Networks of highly branched stigmarian rootlets developed on the first giant trees

Abstract

Lycophyte trees, up to 50 m in height, were the tallest in the Carboniferous coal swamp forests. The similarity in their shoot and root morphology led to the hypothesis that their rooting (stigmarian) systems were modified leafy shoot systems, distinct from the roots of all other plants. Each consists of a branching main axis covered on all sides by lateral structures in a phyllotactic arrangement; unbranched microphylls developed from shoot axes, and largely unbranched stigmarian rootlets developed from rhizomorphs axes. Here, we reexamined the morphology of extinct stigmarian systems preserved as compression fossils and in coal balls from the Carboniferous period. Contrary to the long-standing view of stigmarian systems, where shoot-like rhizomorph axes developed largely unbranched, root-hairless rootlets, here we report that stigmarian rootlets were highly branched, developed at a density of ∼25,600 terminal rootlets per meter of rhizomorph, and were covered in root hairs. Furthermore, we show that this architecture is conserved among their only extant relatives, herbaceous plants in the Isoetes genus. Therefore, despite the difference in stature and the time that has elapsed, we conclude that both extant and extinct rhizomorphic lycopsids have the same rootlet system architecture.evolution | paleobotany | Carboniferous forests | stigmarian root systems | Isoetes T he spread of the first wetland forests with tall trees during the Carboniferous period (359-300 million years ago) had a dramatic impact on the carbon cycle by burying large amounts of organic carbon in the form of peat in coal swamps (1, 2). Lycophyte trees up to 50 m in height (3, 4) were dominant components of coal swamp forests (5, 6). They were key components of coal-forming environments throughout the Carboniferous period but dominated in the lower-middle Pennsylvanian (Namurian-Wetsphalian) where they typically contribute between 60% and 95% of the biomass in buried peat (7-13). The preserved remains of lycophyte trees form some of the most extensive fossil plant deposits of any geological period. This is in part because of their size and ecological dominance but also the result of the high probability of preservation in the waterlogged conditions in which these trees grew (4). Detailed descriptions of the morphology of these plants on a range of scales-from entire in situ tree lycophyte forests (14, 15) to cellular descriptions of developing spores (16)-have made these trees some of the best understood fossil plants of the Carboniferous coal swamps.The rooting system of the arborescent lycopsids-stigmarian systems-consist of large shoot-like axes (rhizomorphs) that develop lateral organs called rootlets (4,(17)(18)(19)(20). Rootlets, which have been described as largely unbranched and root hairless (4,5,(17)(18)(19)(20)(21)(22)(23)(24), are arranged in a characteristic pattern or rhizotaxy on the rhizomorph (25). It is the arrangement of these largely unbranched leaf-like rootlets on a shoot-like axis that first led to the theory that stigm...

The adaptive value of heterospory: Evidence from Selaginella

“…Lepidosigillaria whitei , considered to be isoetalean due to similarities in rooting system architecture with Isoetes (Pigg ; Hetherington et al. ), constrained the divergence of Isoetaceae from Selaginellaceae to a minimum of 370 Ma (prior: exponential, Ma). The second fossil, Selaginella suissei , an early anisophyllous, dichotomously branching, heterosporous fossil clearly within the genus, constrained the crown group of Selaginella to a minimum of 310 Ma (prior: exponential, Ma) (Thomas ; Arrigo et al.…”

The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics

“…Roots evolved at least twice during the early radiation of vascular plants (Tracheophytes; Kenrick & Strullu‐Derrien, ; Hetherington et al ., ), namely in Lycophytes and Euphyllophytes (Fig. ).…”

The evolution of lycopsid rooting structures: conservatism and disparity

“…We recently discovered that the roots of the giant tree lycopsids developed root hairs (Fig. h) and had the same root architecture as extant Isoetes (Hetherington et al ., ). This root architecture is conserved in all geological periods – from Devonian through to today (Kidston & Lang, , ; Foster & Gifford, ; Phillips & Leisman, ; Bhutta, ; Stewart & Rothwell, ; Hetherington et al ., ; Matsunaga & Tomescu, ).…”