Root evolution at the base of the lycophyte clade: insights from an Early Devonian lycophyte

Background and Aims The evolution of complex rooting systems during the Devonian had significant impacts on global terrestrial ecosystems and the evolution of plant body plans. However, detailed understanding of the pathways of root evolution and the architecture of early rooting systems is currently lacking. We describe the architecture and resolve the structural homology of the rooting system of an Early Devonian basal lycophyte. Insights gained from these fossils are used to address lycophyte root evolution and homology. Methods Plant fossils are preserved as carbonaceous compressions at Cottonwood Canyon (Wyoming), in the Lochkovian-Pragian (similar to 411 Ma; Early Devonian) Beartooth Butte Formation. We analysed 177 rock specimens and documented morphology, cuticular anatomy and structural relationships, as well as stratigraphic position and taphonomic conditions. Key Results The rooting system of the Cottonwood Canyon lycophyte is composed of modified stems that bear fine, dichotomously branching lateral roots. These modified stems, referred to as root-bearing axes, are produced at branching points of the above-ground shoot system. Root-bearing axes preserved in growth position exhibit evidence of positive gravitropism, whereas the lateral roots extend horizontally. Consistent recurrence of these features in successive populations of the plant preserved in situ demonstrates that they represent constitutive structural traits and not opportunistic responses of a flexible developmental programme. Conclusions This is the oldest direct evidence for a rooting system preserved in growth position. These rooting systems, which can be traced to a parent plant, include some of the earliest roots known to date and demonstrate that substantial plant-substrate interactions were under way by Early Devonian time. The morphological relationships between stems, root-bearing axes and roots corroborate evidence that positive gravitropism and root identity were evolutionarily uncoupled in lycophytes, and challenge the hypothesis that roots evolved from branches of the above-ground axial system, suggesting instead that lycophyte roots arose as a novel organ.