 Stockholm, Sweden,

    Else Marie Friis & Stefan Bengtson

  2. Department of the Geophysical Sciences, University of Chicago, Chicago, Illinois 60637, USA,

    Peter R. Crane

  3. Department of Earth Sciences, University of Aarhus, DK-8000 Århus C, Denmark

    Kaj Raunsgaard Pedersen

  4. Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK

    Philip C. J. Donoghue

  5. Institute of Geosciences, Eberhard-Karls-University, D-72076 Tübingen, Germany ,

    Guido W. Grimm

  6. Swiss Light Source, Paul Scherrer Institut, CH-5232 Villigen, Switzerland

    Marco Stampanoni

Authors
  1. Else Marie Friis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter R. Crane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kaj Raunsgaard Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Bengtson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philip C. J. Donoghue
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guido W. Grimm
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marco Stampanoni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Else Marie Friis or Marco Stampanoni.

Supplementary information

Supplementary Information

The file contains Supplementary Notes, Supplementary Figures S1-S2 with Legends and Supplementary Tables 1-3. Supplementary Notes include supporting data for the charcoalified fossils; anatomical comparison between the charcoalified seeds and extinct Bennettitales; cladistic analysis expanding the Hilton and Bateman data matrix and additional references. (PDF 1884 kb)

Supplementary Video 1

The file contains Supplementary Video 1 with the reconstructed slice data for specimen S153152 showing transverse sections. (MOV 42932 kb)

Supplementary Video 2

The file contains Supplementary Video 2 with the reconstructed slice data for specimen S153152 showing longitudinal sections. (MOV 30111 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Friis, E., Crane, P., Pedersen, K. et al. Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450, 549–552 (2007). https://doi.org/10.1038/nature06278

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06278

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced 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