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Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms

Nature volume 528, pages 551–554 (2015)Cite this article

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Abstract

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.

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Figure 1: Minute embryos with two cotyledon primordia in Early Cretaceous angiosperms.
Figure 2: Cellular preservation of embryos and associated nutrient storage tissue in Early Cretaceous angiosperm seeds.
Figure 3: Minute and broad embryo and associated nutrient storage tissue in an Early Cretaceous seed (taxon 3).
Figure 4: Embryo and nutrient storage tissue of extant Sarcandra (Chloranthaceae).

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Acknowledgements

We thank A. Lindström for assistance with the SRXTM analyses. Research reported here was supported by the Swedish Research Council, the Edward P. Bass Distinguished Visiting Fellowship and by the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement n. 312284 (for CALIPSO) for the SRXTM analyses at the SLS.

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Authors and Affiliations

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

    Else Marie Friis

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

    Else Marie Friis, Peter R. Crane & Kaj Raunsgaard Pedersen

  3. Department of Earth Science, University of Aarhus, Aarhus, DK-8000, Denmark

    Kaj Raunsgaard Pedersen

  4. Swiss Light Source, Paul Scherrer Institute, Villigen PSI, CH-5232, Switzerland

    Marco Stampanoni & Federica Marone

  5. Institute for Biomedical Engineering, ETZ F 85, Swiss Federal Institute of Technology Zurich, Gloriastrasse 35, Zurich, CH-, 8092, Switzerland

    Marco Stampanoni

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  1. Else Marie Friis
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  4. Marco Stampanoni
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  5. Federica Marone
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Contributions

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.

Corresponding author

Correspondence to Else Marie Friis.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Table 1

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. (PDF 129 kb)

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Marie Friis, E., Crane, P., Raunsgaard Pedersen, K. et al. Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms. Nature 528, 551–554 (2015). https://doi.org/10.1038/nature16441

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