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Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms

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).

References

  1. 1

    Hughes, N. F. The Enigma of Angiosperm Origins (Cambridge Univ. Press, 1994)

  2. 2

    Doyle, J. A. & Hickey, L. J. in Origin and Early Evolution of Angiosperms (ed. Beck, C. B. ) 139–206 (Columbia Univ. Press, 1976)

  3. 3

    Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011)

  4. 4

    Dilcher, D. L. Early angiosperm reproduction: an introductory report. Rev. Palaeobot. Palynol. 27, 291–328 (1979)

    Article  Google Scholar 

  5. 5

    Sun, G. et al. Archaefructaceae, a new basal angiosperm family. Science 296, 899–904 (2002)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Doyle, J. A. & Endress, P. K. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. J. Syst. Evol. 48, 1–35 (2010)

    Article  Google Scholar 

  7. 7

    Stebbins, G. L. The probable growth habit of the earliest flowering plants. Ann. Mo. Bot. Gard. 52, 457–468 (1965)

    Article  Google Scholar 

  8. 8

    Stebbins, G. L. in Origin and Early Evolution of Angiosperms (ed. Beck, C. B. ) 300–311 (Columbia Univ. Press, 1976)

  9. 9

    Taylor, D. W. & Hickey, L. J. in Flowering Plant Origin, Evolution and Phylogeny (eds Taylor, D. W. & Hickey, L. J. ) 232–266 (Chapman & Hall, 1996)

  10. 10

    Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379–421 (1998)

    ADS  CAS  Article  Google Scholar 

  11. 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, 369–382 (2010)

    Article  Google Scholar 

  12. 12

    Jud, N. A. Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous. Proc. R. Soc. B 282, 2015 1045 (2015)

    Article  Google Scholar 

  13. 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, 438–445 (2010)

    Article  Google Scholar 

  14. 14

    Taylor, D. W. & Hickey, L. J. An aptian plant with attached leaves and flowers: implications for angiosperm origin. Science 247, 702–704 (1990)

    ADS  CAS  Article  Google Scholar 

  15. 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, 82–107 (2004)

    Article  Google Scholar 

  16. 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)

    Article  Google Scholar 

  17. 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, 2112–2125 (2002)

    Article  Google Scholar 

  18. 18

    Baskin, C. C. & Baskin, J. M. Seeds, Ecology, Biogeography, and Evolution of Dormancy and Germination 2nd edn, 1–1586 (Academic, 2014)

  19. 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, 684–701 (2014)

    Article  Google Scholar 

  20. 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, 319–329 (2000)

    CAS  Article  Google Scholar 

  21. 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, 184–212 (2015)

    Article  Google Scholar 

  22. 22

    Floyd, S. K. & Friedman, W. E. Evolution of endosperm developmental patterns among basal flowering plants. Int. J. Plant Sci. 161, S57–S81 (2000)

    Article  Google Scholar 

  23. 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, 906–915 (2013)

    Article  Google Scholar 

  24. 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, 153–169 (2001)

    Article  Google Scholar 

  25. 25

    Tobe, H., Jaffre, T. & Raven, P. H. Embryology of Amborella (Amborellaceae): descriptions and polarity of character states. J. Plant Res. 113, 271–280 (2000)

    Article  Google Scholar 

  26. 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, 211–226 (2015)

    Article  Google Scholar 

  27. 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, 11–20 (2007)

    Article  Google Scholar 

  28. 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, 933–943 (1995)

    Article  Google Scholar 

  29. 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, 47–58 (2000)

    Article  Google Scholar 

  30. 30

    Moles, A. T. et al. A brief history of seed size. Science 307, 576–580 (2005)

    ADS  CAS  Article  Google Scholar 

  31. 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, 225–244 (1997)

    Article  Google Scholar 

  32. 32

    Stampanoni, M. et al. in Developments in X-Ray Tomography V Vol. 6318 (ed Bonse, U. ) (International Society for Optical Engineering, 2006)

  33. 33

    Marone, F. & Stampanoni, M. Regridding reconstruction algorithm for real-time tomographic imaging. J. Synchrotron Radiat. 19, 1029–1037 (2012)

    CAS  Article  Google Scholar 

  34. 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, 33–40 (2002)

    MathSciNet  CAS  Article  Google Scholar 

  35. 35

    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676–682 (2012)

    CAS  Article  Google Scholar 

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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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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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