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The evolution of rooting structures was a crucial event in Earth’s history, increasing the ability of plants to extract water, mine for nutrients and anchor above-ground shoot systems. Fossil evidence indicates that roots evolved at least twice among vascular plants, in the euphyllophytes and independently in the lycophytes. Here, we review the anatomy and evolution of lycopsid rooting structures. Highlighting recent discoveries made with fossils we suggest that the evolution of lycopsid rooting structures displays two contrasting patterns – conservatism and disparity. The structures termed roots have remained structurally similar despite hundreds of millions of years of evolution – an example of remarkable conservatism. By contrast, and over the same time period, the organs that give rise to roots have diversified, resulting in the evolution of numerous novel and disparate organs.

The colonization of the land by streptophytes and their subsequent radiation is a major event in Earth history. We report a stepwise increase in the number of transcription factor (TF) families and subfamilies in Archaeplastida before the colonization of the land. The subsequent increase in TF number on land was through duplication within existing TF families and subfamilies. Almost all subfamilies of the Homeodomain (HD) and basic Helix-Loop-Helix (bHLH) had evolved before the radiation of extant land plant lineages from a common ancestor. We demonstrate that the evolution of these TF families independently followed similar trends in both plants and metazoans; almost all extant HD and bHLH subfamilies were present in the first land plants and in the last common ancestor of bilaterians. These findings reveal that the majority of innovation in plant and metazoan TF families occurred in the Precambrian before the Phanerozoic radiation of land plants and metazoans.

Rhizomorphic lycopsids are the land plant group that includes the first giant trees to grow on Earth and extant species in the genus Isoetes . Two mutually exclusive hypotheses account for the evolution of terminal rooting axes called rootlets among the rhizomorphic lycopsids. One hypothesis states that rootlets are true roots, like roots in other lycopsids. The other states that rootlets are modified leaves. Here we test predictions of each hypothesis by investigating gene expression in the leaves and rootlets of Isoetes echinospora . We assembled the de novo transcriptome of axenically cultured I. echinospora . Gene expression signatures of I. echinospora rootlets and leaves were different. Furthermore, gene expression signatures of I. echinospora rootlets were similar to gene expression signatures of true roots of Selaginella moellendorffii and Arabidopsis thaliana . RSL genes which positively regulate cell differentiation in roots were either exclusively or preferentially expressed in the I. echinospora rootlets, S. moellendorffii roots and A. thaliana roots compared to the leaves of each respective species. Taken together, gene expression data from the de-novo transcriptome of I. echinospora are consistent with the hypothesis that Isoetes rootlets are true roots and not modified leaves.

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.

Roots of extant vascular plants proliferate through lateral branching (euphyllophytes) or dichotomy (lycophytes) 1 – 4 . The origin of these distinct modes of branching was key for plant evolution because they enabled the development of structurally and functionally different root systems that supported a diversity of shoot systems 3 – 6 . It has been unclear when lateral branching originated and how many times it evolved 4 , 7 , 8 . Here, we report that many euphyllophytes that were extant during the Devonian and Carboniferous periods developed dichotomous roots. Our data indicate that dichotomous root branching evolved in both lycophytes and euphyllophytes. Lateral roots then evolved at different times in three major lineages of extant euphyllophytes—the lignophytes, ferns and horsetails. The multiple origins of dichotomous and lateral root branching are extreme cases of convergent evolution that occurred during the Devonian and Carboniferous periods when the land-plant flora underwent a radiation in morphological diversity. Dichotomous root branching evolved in both lycophytes and euphyllophytes, followed by lateral branching in separate extant lineages during the Devonian and Carboniferous periods, illustrating extreme cases of divergent evolution.

Two inorganic phosphate (Pi) uptake mechanisms operate in streptophytes and chloro-phytes, the two lineages of green plants. PHOSPHATE TRANSPORTER B (PTB) proteins are hypothesized to be the Na + /Pi symporters catalysing Pi uptake in chlorophytes, whereas PHOSPHATE TRANSPORTER 1 (PHT1) proteins are the H + /Pi symporters that carry out Pi uptake in angiosperms. PHT1 proteins are present in all streptophyte lineages. However, Pi uptake in streptophyte algae and marine angiosperms requires Na + influx, suggesting that Na + /Pi symporters also function in some streptophytes. We tested the hypothesis that Na + /Pi symporters exist in streptophytes. We identified PTB sequences in streptophyte genomes. Core PTB proteins are present at the plasma membrane of the liverwort Marchantia polymorpha. The expression of M. polymorpha core PTB proteins in the Saccharomyces cerevisiae pho2 mutant defective in high-affinity Pi transport rescues growth in low-Pi environments. Moreover, levels of core PTB mRNAs of M. polymorpha and the streptophyte alga Coleochaete nitellarum are higher in low-Pi than in Pi-replete conditions, consistent with a role in Pi uptake from the environment. We conclude that land plants inherited two Pi uptake mechanisms-mediated by the PTB and PHT1 proteins, respectively-from their streptophyte algal ancestor. Both systems operate in parallel in extant early diverging land plants.

This article is a Commentary on Meade et al. (2021), 229: 1782–1794.

There are two general types of rooting systems in extant land plants: gametophyte rhizoids and sporophyte root axes. These structures carry out the rooting function in the free-living stage of almost all land plant gametophytes and sporophytes, respectively. Extant vascular plants develop a dominant, free-living sporophyte on which roots form, with the exception of a small number of taxa that have secondarily lost roots. However, fossil evidence indicates that early vascular plants did not develop sporophyte roots. We propose that the common ancestor of vascular plants developed a unique rooting system—rhizoidal sporophyte axes. Here we present a synthesis and reinterpretation of the rootless sporophytes of Horneophyton lignieri, Aglaophyton majus, Rhynia gwynne-vaughanii and Nothia aphylla preserved in the Rhynie chert. We show that the sporophyte rooting structures of all four plants comprised regions of plagiotropic (horizontal) axes that developed unicellular rhizoids on their underside. These regions of axes with rhizoids developed bilateral symmetry making them distinct from the other regions which were radially symmetrical. We hypothesize that rhizoidal sporophyte axes constituted the rooting structures in the common ancestor of vascular plants because the phylogenetic positions of these plants span the origin of the vascular lineage. This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.

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.

Roots are one of the three fundamental organ systems of vascular plants 1 , and have roles in anchorage, symbiosis, and nutrient and water uptake 2 – 4 . However, the fragmentary nature of the fossil record obscures the origins of roots and makes it difficult to identify when the sole defining characteristic of extant roots—the presence of self-renewing structures called root meristems that are covered by a root cap at their apex 1 – 9 —evolved. Here we report the discovery of what are—to our knowledge—the oldest meristems of rooting axes, found in the earliest-preserved terrestrial ecosystem 10 (the 407-million-year-old Rhynie chert). These meristems, which belonged to the lycopsid Asteroxylon mackiei 11 – 14 , lacked root caps and instead developed a continuous epidermis over the surface of the meristem. The rooting axes and meristems of A. mackiei are unique among vascular plants. These data support the hypothesis that roots, as defined in extant vascular plants by the presence of a root cap 7 , were a late innovation in the vascular lineage. Roots therefore acquired traits in a stepwise fashion. The relatively late origin in lycophytes of roots with caps is consistent with the hypothesis that roots evolved multiple times 2 rather than having a single origin 1 , and the extensive similarities between lycophyte and euphyllophyte roots 15 – 18 therefore represent examples of convergent evolution. The key phylogenetic position of A. mackiei —with its transitional rooting organ—between early diverging land plants that lacked roots and derived plants that developed roots demonstrates how roots were ‘assembled’ during the course of plant evolution. Meristems of the rooting axes of Asteroxylon mackiei preserved in 407-million-year-old Rhynie chert lack root caps, which demonstrates that the evolution of the root systems of modern vascular plants occurred in a stepwise fashion.