Phase-contrast x-ray microtomography links cretaceous seeds with gnetales and bennettitales

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. Access through your

institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 51 print

issues and online access $199.00 per year only $3.90 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to

local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT

BEING VIEWED BY OTHERS FIRST INDISPUTABLE FOSSIL _ILEX_ (AQUIFOLIALES: AQUIFOLIACEAE) FLOWER FOUND IN BALTIC AMBER Article Open access 12 November 2024 A PARASITIC COEVOLUTION SINCE THE

MIOCENE REVEALED BY PHASE-CONTRAST SYNCHROTRON X-RAY MICROTOMOGRAPHY AND THE STUDY OF NATURAL HISTORY COLLECTIONS Article Open access 29 January 2021 MESOZOIC CUPULES AND THE ORIGIN OF THE

ANGIOSPERM SECOND INTEGUMENT Article 26 May 2021 REFERENCES * 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  * Pedersen, K. R., Crane, P. R. & Friis, E. M. Pollen organs and seeds with _Eucommiidites_

pollen. _Grana_ 28, 279–294 (1989) Article  Google Scholar  * 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  * Doyle, J. A. Seed ferns and the origin of angiosperms. _J. Torrey Bot.

Soc._ 133, 169–209 (2006) Article  Google Scholar  * Hilton, J. & Bateman, R. M. Pteridosperms are the backbone of seed-plant phylogeny. _J. Torrey Bot. Soc._ 133, 119–168 (2006) Article

  Google Scholar  * 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  * Donoghue, P. C. J. et al. Synchrotron X-ray tomographic

microscopy of fossil embryos. _Nature_ 442, 680–683 (2006) Article  ADS  CAS  Google Scholar  * 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  * 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  * 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  * 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  * Berridge, E. M. On some points of resemblance between Gnetalean and Bennettitean seeds. _New Phytol._ 10, 140–144 (1911) Article 

Google Scholar  * Pearson, H. H. W. _Gnetales_ (Cambridge Univ. Press, Cambridge, 1929) Google Scholar  * 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  * 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  * Harris, T. M. The fossil flora of

Scoresby Sound East Greenland. Part 3: Caytoniales and Bennettitales. _Medd. Grønl._ 85, 1–133 (1932) Google Scholar  * 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  * Stopes, M. C. New Bennettitean cones from the

British Cretaceous. _Phil. Trans. R Soc. B_ 208, 389–440 (1918) Article  ADS  Google Scholar  * 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  * Crane, P. R. Phylogenetic analysis of seed

plants and the origin of angiosperms. _Ann. Mo. Bot. Gard._ 72, 716–793 (1985) Article  Google Scholar  * Lignier, O. _Végétaux fossiles de Normandie. Structure et affinités du Bennettites

morierei Sap. & Mar. (sp.)_ 1–78 (E. Lanier, Caen, 1894) Google Scholar  * 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  * Arber, E. A. N. & Parkin, J. On the origin of angiosperms. _J. Linn. Soc. Bot._ 38, 29–80

(1907) Article  Google Scholar  * 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  * 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  * Bronnikov, A. V. Reconstruction formulas in phase-contrast tomography. _Opt. Commun._ 171, 239–244 (1999) Article  ADS  CAS

  Google Scholar  * 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  * Weitkamp, T. et al. X-ray phase imaging with a grating interferometer. _Opt. Express_ 13, 6296–6304 (2005) Article  ADS  Google Scholar  *

Bronnikov, A. V. Theory of quantitative phase-contrast computed tomography. _J. Opt. Soc. Am. A_ 19, 472–480 (2002) Article  ADS  Google Scholar  * 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 * Departments of Palaeobotany and Palaeozoology, Swedish Museum of Natural History, SE-104 05

Stockholm, Sweden, Else Marie Friis & Stefan Bengtson * Department of the Geophysical Sciences, University of Chicago, Chicago, Illinois 60637, USA, Peter R. Crane * Department of Earth

Sciences, University of Aarhus, DK-8000 Århus C, Denmark Kaj Raunsgaard Pedersen * Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK Philip C. J. Donoghue * Institute

of Geosciences, Eberhard-Karls-University, D-72076 Tübingen, Germany , Guido W. Grimm * Swiss Light Source, Paul Scherrer Institut, CH-5232 Villigen, Switzerland Marco Stampanoni Authors *

Else Marie Friis View author publications You can also search for this author inPubMed Google Scholar * Peter R. Crane View author publications You can also search for this author inPubMed 

Google Scholar * Kaj Raunsgaard Pedersen View author publications You can also search for this author inPubMed Google Scholar * Stefan Bengtson View author publications You can also search

for this author inPubMed Google Scholar * Philip C. J. Donoghue View author publications You can also search for this author inPubMed Google Scholar * Guido W. Grimm View author publications

You can also search for this author inPubMed Google Scholar * Marco Stampanoni View author publications You can also search for this author inPubMed 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:

08 July 2007 * Accepted: 19 September 2007 * Issue Date: 22 November 2007 * DOI: https://doi.org/10.1038/nature06278 SHARE THIS ARTICLE Anyone you share the following link with will be able

to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing

initiative