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  1. Evaluation Summary:

    This paper will be of interest to readers in the field of plant evolutionary biology and paleontology, paleobotany in particular. Using novel 3D reconstruction techniques, the authors provide the first evidence-based reconstruction of Asteroxylon mackiei, the Early Devonian Rhynie chert plant known for a century, and demonstrate that it possessed an extinct pattern of root development transitional to the evolution of true roots in modern club-mosses. The use of multiple lines of evidence and 3D reconstructions based on serial sections of petrified materials provides compelling support for the key conclusions of the paper.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewers #1, #2, and #3 agreed to share their names with the authors.)

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  2. Reviewer #1 (Public Review):

    Using the noval 3D reconstruction techniques, Hetherington and colleagues investigated the body plan of Asteroxylon mackiei, which is an extinct lycopsid from the Early Devonian Rhynie Lagerstatte. They demonstrate that the body plan of A. mackiei consisted of three distinct axes types and that the rooting axis was developed from root-bearing axes by anisotomous dichotomy.

    The main claims of the manuscript are supported by the data in overall, and the 3D reconstruction techniques used here are informative for broader readers. However, the discussion part of this manuscript should be strengthened to a larger extent, in order to clearly demonstrate the significance or implication of this discovery.

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  3. Reviewer #2 (Public Review):

    Hetherington et al. present a detailed three-dimensional reconstruction of the Rhynie chert vascular plant Asteroxylon mackei, an early lycophyte (club-moss). Rhynie chert fossils preserve exquisite details of anatomy, but our knowledge of the plants preserved in it are based primarily on dissociated thin sections rather than on relatively whole pieces of single plants. The authors present a novel method of three-dimensional reconstruction of Asteroxylon by cutting a length of axis into 31 thick sections, polishing and digitally photographing both sides and digitally stitching them together to produce a nearly 5 cm long reconstructed axis. Using this reconstruction, alongside details of the anatomy of the thick sections, they demonstrate the body plan of this early club-moss was divided into 3 main organs: leafy, largely orthotropic axes, sparsely leaved, plagiotropic root-bearing axes and rooting axes. Importantly, they show that both root-bearing axes and rooting axes in Asteroxylon originated at anisotomous branching points, providing additional support for the centrality of anisotomy in the evolution of complex morphology in vascular plants. In addition, the authors demonstrate that what they term rooting axes lack root caps and root hairs, in contrast to modern lycophytes (and other extant vascular plants). Finally, utilizing images of unrelated peels of another axis, they demonstrate that rooting axes in Asteroxylon underwent dichotomous branching, rather than forming endogenously like all modern lycophytes. These data show that the evolution of true roots proceeded in a stepwise pattern, and that true roots arose twice in the evolution of vascular plants.

    This is an excellent paper: it presents a novel technique for reconstruction of fossil plants, and demonstrates the value of this technique in elucidating the morphology of a basal lycophyte from the Rhynie chert, as well as important aspects of the evolution of roots. The illustrations and 3D reconstructions are clear, and fully support the authors' points.

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  4. Reviewer #3 (Public Review):

    This aim of the work is to investigates the structure and development of one of the oldest known rooting systems. It is based on exceptionally well-preserved fossil plants found in a 407-million-year-old geological site in Scotland.

    The authors use modern imaging techniques to assemble sections through stems and roots of petrified fossils to visualize the development of their organs and tissues. This is feasible because cellular details are preserved within the tissue systems. They demonstrate that the roots of the fossil plants are significantly different to those of modern lycopods (i.e., clubmosses), which are their closest living relatives. This extinct form of rooting system therefore appears to represent an early stage in the evolution of roots. The results are significant for understanding the evolution of roots, and they are relevant to interpreting results from molecular development research on the roots of modern plants, especially lycopods.

    A strength of the work is that it brings multiple lines of enquiry to bear on the central questions of root structure and development in the fossils. This is considered in relation to various types of organ category, including creeping rhizomes and upright leafy shoots. New preparations were made of fossil materials housed in the University of Munster (Germany), and historic collections were examined in The Natural History Museum, London (UK), and in the University of Wales, Cardiff (UK). These materials were prepared in different ways, providing complementary perspectives. The authors carefully document and explain how they interpret the fossils, and the inferences that they draw are well reasoned. The 3D reconstructions created from serial sections are particularly helpful in visualizing how the rooting system developed.

    The work is scholarly, explaining how it builds on previous research, and it references and discusses appropriate work on related living plants. The authors' claims and conclusions are well justified in so far as they apply to the rooting system and basal region of the plant, which is the focus of this work. The form and development of the leafy branching aerial system of the plant are less well evidenced. This aspect of their Figure 1G is a synthesis from other works, and I would say that it is less well supported by the data than their main conclusions about the rooting system.

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