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Stepwise and independent origins of roots among land plants

Naturevolume 561pages235238 (2018) | Download Citation

Abstract

Roots are one of the three fundamental organ systems of vascular plants1, and have roles in anchorage, symbiosis, and nutrient and water uptake2,3,4. However, the fragmentary nature of the fossil record obscures the origins of roots and makes it difficult to identify when the sole defining characteristic of extant roots—the presence of self-renewing structures called root meristems that are covered by a root cap at their apex1,2,3,4,5,6,7,8,9—evolved. Here we report the discovery of what are—to our knowledge—the oldest meristems of rooting axes, found in the earliest-preserved terrestrial ecosystem10 (the 407-million-year-old Rhynie chert). These meristems, which belonged to the lycopsid Asteroxylon mackiei11,12,13,14, lacked root caps and instead developed a continuous epidermis over the surface of the meristem. The rooting axes and meristems of A. mackiei are unique among vascular plants. These data support the hypothesis that roots, as defined in extant vascular plants by the presence of a root cap7, were a late innovation in the vascular lineage. Roots therefore acquired traits in a stepwise fashion. The relatively late origin in lycophytes of roots with caps is consistent with the hypothesis that roots evolved multiple times2 rather than having a single origin1, and the extensive similarities between lycophyte and euphyllophyte roots15,16,17,18 therefore represent examples of convergent evolution. The key phylogenetic position of A. mackiei—with its transitional rooting organ—between early diverging land plants that lacked roots and derived plants that developed roots demonstrates how roots were ‘assembled’ during the course of plant evolution.

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Acknowledgements

A.J.H. was funded by the George Grosvenor Freeman Fellowship by Examination in Sciences, Magdalen College (Oxford). L.D. was funded by a European Research Council Advanced Grant (EVO500, contract 250284) and a European Commission Framework 7 Initial Training Network (PLANTORIGINS, project identifier 238640). We are grateful to the Oxford University Herbaria, the University of Manchester, Manchester Museum, The Hunterian, University of Glasgow and the London Natural History Museum for access to fossil thin sections, and to the curators of these collections (S. Harris, K. Sherburn, N. Clark and P. Hayes) for their assistance. We thank T. Goral, C. Strullu-Derrien, C. Kirchhelle, I. Moore and I. Rahmen for assistance and advice for confocal imaging, segmentation and 3D reconstructions; J. Baker for photographic advice; and A. M. Hetherington, N. J. Hetherington and members of the Dolan laboratory for helpful comments and discussions.

Reviewer information

Nature thanks P. Crane and P. Kenrick for their contribution to the peer review of this work.

Author information

Affiliations

  1. Department of Plant Sciences, University of Oxford, Oxford, UK

    • Alexander J. Hetherington
    •  & Liam Dolan

Authors

  1. Search for Alexander J. Hetherington in:

  2. Search for Liam Dolan in:

Contributions

A.J.H. and L.D. designed the project. A.J.H. carried out the analyses. A.J.H. and L.D. wrote the paper.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Liam Dolan.

Extended data figures and tables

  1. Extended Data Fig. 1 Five root apices were found on three thin sections in which A. mackiei was the only plant species present.

    ac, Diagnostic features of A. mackiei include the apices of leafy shoots (black arrowhead, a), star-shaped xylem (black arrowhead, b) and leaves (black arrowhead, c). a, GLAHM Kid 3080. b, NHMUK V.15642. c, OXF 108. Scale bars, 1 cm.

  2. Extended Data Fig. 2 A. mackiei rooting axes grew in the direction of the gravity vector.

    ac, Positively gravitropic growth of two apices (a) was inferred from their orientation relative to sediment layers in both the growth substrate (dark brown and black bands at base of b) and a geopetally infilled void (c) preserved in the thin section. The position of both the apices and geopetally infilled void are highlighted with black boxes within the thin section (b). ac, NHMUK V.15642. Scale bars, 1 mm (a, c), 1 cm (b).

  3. Extended Data Fig. 3 Fundamental tissues present in an apex of a rooting axis preserved after growth had finished, and a meristem of a rooting axis preserved during active growth.

    a, b, Root apices with fundamental tissue types colour-coded. Blue, epidermis; pink, promeristem; orange, cortex; and green, procambium. c, d, Magnified images of the apical regions of a (c) and b (d). The presence of differentiated vascular tissue (arrowhead, c) close to the tip of the apex indicates that this apex was not active at the time of preservation. By contrast, in d there is no differentiated vascular tissue. Instead, the apex is characterized by large numbers of cells and cell size gradually increases with distance from the tip, which indicates that the apex was active when fossilized. a, c NHMUK V.15642 (same specimen as illustrated in Fig. 1a), b, c, OXF 108 (same specimen as illustrated in Figs. 1d, 2a, b). Scale bars, 500 μm (a), 250 μm (b), 150 μm (c), 100 μm (d).

  4. Extended Data Fig. 4 Mulm coats the rooting axes and leafy shoots of A. mackiei.

    ad, A thin layer of degraded organic material called mulm27 (highlighted with arrowheads, ad) coats both the rooting axes (a, c) and leafy shoots of A. mackiei. a, b, GLAHM Kid 3080. c, d, OXF 108. Scale bars, 500 μm (a, c, d), 1 mm (b).

Supplementary information

  1. Reporting Summary

  2. Video 1

    Segmentation of the epidermal surface of an Asteroxylon mackiei rooting axis meristem. MorphoGraphX was used to segment the epidermal surface from a z-stack of images captured on a confocal microscope. GLAHM Kid 3080. Scale bar 50 µm.

  3. Video 2

    Asteroxylon mackiei rooting axis meristems were covered by a continuous layer of epidermis and lacked a root cap. Animation showing the three-dimensional model produced of the rooting axis meristem of A. mackiei segmented using MorphoGraphX and animated using BlenderTM. GLAHM Kid 3080. Scale bar 50 µm.

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DOI

https://doi.org/10.1038/s41586-018-0445-z

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