An evidence-based 3D reconstruction of Asteroxylon mackiei, the most complex plant preserved from the Rhynie chert

Abstract

The Early Devonian Rhynie chert preserves the earliest terrestrial ecosystem and informs our understanding of early life on land. However, our knowledge of the 3D structure, and development of these plants is still rudimentary. Here we used digital 3D reconstruction techniques to produce the first well-evidenced reconstruction of the structure and development of the rooting system of the lycopsid Asteroxylon mackiei, the most complex plant in the Rhynie chert. The reconstruction reveals the organisation of the three distinct axis types – leafy shoot axes, root-bearing axes, and rooting axes – in the body plan. Combining this reconstruction with developmental data from fossilised meristems, we demonstrate that the A. mackiei rooting axis – a transitional lycophyte organ between the rootless ancestral state and true roots – developed from root-bearing axes by anisotomous dichotomy. Our discovery demonstrates how this unique organ developed and highlights the value of evidence-based reconstructions for understanding the development and evolution of the first complex vascular plants on Earth.

A permineralized Early Cretaceous lycopsid from China and the evolution of crown clubmosses

“…Against this background of previously described homosporous lycopsids, the excellent preservation of Lycopodicaulis oellgaardii is matched only by the quality of preservation seen in the putative lycopsid A. mackiei from the Rhynie Chert (Kidston & Lang, 1920, 1921; Kerp et al ., 2013; Hetherington et al ., 2021) from which A . mackiei differs in the absence of true microphylls, the presence of a strongly lacunate cortex, and a predominantly and poorly dissected actinostele.…”

“…Against this background of previously described homosporous lycopsids, the excellent preservation of Lycopodicaulis oellgaardii is matched only by the quality of preservation seen in the putative lycopsid A. mackiei from the Rhynie Chert (Kidston & Lang, 1920, 1921Kerp et al, 2013;Hetherington et al, 2021) from which A. mackiei differs in the absence of true microphylls, the presence of a strongly lacunate cortex, and a predominantly and poorly dissected actinostele. The well characterized anatomical and morphological features of Lycopodicaulis oellgaardii distinguish it from all other taxa in the extensive fossil record of the lycopsids and provide support for recognizing a new genus placed unequivocally in crown Lycopodiaceae that is most closely related to extant Lycopodioideae.…”

“…Despite the extensive record of Paleozoic and Mesozoic lycopsids, it has been challenging to recognize definitive fossils of crown‐group Lycopodiaceae (see Skog & Hill, 1992; Thomas, 1992; Bateman et al ., 2007; Thomas, 2017), largely due to a lack of fossils with anatomy preserved, the difficulties of confirming the absence of ligules and therefore distinguishing vegetative remains from the distal twigs of species of Lepidodendrales, (Taylor et al ., 2009). A potential early lycopsid is Asteroxylon mackiei Kidston & Lang, an intricate early land plant from the 407‐million‐year‐old Rhynie chert with unvascularized microphylls and a primitive actinostele (Kidston & Lang, 1920, 1921; Taylor et al ., 2009; Kerp et al ., 2013; Hetherington et al ., 2021). Another interesting Paleozoic plant, Hestia eremosa R.M.…”

Shared body plans of lycophytes inferred from root formation of Lycopodium clavatum

“…Drepanophycaleans have aerial shoot systems with dichotomies that resemble those of extant Lycopodiaceae Lang, 1920, 1921;Andrews, 1961;Kerp et al, 2013), although the "leaves" lack a distinct veinlet in many drepanophycaleans (Hueber, 1992;Kenrick and Crane, 1997). Meanwhile, they have subterranean axial organs (root-bearing axes sensu Tomescu (2016, 2017) and Hetherington et al (2021)), which branch exogenously from the aerial shoot axis. Rooting axes without a cap-like structure are born anisotomously from the subterranean axes (Hetherington and Dolan, 2018;Hetherington et al, 2021).…”

“…Meanwhile, they have subterranean axial organs (root-bearing axes sensu Tomescu (2016, 2017) and Hetherington et al (2021)), which branch exogenously from the aerial shoot axis. Rooting axes without a cap-like structure are born anisotomously from the subterranean axes (Hetherington and Dolan, 2018;Hetherington et al, 2021). In some drepanophycaleans, an aerial shoot axis gives rise to two daughter shoots by anisotomous dichotomy and one daughter shoot further branches anisotomously to form the subterranean axis and a shoot .…”