The Silurian–Devonian terrestrial revolution saw the evolution of vascular plants with complex bodies comprising distinct roots, root-bearing organs, shoots, and leaves from morphologically simpler ancestors characterised by networks of undifferentiated axes (Bateman et al., 1998; Gensel and Edwards, 2001; Kenrick and Crane, 1997; Stewart and Rothwell, 1993; Xue et al., 2018). The 407-million-year-old, Pragian–?earliest Emsian, Early Devonian (Wellman, 2006) Rhynie chert fossil site provides a unique insight into the structure of plants during this key time in plant evolution. The Rhynie chert preserves an entire Early Devonian hot spring ecosystem, where plants, animals, fungi, and microbes are preserved in situ (Edwards et al., 2018; Garwood et al., 2020; Rice et al., 2002; Strullu-Derrien et al., 2019; Wellman, 2018). The exceptional preservation has been crucial for our understanding of early land plant evolution because it is the earliest time point in the fossil record where cellular details of rhizoid-based rooting systems, germinating spores, and fossilised meristems are preserved (Edwards, 2003; Hetherington and Dolan, 2018a; Hetherington and Dolan, 2018b; Kerp, 2018; Lyon, 1957; Taylor et al., 2005). Most of the detailed cellular information about these organisms comes from sectioned material. While the cellular detail that can be observed in these sections allows high-resolution reconstruction of tissue systems, the three-dimensional relationship between the cells, tissue, and organs is obscured. This makes generating accurate reconstructions of body plans difficult (Edwards, 2003; Kidston and Lang, 1921). Furthermore, reconstructions that have been published are based on combining material from thin sections from multiple individuals (Kidston and Lang, 1921). These sampling problems mean that key features of the body plans of these organisms are missing in reconstructions. This is particularly problematic for larger, more complex species in the Rhynie chert, such as the lycopsid Asteroxylon mackiei (Bhutta, 1969; Edwards, 2003; Edwards et al., 2018; Hetherington and Dolan, 2018a; Kerp, 2018; Kerp et al., 2013; Kidston and Lang, 1920; Kidston and Lang, 1921).

A. mackiei has been reconstructed as a plant that is approximately 30 cm high (Bhutta, 1969; Edwards, 2003), with highly branched shoot and rooting systems (Chaloner and MacDonald, 1980; Kerp, 2018; Kerp et al., 2013; Kidston and Lang, 1920; Kidston and Lang, 1921). It holds an important phylogenetic position for understanding root and leaf evolution in lycophytes because it is a member of the earliest diverging lineage of the lycopsids, the Drepanophycales (Kenrick and Crane, 1997), and both the rooting axes and leaves of A. mackiei developed some but not all defining characteristics of roots and leaves in more derived species (Bower, 1908; Hetherington and Dolan, 2018a; Kenrick, 2002; Kidston and Lang, 1920). However, the precise number of distinct axis types and their interconnection is still unclear (Bhutta, 1969; Kidston and Lang, 1920; Kidston and Lang, 1921). Without a complete understanding of the growth habit of A. mackiei, it is not possible to compare its structure with living lycopsids or other drepanophycalean lycopsids found in Devonian compression fossils. The drepanophycalean lycopsids are the earliest group of land plants in the fossil record with complex body plans comprising distinct rooting axes, root-bearing organs, and leafy shoots (Gensel et al., 2001; Gensel and Edwards, 2001; Hueber, 1992; Kenrick and Crane, 1997; Lang and Cookson, 1935; Matsunaga and Tomescu, 2016; Matsunaga and Tomescu, 2017; Stewart and Rothwell, 1993). Their evolution, radiation, and spread across all continents contributed to the transformation of the terrestrial environment through their impact on soil formation and stabilisation, surface hydrology, and silicate weathering (Algeo and Scheckler, 1998; Gibling and Davies, 2012; Matsunaga and Tomescu, 2016; Xue et al., 2016). Given the recognition of the importance of the drepanophycalean lycopsids in the evolution of complex body plans and changes to global nutrient and hydrological cycles, we generated a reconstruction of the 3D structure of A. mackiei based entirely on serial sections from complete specimens fossilised in situ.

Here we report the 3D reconstruction of A. mackiei based on both morphology and anatomy of two different plants. This reconstruction allowed us to define the 3D organisation of the three axis types of the A. mackiei body and to describe how the rooting system developed.

To discover the structure and infer the development of the lycopsid A. mackiei, we produced a series of 31 consecutive thick sections through a block of Rhynie chert that preserved a branched network of connected A. mackiei axes in situ (Figure 1—figure supplement 1, Figure 1—figure supplement 2). Using images of these thick sections, we digitally reconstructed the A. mackiei plant in a volume of 4.8 cm in length, 3.5 cm in width, and 2.8 cm in height (Figure 1A,B,G Video 1), which, to our knowledge, represents the largest evidence-based reconstruction for any Rhynie chert plant to date. We distinguished three distinct axis types in a single individual plant that we designate: leafy shoot axes, root-bearing axes, and rooting axes.

Figure 1 with 2 supplements see all

Download asset Open asset

Video 1

Download asset

Root-bearing axes

Root-bearing axes of A. mackiei were attached to leafy shoot axes at anisotomous branch points, where the thinner daughter axis developed as a root-bearing axis and the thicker daughter axis developed as a leafy shoot axis (Figures 1 and 2). Diameters of root-bearing axes were ca. 0.35 cm compared to leafy shoots axes typically over 0.6 cm. In one of the five examples (Figure 2A–C), the root-bearing axis was attached directly to the main leafy shoot axis. In the four other examples (Figure 2D–I), root-bearing axes were attached to side branches of the main leafy shoot. These branches were termed first-order leafy shoots because they were separated from the main shoot by a single branching event. Root-bearing axes attached to first-order leafy shoot axes close to where the latter attached to the main shoot. The branch arrangement where two adjacent anisotomous branches originate close to each other is termed k-branching (Chomicki et al., 2017; Edwards, 1994; Gensel et al., 2001; Gensel and Berry, 2001; Gerrienne, 1988; Matsunaga and Tomescu, 2016; Matsunaga and Tomescu, 2017). The root-bearing axes of the Drepanophycalean lycopsid Sengelia radicans (Matsunaga and Tomescu, 2016; Matsunaga and Tomescu, 2017) are attached to leafy shoot axes at k-branch points. In both A. mackiei and S. radicans, root-bearing axes developed an epidermis and cuticle with occasional stomata and scale leaves. In the root-bearing axes of A. mackiei where anatomy could be investigated the xylem strand was elliptical, not lobed as in leafy shoot axes, and there were few or no leaf traces, which distinguishes them from leafy shoots in which leaf traces were abundant (Figure 1E). Root-bearing axes were aligned with the gravity vector, indicating strong positive gravitropic growth (Figures 1A,B and 2). These differences in anatomy and morphology between root-bearing axes and leafy shoots demonstrate that root-bearing axes were a distinct axis type and not merely a transitional zone between two axis types as previously suggested (Bhutta, 1969; Kidston and Lang, 1920; Kidston and Lang, 1921). The apex of a root-bearing axis had not been described previously. We searched for apices on axes with the characters of root-bearing axes and discovered an isolated bifurcating axis with two apices (Figure 2J,K). The apices were assigned to A. mackiei because of the presence of leaves on the parent axis (Figure 2J, arrowheads) and a small leaf on the flank of the upper apex (Figure 2J,K), A. mackiei is the only Rhynie chert plant with leaves. Both apices were covered by an unbroken cuticle, and a single small leaf was present on the upper apex, which together demonstrate that these are apices of root-bearing axes and not apices of rooting axes that lack leaves and cuticles (Hetherington and Dolan, 2018a), or leafy shoots where the apex is covered by a large number of leaves (Edwards, 2003; Hueber, 1992; Kerp, 2018; Kerp et al., 2013). These apices were found in a single thin section that was not part of a set of serial sections and therefore it was not possible to reconstruct the apex in 3D. The root-bearing axes described here are similar to the axes described as either root-bearing axes (Matsunaga and Tomescu, 2016; Matsunaga and Tomescu, 2017) or rhizomes (Rayner, 1984; Schweitzer, 1980; Schweitzer and Giesen, 1980; Xu et al., 2013) in other members of the Drepanophycales. The occurrence of these root-bearing axes in A. mackiei and multiple other species highlights the conservation of body plans among members of the Drepanophycales.

Figure 2

Download asset Open asset

Rooting axes

A. mackiei rooting axes are similar to roots of extant lycopsids. However, they are designated rooting axes because they lack root hairs and their meristems lack a root cap and are consequently interpreted as transitional to the roots of extant plants (Hetherington and Dolan, 2018a; Hetherington and Dolan, 2019). These rooting axes include structures called rhizomes (Bhutta, 1969), small root-like rhizomes (Kidston and Lang, 1920; Kidston and Lang, 1921), and rooting axes (Hetherington and Dolan, 2018a; Hetherington and Dolan, 2019) of A. mackiei from previous descriptions of plant fragments. Rooting axes were always less than 2 mm in diameter and frequently less than 1 mm and were highly branched (Bhutta, 1969; Hetherington and Dolan, 2018a; Kidston and Lang, 1920; Kidston and Lang, 1921). Leaves, leaf traces, stomata, and cuticles were never found on rooting axes, even when the epidermis was well preserved (Kidston and Lang, 1920). The epidermis was frequently missing, suggesting that it was lost in older axes and the outer cortex was often limited to one or two cell layers (Figure 1F; Kidston and Lang, 1920). We found a single well-preserved highly branched rooting axis in our reconstruction (Figure 3A–F). This rooting axis was attached to a root-bearing axis at an anisotomous branch point (Figure 3C). There was a circular xylem strand at the centre of the rooting axis. The diameter of the rooting axis where it attached to the root-bearing axis was ca. 2 mm but decreased in size distally at successive branch points. Leaves, leaf traces, stomata, and cuticles were never observed on the rooting axis. The rooting axis was weakly gravitropic in contrast to the strong gravitropic growth observed in root-bearing axes (Figure 3A,E). The profuse branching of the rooting axis is evident with over four orders of branching preserved in less than 1 cm in our reconstruction (Figure 3E). We found no evidence that other axis types developed from the rooting axis. The morphological and anatomical boundary between the root-bearing axis and rooting axis was clear (Figure 3C); it involved the change from strong gravitropic growth to weak gravitropic growth, and the absence of scale leaves, stomata, and a well-marked cuticle all found on root-bearing axes but absent on rooting axes. This suggests that the boundary between the two axis types is defined at the point of branching and not in a continuum along a single axis. The rooting axis and its attachment to root-bearing axes described here correspond to the axes termed, roots (Matsunaga and Tomescu, 2016; Matsunaga and Tomescu, 2017; Schweitzer, 1980; Schweitzer and Giesen, 1980), root-like axes (Gensel et al., 2001; Rayner, 1984), and rootlets (Xu et al., 2013) in other members of the Drepanophycales. This suggests that the body plan of A. mackiei was similar to other members of the Drepanophycales.

Figure 3

Download asset Open asset

Our new reconstruction from serial thick sections through an individual A. mackiei plant demonstrates that the A. mackiei body plan consisted of three distinct axis types – leafy shoot axes, root-bearing axes, and rooting axes – each with characteristic anatomy and morphology.

Dichotomous origin of rooting axes

The rooting axes of A. mackiei hold a key position for interpreting the origin of roots in lycopsids because they were transitional between the ancestral rootless state and the derived state characterised by true roots with caps as found in extant lycopsids (Hetherington and Dolan, 2018a; Hetherington and Dolan, 2019). Our new reconstruction enables interpretation of these rooting axes and comparison with the rooting axes variously called roots, root-like axes, or rootlets in other members of the Drepanophycales that have been reported in the literature. Our reconstruction demonstrates that a number of characters are shared between the rooting axes of A. mackiei and rooting axes of other members of the Drepanophycales, including their attachment to root-bearing axes, weak gravitropic growth, and profuse dichotomous branching.

These shared characters suggest that the rooting system of A. mackiei was representative of the Drepanophycales and that inferences made with the exceptional preservation of A. mackiei can elucidate the characteristics of other members of the Drepanophycales that are preserved primarily as compression fossils. Our new reconstruction indicates that rooting axes connected to root-bearing axes at anisotomous branch points. Based on development of extant lycopsids (Bierhorst, 1971; Fujinami et al., 2021; Gola, 2014; Guttenberg, 1966; Harrison et al., 2007; Hetherington and Dolan, 2017; Imaichi, 2008; Imaichi and Kato, 1989; Ogura, 1972; Ollgaard, 1979; Spencer et al., 2021; Yi and Kato, 2001; Yin and Meicenheimer, 2017), there are two modes of branching that could produce anisotomous branch point morphology, endogenous branching, or dichotomous branching. Endogenous branching is the mode of branching where the meristem of the new axis develops from the internal tissues of the parent axis and breaks through the parent tissue to emerge, a mode of development typical of the initiation of roots of extant lycopsid species. Dichotomous branching is the mode of branching where the parent meristem splits in two to produce two daughter axes, a mode of development typical of roots, shoots, and rhizophores in extant lycopsids (Bierhorst, 1971; Bruchmann, 1874; Gola, 2014; Guttenberg, 1966; Harrison et al., 2007; Hetherington and Dolan, 2017; Imaichi, 2008; Imaichi and Kato, 1989; Ogura, 1972; Ollgaard, 1979; Spencer et al., 2021; Wigglesworth, 1907; Yi and Kato, 2001; Yin and Meicenheimer, 2017). To investigate which mode of development operated in A. mackiei, we examined anatomy of branch points.

If the rooting axes developed by endogenous branching from root-bearing axes, there would likely be a disruption to the tissues of the leafy shoot and evidence that the vascular trace of the root-bearing axes connected at right angles to the vascular trace of the leafy shoot (Bruchmann, 1874; Guttenberg, 1966; Imaichi, 2008; Ogura, 1972; Van Tieghem and Douliot, 1888; Wigglesworth, 1907; Yi and Kato, 2001). Our thick sections only provided a small organic connection between the two axes (Figure 3C) limiting our ability to investigate the anatomical changes associated with branching. We therefore searched other Rhynie chert collections for rooting axes attached to root-bearing axes at anisotomous branching points. We reinvestigated an example originally described as a branching rhizome by Bhutta, 1969. The presence of scale leaves, a small number of leaf traces, and clear epidermis and cuticle on the main axis suggested that it was a root-bearing axis. Attached to this root-bearing axis was a smaller axis that we interpret as a rooting axis because of its rounded xylem, poorly preserved epidermis and the lack of both cuticle and root cap (Figure 4, Figure 4—figure supplement 1). We produced a 3D reconstruction of the anisotomous branch point that connects the two axes based on 119 peels (Figure 4, Video 2). Tissues were continuous between the root-bearing axis and rooting axis. The vascular trace for the rooting axis was seen to branch off and then run parallel to the main vascular trace before gradually arcing into the rooting axis (Figure 4). These characteristics, especially the dichotomy of the vascular trace, suggest that rooting axes developed from root-bearing axes by dichotomous branching.

Figure 4 with 1 supplement see all

Download asset Open asset

Video 2

Download asset

While branching evidence in our reconstruction is consistent with the development of rooting axes from root-bearing axes by dichotomy, we tested if there was evidence for endogenous development because roots originate endogenously in extant lycopsids. Therefore, we searched for meristems of rooting axes preserved soon after they originated from root-bearing axes. We identified two fossilised A. mackiei meristems on a single thin section. This thin section preserves a large A. mackiei leafy shoot axis ca. 5 mm in diameter with stellate xylem cut in transverse section at the top of the image (Figure 5A, green arrowhead). Attached to the leafy shoot axis is a smaller root-bearing axis ca. 1.9 mm in diameter close to the attachment with the leafy shoot. This axis is identified as a root-bearing axis by the presence of a small scale leaf (Figure 5A, blue arrowhead, B), and its orientation aligned with the gravity vector based on a geopetally infilled void (Figure 5—figure supplement 1). Close to the base of the thin section are two apices on either side of the root-bearing axis (Figure 5A, white arrowheads). We interpret these as meristems because of their domed structure and the large number of small cells close to the apices. Given the attachment of these meristems to root-bearing axes and their small size, we interpret them as meristems of rooting axes. Cellular organisation of the promeristems (Figure 5C–E, Figure 5—figure supplement 2) is poorly preserved compared to other meristems we described (Hetherington and Dolan, 2018a), but the overall organisation including cell files running from the central vascular trace, and a cuticle covering the apices can be clearly recognised. There is no root cap as previously reported for rooting axes (Hetherington and Dolan, 2018a). Cell files are continuous between the root-bearing axes and rooting axes, and there is no evidence that the rooting axes initiated by endogenous branching and broke through the ground or dermal tissues of the root-bearing axes. The organisation of cells in these meristems is consistent with our hypothesis based on 3D reconstructed anatomy that the rooting axes developed by dichotomous branching from root-bearing axes.

Figure 5 with 2 supplements see all

Download asset Open asset

We discovered that A. mackiei rooting axes originate by dichotomous branching. Furthermore, the branch connecting rooting axes and root-bearing axes was always anisotomous. This finding is significant because roots do not originate by dichotomy in extant lycopsids. Instead, roots of extant lycopsids originate endogenously from shoots, rhizophores, and rhizomorphs (Bruchmann, 1874; Guttenberg, 1966; Hetherington and Dolan, 2017; Imaichi, 2008; Imaichi and Kato, 1989; Ogura, 1972; Yi and Kato, 2001), and in rare cases by exogenous development in embryos, protocorms, or tubers where dichotomous branching does not occur (Bower, 1908; Hetherington and Dolan, 2017). The origin of A. mackiei rooting axes by anisotomous dichotomy was therefore different from the origin of roots in extant lycopsids, and this developmental mechanism is now extinct (Figure 6).

Figure 6

Download asset Open asset

Specimen accession code abbreviations: Forschungsstelle für Paläobotanik, Institut für Geologie und Paläontologie, Westfälische Wilhelms-Universität, Münster, Germany; Pb. The Hunterian, University of Glasgow, GLAHM. Natural History Museum, London, NHMUK.

Fossil preparations described in this study are housed in the A. Bhutta collection at the University of Cardiff, UK. Forschungsstelle für Paläobotanik, Institut für Geologie und Paläontologie, Westfälische Wilhelms-Universität, Münster, Germany. The Hunterian, University of Glasgow, UK and the Natural History Museum, London, UK. Photographs of the series of thick sections and peels used to create 3D reconstructions of A. mackiei have been deposited on Zenodo (http://doi.org/10.5281/zenodo.4287297). All other data supporting the findings of this study are included in the paper.

1. 1. Hetherington AJ
   2. Bridson SL
   3. Jones AL
   4. Hass H
   5. Kerp H
   6. Dolan L

   (2020) Zenodo

   Supplementary information: An evidence-based 3D reconstruction of Asteroxylon mackiei the most complex plant preserved from the Rhynie chert.

   https://doi.org/10.5281/zenodo.4287297

1. 1. Algeo TJ
   2. Scheckler SE

   (1998) Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events

   Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 353:113–130.

   https://doi.org/10.1098/rstb.1998.0195

   • Google Scholar
2. 1. Bateman RM
   2. Crane PR
   3. DiMichele WA
   4. Kenrick PR
   5. Rowe NP
   6. Speck T
   7. Stein WE

   (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation

   Annual Review of Ecology and Systematics 29:263–292.

   https://doi.org/10.1146/annurev.ecolsys.29.1.263

   • Google Scholar
3. Book

   1. Bhutta AA

   (1969)

   Studies on the Flora of the Rhynie Chert

   University of Wales.

   • Google Scholar
4. Book

   1. Bierhorst DW

   (1971)

   Morphology of Vascular Plants

   Macmillan.

   • Google Scholar
5. Book

   1. Bower FO

   (1908)

   The Origin of a Land Flora

   Macmillan and Co.

   • Google Scholar
6. 1. Bruchmann H

   (1874)

   Ueber anlage und wachsthum der wurzeln von Lycopodium und Isoetes jenaische zeitschrift

   Für. Naturwissenschaft 9:522–578.

   • Google Scholar
7. Book

   1. Chaloner WG
   2. MacDonald P

   (1980)

   Plants invade the land

   H.M.S.O. for the Royal Scottish Museum.

   • Google Scholar
8. 1. Chomicki G
   2. Coiro M
   3. Renner SS

   (2017) Evolution and ecology of plant architecture: integrating insights from the fossil record, extant morphology, developmental genetics and phylogenies

   Annals of Botany 120:855–891.

   https://doi.org/10.1093/aob/mcx113

   • PubMed
   • Google Scholar
9. 1. Edwards D

   (1970) Further observations on the Lower Devonian Plant, Gosslingia breconensis Heard

   Philosophical transactions of the Royal Society of London. Series B, Biological sciences 258:225–243.

   https://doi.org/10.1098/rstb.1970.0034

   • PubMed
   • Google Scholar
10. 1. Edwards D
    2. Kenrick P
    3. Carluccio LM

    (1989) A reconsideration of cf Psilophyton princeps (Croft & Lang, 1942), a zosterophyll widespread in the Lower Old Red Sandstone of South Wales

    Botanical Journal of the Linnean Society 100:293–318.

    https://doi.org/10.1111/j.1095-8339.1989.tb01723.x

    • Google Scholar
11. Book

    1. Edwards D

    (1994)

    Towards an understanding of pattern and process in the growth of early vascular plants

    In: Ingram D, Hudson A, editors. Shape and Form in Plants and Fungi, Linnean Society Symposium Series, Linnean Society of London. Academic Press. pp. 39–59.

    • Google Scholar
12. 1. Edwards D

    (2003) Embryophytic sporophytes in the rhynie and windyfield cherts

    Transactions of the Royal Society of Edinburgh: Earth Sciences 94:397–410.

    https://doi.org/10.1017/S0263593300000778

    • Google Scholar
13. 1. Edwards D
    2. Kenrick P
    3. Dolan L

    (2018) History and contemporary significance of the Rhynie cherts—our earliest preserved terrestrial ecosystem

    Philosophical Transactions of the Royal Society B: Biological Sciences 373:20160489.

    https://doi.org/10.1098/rstb.2016.0489

    • Google Scholar
14. 1. Edwards D
    2. Kenrick P

    (1986) A new zosterophyll from the Lower Devonian of Wales

    Botanical Journal of the Linnean Society 92:269–283.

    https://doi.org/10.1111/j.1095-8339.1986.tb01432.x

    • Google Scholar
15. 1. Fujinami R
    2. Nakajima A
    3. Imaichi R
    4. Yamada T

    (2021) Lycopodium root meristem dynamics supports homology between shoots and roots in lycophytes

    New Phytologist 229:460–468.

    https://doi.org/10.1111/nph.16814

    • PubMed
    • Google Scholar
16. 1. Garwood RJ
    2. Oliver H
    3. Spencer ART

    (2020) An introduction to the Rhynie chert

    Geological Magazine 157:47–64.

    https://doi.org/10.1017/S0016756819000670

    • Google Scholar
17. Book

    1. Gensel PG
    2. Kotyk ME
    3. Brasinger JF

    (2001) Morphology of above- and below-ground structures in Early Devonian (Pragian–Emsian) plants

    In: Gensel P. G, Edwards D, editors. Plants Invade the Land: Evolutionary and Environmental Perspectives. New York, USA: Columbia University Press. pp. 83–102.

    https://doi.org/10.7312/gens11160-006

    • Google Scholar
18. 1. Gensel PG
    2. Berry CM

    (2001) Early Lycophyte Evolution

    American Fern Journal 91:74–98.

    https://doi.org/10.1640/0002-8444(2001)091[0074:ELE]2.0.CO;2

    • Google Scholar
19. Book

    1. Gensel PG
    2. Edwards D

    (2001) Plants Invade the Land : Evolutionary and Environmental Perspectives

    New York, USA: Columbia University Press.

    https://doi.org/10.7312/gens11160

    • Google Scholar
20. 1. Gerrienne P

    (1988) Early Devonian plant remains from Marchin (North of Dinant Synclinorium, Belgium), I. Zosterophyllum deciduum sp. nov

    Review of Palaeobotany and Palynology 55:317–335.

    https://doi.org/10.1016/0034-6667(88)90091-7

    • Google Scholar
21. 1. Gibling MR
    2. Davies NS

    (2012) Palaeozoic landscapes shaped by plant evolution

    Nature Geoscience 5:99–105.

    https://doi.org/10.1038/ngeo1376

    • Google Scholar
22. 1. Gola EM

    (2014) Dichotomous branching: the plant form and integrity upon the apical meristem bifurcation

    Frontiers in Plant Science 5:1–7.

    https://doi.org/10.3389/fpls.2014.00263

    • PubMed
    • Google Scholar
23. Book

    1. Guttenberg HV

    (1966)

    Histogenese Der Pteridophyten. Handbuch Der Pflanzenanatomie

    Berlin, Germany: Gebrüder Borntraeger.

    • Google Scholar
24. 1. Hao S
    2. Xue J
    3. Liu Z
    4. Wang D

    (2007) Zosterophyllum Penhallow around the Silurian‐Devonian Boundary of Northeastern Yunnan, China

    International Journal of Plant Sciences 168:477–489.

    https://doi.org/10.1086/511011

    • Google Scholar
25. 1. Hao S
    2. Xue J
    3. Guo D
    4. Wang D

    (2010) Earliest rooting system and root: shoot ratio from a new Zosterophyllum plant

    New Phytologist 185:217–225.

    https://doi.org/10.1111/j.1469-8137.2009.03056.x

    • PubMed
    • Google Scholar
26. 1. Harrison CJ
    2. Rezvani M
    3. Langdale JA

    (2007) Growth from two transient apical initials in the meristem of Selaginella kraussiana

    Development 134:881–889.

    https://doi.org/10.1242/dev.001008

    • PubMed
    • Google Scholar
27. Book

    1. Hass H
    2. Rowe NP

    (1999)

    Thin sections and wafering

    In: Jones T. P, Rowe N. P, editors. Fossil Plants and Spores: Modern Techniques. London: Geological Society. pp. 76–81.

    • Google Scholar
28. 1. Hetherington AJ
    2. Dolan L

    (2017) The evolution of lycopsid rooting structures: conservatism and disparity

    New Phytologist 215:538–544.

    https://doi.org/10.1111/nph.14324

    • PubMed
    • Google Scholar
29. 1. Hetherington AJ
    2. Dolan L

    (2018a) Stepwise and independent origins of roots among land plants

    Nature 561:235–238.

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

    • Google Scholar
30. 1. Hetherington AJ
    2. Dolan L

    (2018b) Bilaterally symmetric axes with rhizoids composed the rooting structure of the common ancestor of vascular plants

    Philosophical Transactions of the Royal Society B: Biological Sciences 373:20170042.

    https://doi.org/10.1098/rstb.2017.0042

    • Google Scholar
31. 1. Hetherington AJ
    2. Dolan L

    (2019) Rhynie chert fossils demonstrate the independent origin and gradual evolution of lycophyte roots

    Current Opinion in Plant Biology 47:119–126.

    https://doi.org/10.1016/j.pbi.2018.12.001

    • PubMed
    • Google Scholar
32. 1. Hueber FM

    (1992) Thoughts on the early lycopsids and zosterophylls

    Annals of the Missouri Botanical Garden 79:474–499.

    https://doi.org/10.2307/2399751

    • Google Scholar
33. Book

    1. Imaichi R

    (2008) Meristem organization and organ diversity

    In: Ranker T. A, Haufler C. H, editors. Biology and Evolution of Ferns and Lycophytes. Cambridge: Cambridge University Press. pp. 75–104.

    https://doi.org/10.1017/CBO9780511541827.004

    • Google Scholar
34. 1. Imaichi R
    2. Kato M

    (1989) Developmental anatomy of the shoot apical cell, rhizophore and root ofSelaginella uncinata

    The Botanical Magazine Tokyo 102:369–380.

    https://doi.org/10.1007/BF02488120

    • Google Scholar
35. 1. Imaichi R
    2. Kato M

    (1991) Developmental study of branched rhizophores in three Selaginella species

    American Journal of Botany 78:1694–1703.

    https://doi.org/10.1002/j.1537-2197.1991.tb14533.x

    • Google Scholar
36. Book

    1. Kenrick P

    (2002)

    The telome theory

    In: Cronk Q. C. B, Bateman R. M, Hawkins J, editors. Developmental Genetics and Plant Evolution. London: Taylor & Francis. pp. 365–387.

    • Google Scholar
37. Book

    1. Kenrick P
    2. Crane PR

    (1997)

    The Origin and Early Diversification of Land Plants: A Cladistic Study. Smithsonian Series in Comparative Evolutionary Biology

    Washington, DC, USA: Smithsonian Institute Press.

    • Google Scholar
38. Book

    1. Kerp H
    2. Hass H
    3. Mosbrugger V

    (2001) New data on Nothia aphylla Lyon 1964 ex El-Saadawy et Lacey 1979, a poorly known plant from the Lower Devonian Rhynie Chert

    In: Gensel P. G, Edwards D, editors. Plants Invade the Land: Evolutionary and Environmental Perspectives. New York, USA: Columbia University Press. pp. 52–82.

    https://doi.org/10.7312/gens11160-005

    • Google Scholar
39. 1. Kerp H
    2. Wellman CH
    3. Krings M
    4. Kearney P
    5. Hass H

    (2013) Reproductive Organs and In Situ Spores of Asteroxylon mackiei Kidston & Lang, the Most Complex Plant from the Lower Devonian Rhynie Chert

    International Journal of Plant Sciences 174:293–308.

    https://doi.org/10.1086/668613

    • Google Scholar
40. 1. Kerp H

    (2018) Organs and tissues of Rhynie chert plants

    Philosophical Transactions of the Royal Society B: Biological Sciences 373:20160495.

    https://doi.org/10.1098/rstb.2016.0495

    • Google Scholar
41. 1. Kerp H
    2. Bomfleur B

    (2011) Photography of plant fossils—New techniques, old tricks

    Review of Palaeobotany and Palynology 166:117–151.

    https://doi.org/10.1016/j.revpalbo.2011.05.001

    • Google Scholar
42. 1. Kidston R
    2. Lang WH

    (1920) XXVI.—On old red sandstone plants showing structure, from the rhynie chert bed, aberdeenshire Part III Asteroxylon Mackiei, Kidston and Lang

    Transactions of the Royal Society of Edinburgh 52:643–680.

    https://doi.org/10.1017/S0080456800004506

    • Google Scholar
43. 1. Kidston R
    2. Lang WH

    (1921) On old red sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire Part IV Restorations of the vascular cryptogams, and discussion of their bearing on the general morphology of the pteridophyta and the origin of the organisation of land-plants

    Transactions of the Royal Society of Edinburgh 52:831–854.

    https://doi.org/10.1017/S0080456800016033

    • Google Scholar
44. 1. Kotyk ME
    2. Basinger JF

    (2000) The early devonian (Pragian) zosterophyll bathurstia denticulata Hueber

    Canadian Journal of Botany 78:193–207.

    https://doi.org/10.1139/b99-179

    • Google Scholar
45. 1. Lang WH
    2. Cookson IC

    (1935)

    On a flora, including vascular land plants, associated with Monograptus, in rocks of silurian age, from Victoria, Australia

    Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 224:421–449.

    • Google Scholar
46. 1. Li CS

    (1992) An early devonian plant from Yunnan Province, China and its bearing on some structures of early land plants

    Review of Palaeobotany and Palynology 71:121–147.

    https://doi.org/10.1016/0034-6667(92)90160-I

    • Google Scholar
47. 1. Li CS
    2. Edwards D

    (1995)

    A reinvestigation of Halle’s drepanophycus spinaeformis göpp from the lower devonian of Yunnan Province, southern china

    Botanical Journal of the Linnean Society 118:163–192.

    • Google Scholar
48. 1. Lyon AG

    (1957) Germinating spores in the rhynie chert

    Nature 180:1219–1220.

    https://doi.org/10.1038/1801219a0

    • Google Scholar
49. 1. Lyon AG

    (1964) Probable fertile region of Asteroxylon mackiei K. and L

    Nature 203:1082–1083.

    https://doi.org/10.1038/2031082b0

    • Google Scholar
50. 1. Matsunaga KK
    2. Tomescu AM

    (2016) Root evolution at the base of the lycophyte clade: insights from an early devonian lycophyte

    Annals of Botany 117:585–598.

    https://doi.org/10.1093/aob/mcw006

    • PubMed
    • Google Scholar
51. 1. Matsunaga KKS
    2. Tomescu AMF

    (2017) An organismal concept for Sengelia radicans gen et sp nov - morphology and natural history of an Early Devonian lycophyte

    Annals of Botany 119:1097–1113.

    https://doi.org/10.1093/aob/mcw277

    • PubMed
    • Google Scholar
52. Book

    1. Ogura Y

    (1972)

    Comparative Anatomy of Vegetative Organs of the Pteridophytes

    Gebrüder Borntraeger.

    • Google Scholar
53. 1. Ollgaard B

    (1979) Studies in Lycopodiaceae, II. the branching patterns and infrageneric groups of Lycopodium sensu lato

    American Fern Journal 69:49.

    https://doi.org/10.2307/1546896

    • Google Scholar
54. 1. Rayner RJ

    (1984) New finds of Drepanophycus spinaeformis Göppert from the Lower Devonian of Scotland

    Transactions of the Royal Society of Edinburgh: Earth Sciences 75:353–363.

    https://doi.org/10.1017/S0263593300013997

    • Google Scholar
55. 1. Rice CM
    2. Trewin NH
    3. Anderson LI

    (2002) Geological setting of the Early Devonian rhynie cherts, Aberdeenshire, Scotland: an early terrestrial hot spring system

    Journal of the Geological Society 159:203–214.

    https://doi.org/10.1144/0016-764900-181

    • Google Scholar
56. 1. Sanders H
    2. Rothwell GW
    3. Wyatt S

    (2007) Paleontological context for the developmental mechanisms of evolution

    International Journal of Plant Sciences 168:719–728.

    https://doi.org/10.1086/513519

    • Google Scholar
57. 1. Schweitzer H-J

    (1980)

    Über Drepanophycus spinaeformis Göppert

    Bonner Paläobotanische Mitteilungen 7:1–29.

    • Google Scholar
58. 1. Schweitzer H-J
    2. Giesen P

    (1980)

    Über Taeniophyton inopinatum, Protolycopodites devonicus und Cladoxylon scoparium aus dem Mitteldevon von Wuppertal

    Palaeontogr Abteilung B 173:1–25.

    • Google Scholar
59. 1. Spencer V
    2. Nemec Venza Z
    3. Harrison CJ

    (2021) What can lycophytes teach us about plant evolution and development? modern perspectives on an ancient lineage

    Evolution & Development 23:174–196.

    https://doi.org/10.1111/ede.12350

    • PubMed
    • Google Scholar
60. Book

    1. Stewart W
    2. Rothwell GW

    (1993)

    Paleobotany and the Evolution of Plants (Second. ed)

    Cambridge, UK: Cambridge University Press.

    • Google Scholar
61. 1. Strullu-Derrien C
    2. Kenrick P
    3. Knoll AH

    (2019) The Rhynie chert

    Current Biology 29:R1218–R1223.

    https://doi.org/10.1016/j.cub.2019.10.030

    • PubMed
    • Google Scholar
62. 1. Taylor TN
    2. Kerp H
    3. Hass H

    (2005) Life history biology of early land plants: deciphering the gametophyte phase

    PNAS 102:5892–5897.

    https://doi.org/10.1073/pnas.0501985102

    • PubMed
    • Google Scholar
63. 1. Trewin NH
    2. Fayers SR

    (2015) Macro to micro aspects of the plant preservation in the early devonian rhynie cherts, Aberdeenshire, Scotland

    Earth and Environmental Science Transactions of the Royal Society of Edinburgh 106:67–80.

    https://doi.org/10.1017/S1755691016000025

    • Google Scholar
64. 1. Van Tieghem P
    2. Douliot H

    (1888)

    Recherches comparatives sur l’origine des membres endogenes dans les plantes vasculaires

    Ann Des Sci Nat Bot Paris 8:1–656.

    • Google Scholar
65. 1. Wellman CH

    (2006) Spore assemblages from the Lower Devonian ‘Lower Old Red Sandstone’ deposits of the Rhynie outlier, Scotland

    Transactions of the Royal Society of Edinburgh: Earth Sciences 97:167–211.

    https://doi.org/10.1017/S0263593300001449

    • Google Scholar
66. 1. Wellman CH

    (2018) Palaeoecology and palaeophytogeography of the Rhynie chert plants: further evidence from integrated analysis of in situ and dispersed spores

    Philosophical Transactions of the Royal Society B: Biological Sciences 373:20160491.

    https://doi.org/10.1098/rstb.2016.0491

    • PubMed
    • Google Scholar
67. 1. Wigglesworth G

    (1907) The young sporophytes of Lycopodium complanatum and Lycopodium clavatum

    Annals of Botany 21:211–234.

    https://doi.org/10.1093/oxfordjournals.aob.a089131

    • Google Scholar
68. 1. Xu H-H
    2. Feng J
    3. Jiang Q
    4. Wang Y

    (2013) Report of Drepanophycus Göppert (Lycopsida) from the Middle Devonian of Xinjiang, China

    Journal of Systematics and Evolution 51:765–772.

    https://doi.org/10.1111/jse.12043

    • Google Scholar
69. 1. Xue J
    2. Deng Z
    3. Huang P
    4. Huang K
    5. Benton MJ
    6. Cui Y
    7. Wang D
    8. Liu J
    9. Shen B
    10. Basinger JF
    11. Hao S

    (2016) Belowground rhizomes in paleosols: The hidden half of an Early Devonian vascular plant

    PNAS 113:9451–9456.

    https://doi.org/10.1073/pnas.1605051113

    • PubMed
    • Google Scholar
70. 1. Xue J
    2. Huang P
    3. Wang D
    4. Xiong C
    5. Liu L
    6. Basinger JF

    (2018) Silurian-Devonian terrestrial revolution in south China: taxonomy, diversity, and character evolution of vascular plants in a paleogeographically isolated, low-latitude region

    Earth-Science Reviews 180:92–125.

    https://doi.org/10.1016/j.earscirev.2018.03.004

    • Google Scholar
71. 1. Yi S
    2. Kato M

    (2001) Basal meristem and root development in Isoetes asiatica and Isoetes japonica

    International Journal of Plant Sciences 162:1225–1235.

    https://doi.org/10.1086/322942

    • Google Scholar
72. 1. Yin X
    2. Meicenheimer RD

    (2017) Anisotomous dichotomy results from an unequal bifurcation of the original shoot apical meristem in Diphasiastrum digitatum (Lycopodiaceae)

    American Journal of Botany 104:782–786.

    https://doi.org/10.3732/ajb.1700021

    • PubMed
    • Google Scholar
73. 1. Zimmerman W

    (1952)

    Main results of the “Telome Theory

    Palaeobot 1:456–470.

    • Google Scholar

Author details

1. Alexander J Hetherington

   Department of Plant Sciences, University of Oxford, Oxford, United Kingdom

   Present address

   Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Conceptualization, Formal analysis, Supervision, Funding acquisition, Investigation, Methodology, Writing - original draft, Writing - review and editing

   For correspondence

   sandy.hetherington@ed.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1687-818X

2. Siobhán L Bridson

   Department of Plant Sciences, University of Oxford, Oxford, United Kingdom

   Contribution

   Formal analysis, Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

3. Anna Lee Jones

   1. Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
   2. Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom

   Present address

   Oxford Long-term Ecology Laboratory, Department of Zoology, University of Oxford, Oxford, United Kingdom

   Contribution

   Formal analysis, Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

4. Hagen Hass

   Research Group for Palaeobotany, Institute for Geology and Palaeontology, Westfälische Wilhelms-Universität Münster, Münster, Germany

   Contribution

   Resources, Methodology

   Competing interests

   No competing interests declared

5. Hans Kerp

   Research Group for Palaeobotany, Institute for Geology and Palaeontology, Westfälische Wilhelms-Universität Münster, Münster, Germany

   Contribution

   Resources, Data curation, Funding acquisition, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

6. Liam Dolan

   Department of Plant Sciences, University of Oxford, Oxford, United Kingdom

   Present address

   Gregor Mendel Institute of Molecular Plant Biology GmbH, Vienna, Austria

   Contribution

   Conceptualization, Supervision, Funding acquisition, Writing - original draft, Writing - review and editing

   For correspondence

   liam.dolan@gmi.oeaw.ac.at

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1206-7096

• 4,615

  views

• 547

  downloads

• 18

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.