"Roots evolved at least twice during the early radiation of vascular plants (Tracheophytes; Kenrick & Strullu-Derrien, 2014; Hetherington et al., 2016), namely in Lycophytes and Euphyllophytes (Fig. 5). In contrast to the wealth of information from plants with rhizoid-based rooting systems from the Rhynie chert, knowledge of fungal symbioses associated with the primitive roots remains surprisingly limited. Nothing is known about fungal mycorrhizal symbionts in the rooting systems of the trees in the earliest forests of the Mid and Late Devonian (398–359 million yr ago (Ma); Morris et al., 2015). These forests were formed by Cladoxylales (an extinct group of uncertain affinities, reproducing by spores) (Xu et al., 2017) and progymnosperms, (a group of plants reproducing by spores but with secondary growth of the vascular tissues similar to true gymnosperms; Figs 3, 5). Improving our knowledge of early root symbionts would benefit from an approach that targets specifically permineralized rooting systems (e.g. specimens from China; Xu et al., 2017) and focuses on documenting the fungal component.

By the Carboniferous Period (359–299 Ma), forests containing extinct vascular plants, including arborescent Lycopsida (clubmosses), ferns, sphenopsids, pteridosperms (or seed ferns, a polyphyletic collection of distinct groups of extinct seed plants with fern foliage), Cordaites (sister group to conifers) and conifers (Taylor et al., 2009; Fig. 5) were well established in lowland coastal sites. The earliest evidence of mycorrhizas confined to roots comes from fossils preserved in carbonate concretions of Late Carboniferous age (c. 315 Ma; Box 3). An AM fungus was reported colonizing the tips of the rootlets of an arborescent clubmoss (Krings et al., 2011c) (Figs 1, 3, 4d, 5). Large vesicles or spores were attached to hyphal threads, while other hyphae penetrated cortical cells where they formed arbuscules. AM fungi were also documented in a Cordaites tree (Strullu-Derrien et al., 2009) preserved in cherts from the Late Carboniferous (Figs 1, 3, 4e, 5). The fungus developed an extensive intracellular phase without vesicle formation. Small arbuscules formed within the cortical cells, except for those that developed bands of secondary wall (‘phi thickenings’) reinforcing the primary wall (Idris & Collins, 2015).


A key difference between the rootlets of the lycophyte and those of the Cordaites is that the latter possess an endodermis, which is a ring of cells surrounding the vascular system whose cell walls contain hydrophobic substances. The endodermis is speculated to have been important in the evolution of true mycorrhizas by acting as a barrier to the fungal colonization of the vascular system (Strullu-Derrien et al., 2009). As roots in lycophytes and other vascular plants evolved independently (Kenrick & Strullu-Derrien, 2014), mycorrhizas in both Lycophytes and Cordaites may indicate at least two separate origins for root colonization. The shift from paramycorrhizas to true mycorrhizas (i.e. fungi harboured in root cortex exclusively) occurred in the rooting systems of the sporophytic (diploid) generation of vascular plants. While extant roots are sometimes viewed as organs exploiting soil autonomously, and they perform this function in nonmycorrhizal plants, it has been hypothesized that roots first evolved as symbiotic axes, interacting with soil fungi (Brundrett, 2002). Strikingly, similar underground interaction organs also evolved in some liverworts, namely the underground ‘flagelliform axes’ that are densely colonized by soil fungi (Read et al., 2000; Selosse, 2005)."