Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms

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The rapid diversification of angiosperms through the Early Cretaceous period, between about 130–100 million years ago, initiated fundamental changes in the composition of terrestrial vegetation and is increasingly well understood on the basis of a wealth of palaeobotanical discoveries over the past four decades1, 2, 3, 4, 5 and their integration with improved knowledge of living angiosperms3, 6. Prevailing hypotheses, based on evidence both from living and from fossil plants, emphasize that the earliest angiosperms were plants of small stature7, 8, 9, 10, 11, 12 with rapid life cycles7, 8, 12, 13 that exploited disturbed habitats3, 9, 11, 13, 14 in open3, 9, 11, 13, 14, or perhaps understorey, conditions15, 16. However, direct palaeontogical data relevant to understanding the seed biology and germination ecology of Early Cretaceous angiosperms are sparse. Here we report the discovery of embryos and their associated nutrient storage tissues in exceptionally well-preserved angiosperm seeds from the Early Cretaceous. Synchrotron radiation X-ray tomographic microscopy of the fossil embryos from many taxa reveals that all were tiny at the time of dispersal. These results support hypotheses based on extant plants that tiny embryos and seed dormancy are basic for angiosperms as a whole17, 18. The minute size of the fossil embryos, and the modest nutrient storage tissues dictated by the overall small seed size, is also consistent with the interpretation that many early angiosperms were opportunistic, early successional colonizers of disturbance-prone habitats2, 15, 16.

At a glance


  1. Minute embryos with two cotyledon primordia in Early Cretaceous angiosperms.
    Figure 1: Minute embryos with two cotyledon primordia in Early Cretaceous angiosperms.

    SRXTM reconstructions of embryos embedded in seeds (a, c, f, h, j) and isolated from seeds (b, d, e, g, i, k). a, b, Exotestal seed and embryo (taxon 1; S170235, Famalicão). ce, Canrightiopsis with seed and embryo (S174005, Famalicão). f, g, Anacostia fruit with seed and embryo (PP54021, Kenilworth). h, i, Appomattoxia with seed and embryo (PP54064, Puddledock). j, k, Fruit with seed and embryo (taxon 2; PP53991, Kenilworth). Scale bars, 500 μm (a, c, f, h, j), 100 μm (b, d, e, g, i, k).

  2. Cellular preservation of embryos and associated nutrient storage tissue in Early Cretaceous angiosperm seeds.
    Figure 2: Cellular preservation of embryos and associated nutrient storage tissue in Early Cretaceous angiosperm seeds.

    Longitudinal orthoslices through SRXTM volumes. a, Apical part of fruit in Fig. 1j (taxon 2) showing embryo and surrounding storage tissue with remains of nutritive bodies (arrow). b, Detail of embryo in a showing the cotyledon primordia (asterisks) and embryo cells with a central body that may represent remains of the nucleus; thin-walled storage tissue is preserved between the cotyledons. c, Details of nutrient storage tissue from an Early Cretaceous exotestal seed (PP53973, Puddledock) with remains of nutritive bodies (arrow). Scale bars, 100 μm.

  3. Minute and broad embryo and associated nutrient storage tissue in an Early Cretaceous seed (taxon 3).
    Figure 3: Minute and broad embryo and associated nutrient storage tissue in an Early Cretaceous seed (taxon 3).

    Longitudinal two-dimensional SRXTM reconstructions of micropylar region of exotesal seed (S174472, Famalicão 25) showing the broad shape and poorly differentiated embryo (arrow). a, Cut volume rendering (between orthoslices 1380–1420) coloured to emphasize the shape and position of embryo. b, Single orthoslice (orthoslice 1420) in same position as in a. Scale bars, 100 μm.

  4. Embryo and nutrient storage tissue of extant Sarcandra (Chloranthaceae).
    Figure 4: Embryo and nutrient storage tissue of extant Sarcandra (Chloranthaceae).

    Two- (a, c) and three-dimensional (b) SRXTM reconstructions. a, Longitudinal orthoslice through seed showing rudimentary embryo with two cotyledon primordia (asterisks) embedded in copious nutrient storage tissue (endosperm); cells in the vicinity of the embryo lack the nutritive bodies that are abundant in other endosperm cells. b, Surface rendering of embryo showing the two small cotyledon primordia. c, Detail of endosperm with nutritive bodies (protein and lipids). Scale bars, 100 μm.


  1. Hughes, N. F. The Enigma of Angiosperm Origins (Cambridge Univ. Press, 1994)
  2. Doyle, J. A. & Hickey, L. J. in Origin and Early Evolution of Angiosperms (ed. Beck, C. B.) 139206 (Columbia Univ. Press, 1976)
  3. Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011)
  4. Dilcher, D. L. Early angiosperm reproduction: an introductory report. Rev. Palaeobot. Palynol. 27, 291328 (1979)
  5. Sun, G. et al. Archaefructaceae, a new basal angiosperm family. Science 296, 899904 (2002)
  6. Doyle, J. A. & Endress, P. K. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. J. Syst. Evol. 48, 135 (2010)
  7. Stebbins, G. L. The probable growth habit of the earliest flowering plants. Ann. Mo. Bot. Gard. 52, 457468 (1965)
  8. Stebbins, G. L. in Origin and Early Evolution of Angiosperms (ed. Beck, C. B.) 300311 (Columbia Univ. Press, 1976)
  9. Taylor, D. W. & Hickey, L. J. in Flowering Plant Origin, Evolution and Phylogeny (eds Taylor, D. W. & Hickey, L. J.) 232266 (Chapman & Hall, 1996)
  10. Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379421 (1998)
  11. Friis, E. M., Pedersen, K. R. & Crane, P. R. Diversity in obscurity: fossil flowers and the early history of angiosperms. Phil. Trans. R. Soc. B 365, 369382 (2010)
  12. Jud, N. A. Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous. Proc. R. Soc. B 282, 20151045 (2015)
  13. Royer, D. L., Miller, I. M., Peppe, D. J. & Hickey, L. J. Leaf economic traits from fossils support a weedy habit for early angiosperms. Am. J. Bot. 97, 438445 (2010)
  14. Taylor, D. W. & Hickey, L. J. An aptian plant with attached leaves and flowers: implications for angiosperm origin. Science 247, 702704 (1990)
  15. Feild, T. S., Arens, A. C., Doyle, J. A., Dawson, T. E. & Donoghue, M. J. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30, 82107 (2004)
  16. Lee, A. P., Upchurch, G., Jr, Murchie, E. H. & Lomax, B. H. Leaf energy balance modelling as a tool to infer habitat preference in the early angiosperms. Proc. R. Soc. B 282, 20143052 (2015)
  17. Forbis, T. A., Floyd, S. K. & de Queiroz, A. The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56, 21122125 (2002)
  18. Baskin, C. C. & Baskin, J. M. Seeds, Ecology, Biogeography, and Evolution of Dormancy and Germination 2nd edn, 11586 (Academic, 2014)
  19. Friis, E. M., Marone, F., Pedersen, K. R., Crane, P. R. & Stampanoni, M. Three-dimensional visualization of fossil flowers, fruits, seeds and other plant remains using synchrotron radiation X-ray tomographic microscopy (SRXTM): new insights into Cretaceous plant diversity. J. Paleontol. 88, 684701 (2014)
  20. Eriksson, O., Friis, E. M., Pedersen, K. R. & Crane, P. R. Seed size and dispersal systems of Early Cretaceous angiosperms from Famalicão, Portugal. Int. J. Plant Sci. 161, 319329 (2000)
  21. Friis, E. M., Grimm, G. W., Mendes, M. M. & Pedersen, K. R. Canrightiopsis, a new Early Cretaceous fossil with Clavatipollenites-type pollen bridge the gap between extinct Canrightia and extant Chloranthaceae. Grana 54, 184212 (2015)
  22. Floyd, S. K. & Friedman, W. E. Evolution of endosperm developmental patterns among basal flowering plants. Int. J. Plant Sci. 161, S57S81 (2000)
  23. Friedman, W. E. & Bachelier, J. B. Seed development in Trimenia (Trimeniaceae) and its bearing on the evolution of embryo-nourishing strategies in early flowering plant lineages. Am. J. Bot. 100, 906915 (2013)
  24. Floyd, S. K. & Friedman, W. E. Developmental evolution of endosperm in basal angiosperms: Evidence from Amborella (Amborellaceae), Nuphar (Nymphaeaceae), and Illicium (Illiciaceae). Plant Syst. Evol. 228, 153169 (2001)
  25. Tobe, H., Jaffre, T. & Raven, P. H. Embryology of Amborella (Amborellaceae): descriptions and polarity of character states. J. Plant Res. 113, 271280 (2000)
  26. Povilus, R. A., Losada, J. M. & Friedman, W. E. Floral biology and ovule and seed ontogeny of Nymphaea thermarum, a water lily at the brink of extinction with potential as a model system for basal angiosperms. Ann. Bot. (Lond.) 115, 211226 (2015)
  27. Baskin, C. C. & Baskin, J. M. A revision of Martin’s seed classification system, with particular reference to his dwarf-seed type. Seed Sci. Res. 17, 1120 (2007)
  28. Friis, E. M., Pedersen, K. R. & Crane, P. R. Appomattoxia ancistrophora gen. et sp. nov., a new Early Cretaceous plant with similarities to Circaeaster and extant Magnoliidae. Am. J. Bot. 82, 933943 (1995)
  29. Eriksson, O., Friis, E. M. & Löfgren, P. Seed size, fruit size, and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. Am. Nat. 156, 4758 (2000)
  30. Moles, A. T. et al. A brief history of seed size. Science 307, 576580 (2005)
  31. Friis, E. M., Crane, P. R. & Pedersen, K. R. Anacostia, a new basal angiosperm from the Early Cretaceous of North America and Portugal with monocolpate/trichotomocolpate pollen. Grana 36, 225244 (1997)
  32. Stampanoni, M. et al. in Developments in X-Ray Tomography V Vol. 6318 (ed Bonse, U.) (International Society for Optical Engineering, 2006)
  33. Marone, F. & Stampanoni, M. Regridding reconstruction algorithm for real-time tomographic imaging. J. Synchrotron Radiat. 19, 10291037 (2012)
  34. Paganin, D., Mayo, S. C., Gureyev, T. E., Miller, P. R. & Wilkins, S. W. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J. Microsc. 206, 3340 (2002)
  35. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676682 (2012)

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Author information


  1. Department of Palaeobiology, Swedish Museum of Natural History, SE-104 05 Stockholm, Sweden

    • Else Marie Friis
  2. Yale School of Forestry and Environmental Studies, 195 Prospect Street, New Haven, Connecticut 06511, USA

    • Else Marie Friis,
    • Peter R. Crane &
    • Kaj Raunsgaard Pedersen
  3. Department of Earth Science, University of Aarhus, DK-8000 Aarhus, Denmark

    • Kaj Raunsgaard Pedersen
  4. Swiss Light Source, Paul Scherrer Institute, CH-5232 Villigen PSI, Switzerland

    • Marco Stampanoni &
    • Federica Marone
  5. Institute for Biomedical Engineering, ETZ F 85, Swiss Federal Institute of Technology Zurich, Gloriastrasse 35, CH-8092 Zurich, Switzerland

    • Marco Stampanoni


E.M.F., K.R.P. and P.R.C. collected and prepared the fossil material for analyses. The measurements and reconstructions were performed by E.M.F. F.M. and M.S. developed the algorithms for the analyses and enhanced the measurements. The paper was jointly prepared by the authors.

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The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Table 1 (129 KB)

    This file contains a list of Early Cretaceous fruits with mature seeds and isolated, mature seeds studied using SRXTM. Currently undescribed seeds are grouped into informal taxa numbered Taxon 1, Taxon 2 etc.

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