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Remarkable preservation in coalified and pennineralized fossils from Upper Silurian and Lower Devonian sediments deposited some 420 to 390 million years ago provides insight into the major anatomical innovations associated with the early stages in the colonization of the land by higher plants. Using uniformitarian principles, such information, combined with gross morphology, can then be used to reconstruct the pioneers as growing, metabolizing and reproducing organisms, as well as allowing assessment of affinity, although apart from the lycophytes, they have no close relationship with extant groups. In considering vascular tissues, diversity is exemplified by descriptions of the metaxylem in protosteles of Zosterophyllopsida and Drepanophycopsida (putative lycophytes), of Psilophyton (Trimerophytopsida), of the Rhyniaceae (including Rhynia gwynnevaughanii, certain Taeniocrada spp., Sennicaulis) and of Cooksonia pertoni, a Lower Devonian representative of the organization found in the oldest pteridophyte-like land plants. Aglaophyton major is included as a plant with bryophyte-like vascular tissues in a branching sporophyte with cuticle, stomata and intercellular space system typical of the homoiohydric tracheophyte. In all water-conducting cells, interpretation of the primary and secondary wall results from comparisons involving the anatomy and chemistry of extant examples and an understanding of taphonomic processes. Phloem is only rarely preserved and usually identified from its position around the xylem. In contrast, dermal features are better known, because of penetration of the resilient cuticle between epidermal cells. They appear conservative. Thus stomata with two guard cells look remarkably similar to extant forms in surface view, and by consideration of their relationship with surrounding epidermal cells and of extent of cuticularization, seem to have operated in a similar way to those in certain mosses and ferns. Cuticular ornamentation (papillae, striations) and epidermal outgrowths (unicellular and multicellular) are described and their adaptive significance conjectured. Ground tissue systems are best preserved in Rhynie Chert permineralizations where zonation of the cortex is tentatively related to photosynthetic and structural roles. The latter function is also attributed to thick-walled, outer cortical cells recorded in many zosterophylls and in Psilophyton, although the chemical nature of the walls themselves remains equivocal. Problems of identification of roots in plants possessing axial organization with exarch xylem, and in leafy plants with smooth lateral branching systems are briefly addressed. Finally axis apices in Rhynia givynne-vaughanii and sections showing stages in the maturation of Asteroxylon stems are described from the Rhynie Chert. Contents Summary 225 I. Introduction 226 II. Vascular systems 226 III. Dermal systems 237 IV. Ground tissue systems 241 V. Apical meristems 244 VI. Distinction of aerial stems, rhizomes and roots 245 VII. Why anatomy? 245 Acknowledgements 245 References 245.

The 407-million-year-old 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 complete reconstruction of the lycopsid Asteroxylon mackiei, the most complex plant in the Rhynie chert. The reconstruction reveals the organisation of the three distinct axes 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 plants on Earth.

Mathematical models of fluid flow through and embolism resistance of extinct plant xylem provide insight into the ecology and physiology of individual fossil plants. Disparate lineages of vascular plants exhibit a variety of ecophysiological strategies: extreme adaptations for maximum flow and maximum safety have both been documented in living and extinct plants. Analysis of early-diverging vascular plants and early-diverging seed plants shows that a variety of hydraulic strategies were pursued early in the evolution of terrestrial plants, especially during the Devonian and Carboniferous Periods. Analysis of five species of the Lower and Middle Devonian trimerophyte genus Psilophyton indicates that some species possess low-resistance metaxylem tracheids with numerous, highly porous pits and relatively low embolism resistance, whereas other species contain xylem with higher embolism resistance and lower hydraulic conductivity. Despite a simple vegetative morphology, physiological analysis of several Psilophyton fossils suggests that species possessed distinct ecophysiological strategies and there may be cryptic functional diversity within other trimerophyte genera. When integrated with previous hydraulic analyses of extinct and extant plants, including the Lower Devonian stem group lycophyte Asteroxylon mackiei; a series of Carboniferous stem group seed plants, including Medullosa, Callistophyton, and Lyginopteris; eleven genera of extant conifers and cycads; two species of ginkgophytes, and others, the occupation of tracheid-based hydraulic ecospace can be mapped. Soon after the evolution of vascular tissue in land plants, the high-conductivity/low-safety-margin space was occupied; particularly by plants that grew in the tropical lowland swamps during the Carboniferous Period. Upon the disappearance of the coal swamp floras during the Permian Period, that portion of the ecospace may have remained unoccupied until the evolution of angiosperms with vessels in the Cretaceous Period. Taken as a whole, the evolution of vascular tissue during (and after) the terrestrialization process records several physiological adaptive radiations, occurring early in plant evolution, which likely had major effects on global environmental and biogeochemical processes.

Mapping fossil traits onto the land plant phylogenetic framework indicates that there were at least two independent origins of roots among extant vascular plants — once in lycophytes and independently in euphyllophytes. At least two rooting structural types are found among extinct species preserved in the Rhynie chert. First, species that lacked roots and developed horizontal axes that developed rhizoids. Second, the rooting axes of Asteroxylon mackiei resembled the roots of extant lycopsids but lacked root hairs and root caps. These two rooting structures preceded the evolution of the roots of extant lycophytes comprising axes on which root hairs and root caps developed. These data demonstrate the defining root characters evolved gradually in the lycophyte lineage.

Roots are one of the three fundamental organ systems of vascular plants1, and have roles in anchorage, symbiosis, and nutrient and water uptake2–4. 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 apex1–9—evolved. Here we report the discovery of what are—to our knowledge—the oldest meristems of rooting axes, found in the earliest-preserved terrestrial ecosystem10 (the 407-million-year-old Rhynie chert). These meristems, which belonged to the lycopsid Asteroxylon mackiei11–14, 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 cap7, 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 times2 rather than having a single origin1, and the extensive similarities between lycophyte and euphyllophyte roots15–18 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.

Brief descriptions and comments on relationships are given for the seven embryophytic sporophytes in the cherts at Rhynie, Aberdeenshire, Scotland. They are Rhynia gwynnevaughanii Kidston & Lang, Aglaophyton major D. S. Edwards, Horneophyton lignieri Barghoorn & Darrah, Asteroxylon mackiei Kidston & Lang, Nothia aphylla Lyon ex Høeg, Trichopherophyton teuchansii Lyon & Edwards and Ventarura lyonii Powell, Edwards & Trewin. The superb preservation of the silica permineralisations produced in the hot spring environment provides remarkable insights into the anatomy of early land plants which are not available from compression fossils and other modes of permineralisation. They include soft tissues, such as those surrounding stomata, rhizoids, apical and lateral meristems, and diversity in conducting cells, with inferences for palaeoecophysiology, including water use efficiency, transport and absorption, and for growth processes and patterns.

Anatomically preserved land plant fossils from the Lower Devonian Rhynie Chert contain conducting tissues with cells that range from dark-colored, elongated cells without secondary wall thickenings to tracheids similar to those of extant tracheophytes. A suite of tissue-specific microanalytical techniques was used to assess lignification in fossils of Aglaophyton, Rhynia, and Asteroxylon. Isotope ratio mass spectrometry provides millimeter-scale resolution of carbon isotopic abundances, whereas soft X-ray carbon (1s) spectromicroscopy provides micrometer-scale resolution of the preservation of organic molecular functionality. The isotopic and organic chemistry of Rhynie Chert plants indicates that the earliest vascular thickenings were probably unlignified and that cell wall lignification may have first appeared in the outer cortex. Only in more derived plants, it seems, was lignin deposited in conducting cells to produce the true tracheids seen today in vascular plants.

New morphometric data gathered from cross-sections of two Lower Devonian land plants (Rhynia gwynne-vaughanii and Asteroxylon mackiei) are interpreted in terms of the evolution of the function of vascular bundles in early land plants. The following conclusions can be drawn from these new data: (1) The ratio of the cross-sectional area of the xylem (representing the conducting volume supplying the axis with water) to the xylem perimeter (representing the “contact area” between xylem and parenchyma through which water leaves the xylem and enters the parenchyma) is not constant for Rhynia axes, almost constant for Asteroxylon axes, and different between Rhynia and Asteroxylon. Thus, Bowers hypothesis that the ratio of cross-sectional area of the xylem to xylem perimeter is constant during ontogenetic development is true for Asteroxylon. That this ratio is constant during phylogeny, however, is not supported by our data. (2) The ratio between cross-sectional area of xylem to parenchyma is higher in Asteroxylon than in Rhynia. (3) As predicted by previous computer simulations, the ratio of the xylem perimeter to the axis perimeter plays a major role in determining water transport performance of the transpiring axis. This ratio is constant within ontogeny but is different in Asteroxylon and Rhynia. In Asteroxylon axes, this ratio is about twice as large as in Rhynia axes. (4) Contrary to the expectations, the distance between the outermost layer of the xylem and the transpiring surface, which represents the low-conductivity pathway through the parenchyma, appears not to be a limiting factor for the water transport in axes of Rhynia and Asteroxylon. (5) From the analysis of the geometric parameters, it is evident that Rhynia and Asteroxylon with their distinct stelar geometries represent two different constructional types for which no transitional stages are known.

The core of plant physiology is a set of functional solutions to a tradeoff between CO_2 acquisition and water loss. To provide an important evolutionary perspective on how the earliest land plants met this tradeoff, we constructed a mathematical model (constrained geometrically with measurements of fossils) of the hydraulic resistance of Asteroxylon, an Early Devonian plant. The model results illuminate the water transport physiology of one of the earliest vascular plants. Results show that Asteroxylon’s vascular system contains cells with low hydraulic resistances; these resistances are low because cells were covered by scalariform pits, elliptical structures that permit individual cells to have large areas for water to pass fromone cell to another. Asteroxylon could move a large amount of water quickly given its large pit areas; however, this would have left these plants particularly vulnerable to damage from excessive evapotranspiration. These results highlight a repeated pattern in plant evolution, wherein the evolution of highly conductive vascular tissue precedes the appearance of adaptations to increase water transport safety. Quantitative insight into the vascular transport of Asteroxylon also allows us to reflect on the quality of CO_2 proxy estimates based on early land plant fossils. Because Asteroxylon’s vascular tissue lacked any safety features to prevent permanent damage, it probably used stomatal abundance and behavior to prevent desiccation. If correct, low stomatal frequencies in Asteroxylon reflect the need to limit evapotranspiration, rather than adaptation to high CO_2 concentrations in the atmosphere. More broadly, methods to reveal and understand water transport in extinct plants have a clear use in testing and bolstering fossil plant-based paleoclimate proxies.

Wall structure in the water-conducting cells of Rhynia gwynne-vaughanii and Asteroxylon mackiei from the Lower Devonian Rhynie Chert was examined and compared using thin sections and scanning electron microscopy of etched sections. Although the internal thickenings of these cells are superficially similar in both plants, there are significant differences in other aspects of wall structure. The tracheids of A. mackiei are shown to be of a basic type (G-type) that is common in some early land plant fossils such as zosterophylls and lycopods, and they are comparable to protoxylem elements in some extant `pteridophytes'. The "tracheids" of R. gwynne-vaughanii are more similar to another kind of water-conducting cell (S-type) that combines certain features of tracheids and moss hydroids. The S-type cell is known from two other Lower Devonian sporophytes, Stockmansella langii and Huvenia kleui, supporting recent suggestions that these three taxa form a natural group. S-type cells are also found in the gametophy...

We describe a perithecial, pleomorphic ascomycetous fungus from the Early Devonian (400 mya) Rhynie chert; the fungus occurs in the cortex just beneath the epidermis of aerial stems and rhizomes of the vascular plant Asteroxylon. Perithecia are nearly spherical with a short, ostiolate neck that extends into a substomatal chamber of the host plant; periphyses line the inner surface of the ostiole. The ascocarp wall is multilayered and formed of septate hyphae; extending from the inner surface are elongate asci interspersed with delicate paraphyses. Asci appear to be unitunicate and contain up to 16 smooth, uniseriate-biseriate ascospores. The method of ascospore liberation is unknown; however, the tip of the ascus is characterized by a narrow, slightly elevated circular collar. Ascospores appear 1-5 celled, and germination is from one end of the spore. Also present along the stems and interspersed among the perithecia are acervuli of conidiophores that are interpreted as the anamorph of the fungus. Conidiogenesis is thallic, basipetal and probably of the holoarthric-type; arthrospores are cube-shaped. Some perithecia contain mycoparasites in the form of hyphae and thick-walled spores of various sizes. The structure and morphology of the fossil fungus is compared with modern ascomycetes that produce perithecial ascocarps, and characters that define the fungus are considered in the context of ascomycete phylogeny.

Biophysical methods allow quantitative deductions as to the “bending effectivity” of various stele types and the contribution of different tissues to the stability of upright plant axes. Considering the first occurrence of the different stele types in geological history, a strong tendency towards a higher “bending effectivity” can be observed. It can be shown that Rhynia gwynne-vaughanii, Aglaophyton major (Rhynia major) and Asteroxylon mackiei as well as probably the vast majority of early “vascular” land plants were turgor systems, i.e. that the parenchyma (when fully turgescent) is by far the most important contributory factor towards the bending stability of the upright axes.

Naked branched axes associated with sporangia, originally described by Kidston and Lang (1920) as the probable fertile region of Asteroxylon mackiei, were later shown by Lyon (1964) to belong to an unknown plant which he named Nothia aphylla. The name was validated by Hoeg in 1967. Nothia aphylla is described here in greater detail from new material collected from the Rhynie locality. The sporangia are lateral in terminal branched spikes. Their arrangement ranges from spiral to semiverticillate. The fertile axes terminate in clusters of 2–5 sporangia. The stalked sporangia are rather reniform with a distal transversely-extended dehiscence slit. Systematically Nothia has similarities to both Zosterophyllophytina and Rhyniophytina.

N I923 Drs Krausel and Weyland published a paper on the lDevonian Flora of the neighbourhood of Elberfeld1. This work, though containing much of interest, was to some extent a preliminary notice; since then important new researches have been carried out, and the authors' second paper, published this summer2, is the most considerable contribution to Devonian palaeobotany since the Rhynie discoveries. It is on this second paper that the following remarks are based. The specimens came from several localities near Elberfeld. Use was made of various public and private collections especially those of Herr Piedboeuf, who gave much help. The new finds seem to have been chiefly made in the quarry at Kirberg. The horizon is that of the "Honseler Schichten," belonging to the lowest division of the upper Middle Devonian. It is a fortunate circumstance that the plant remains, while showing the external habit, are often partly petrified, allowing of anatomical investigation. Owing to the nature of this petrification no thin sections could be made; polished surfaces were therefore examined, in reflected light, with good results. Five plants are described. Others still remain to be investigated. The plants dealt with are: Asteroxylon elberfeldense n. sp., Aneurophyion germanicum K. and W., Hyenia elegans n. sp., Calamophyion primaevum n. gen. et sp., Cladoxylon scoparium n. sp. The Asteroxylon is of great interest, for comparison with the now well-known Rhynie species. Branching, naked axes, formerly referred to Hostiimella, are extremely common in the deposit. The ends of the shoots are sometimes circinate. In two cases a sporangium was found terminating a branch. It is now shown that these "Hostimella" branches pass over below into spiny stems, of the Psilophy5on type. Still lower down, the thorny axes are continuous with stems bearing

Asteroxylon Mackiei was a plant of more complicated organisation and larger size than either Rhynia or Hornea, which have been described from the silicified peat-bed at Rhynie in the two preceding papers of this series. The generic name refers to the stellate outline of the xylem of the stem as seen in cross section, while the specific name commemorates the original discovery of the plant remains by Dr Mackie.

Selaginella harrisiana ap. nov. is described from the Permian (Kungurian) Upper Coal Measures at Victoria Pass, N.S.W. It resembles Selaginella selaginoides in its leafy parts but has a long leafless rhizome recalling Asteroxylon. The present evidence suggests that the herbaceous and arborescent ly copsids are taxonomically remote.

The remarkable growth of paleobotany within recent years is revealed in the expanded body of literature and by the increase in number of languages in which it is written. New techniques are involved in the use of cuticles and the electron microscope. Precambrian rocks, once regarded as essentially without fossils, have been found to contain a variety of micro-organisms, and compounds believed to be decomposition products of chlorophyll have been identified in rocks three billion years old. Some new ideas have developed concerning the morphology and relationships of some of the very old vascular plants. The original reconstruction of Psilophyton embodied more than one plant, and Asteroxylon now appears to be a lycopod. The Hyeniales and Pseudosporochnus belong to the Cladoxylales. Archaeopteris and Callixylon are the foliage and woody trunks of the same plant which has been designated a “progymnosperm”. Seeds now appear to have been recognized in the Upper Devonian, and a considerable number of primitive seeds have lately been found in the Lower Carboniferous calciferous sandstone. Decreased coal mining has curtailed the supply of Carboniferous compressions. In North America outstanding progress has been made in the study of petrified plants in coal balls. Studies of the Glossopteris flora have been extended into Antarctica. Continental drift seems to be the only hypothesis that satisfactorily explains the position of the fragments of ancient Gondwanaland at the present time. Reinvestigations of the inflorescences of Cycadeoidea have shown that the structure of the staminate disc was originally misinterpreted. It is a complex synangium that encircles the gynoecium, rather than being a whorl of pinnate stamens. The occurrence of angiosperm leaves in the Lower Cretaceous of Greenland is questioned. Some investigators now believe that angiosperms originated at high altitudes in the tropics during the Permian Period. Others would derive them from the Glossopteridae during the same period. Fruits and seeds have proved quite useful in accurate determination of Tertiary angiosperms. Petrified woods create special problems in identification and nomenclature.

Summary An investigation of the cuticle of Psilophyton princeps Dawson from the original locality in Canada has revealed the presence of stomata on the epidermis of the stem. This epidermis resembles in a general wily that of the petrified members of the Psilophytales from the Rhynie Chert, but the stomata differ in the presence of cuticular thickenings and the epidermal cells are usually papillate and not ridged. In the numerical distribution of stomata on the stem, Psilophyton agrees with Asteroxylon rather than Rhynia. There is no evidence that the highly cuticularised spines are homologous with the traumatic intumescences of Rhynia, and they differ from the slightly larger and less spine-like leaves of Asteroxylon, with which a closer comparison is possible, in the absence of stomata.

This part of the account of our examination of the plants preserved in the silicified peat-bed of early Old Red Sandstone age found at Rhynie will be devoted to the consideration of a number of general questions concerning the four Vascular Cryptogams which it has yielded.1. In the first place the morphological characters of Rhynia Gwynne-Vaughani, R. major, Hornea, and Asteroxylon will be reviewed and the attempt made to reconstruct the external appearance of these plants as they grew. In relation to this a few additional features of the plants will be described.2. This will lead naturally to a consideration of the general bearings upon plant-morphology of the facts mentioned in this series of papers.

In Part I a general account was given of the silicified peat-bed found at Rhynie, and one vascular plant was described in detail under the name of Rhynia Gwynne-Vaughani. Further study has shown that there are two species of Rhynia which we now distinguish as Rhynia Gwynne-Vaughani and Rhynia major. The account in Part I applies to both these species. Along with them there occurs a plant of similar grade of organisation to Rhynia, though quite distinct from that genus: this we name Hornea Lignieri. Asteroxylon Machiei, on the other hand, which will be described in the next part, was a plant of larger size and much more complex morphology.We are thus now able to establish the existence and main features of four archaic Vascular Cryptogams from the Rhynie bed. In the present paper additional notes on R. Gwynne-Vaughani are given, and R. major and Hornea Lignieri described in detail. In conclusion, the morphological bearings of the facts will be briefly considered.

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.

Funder: Biotechnology and Biological Sciences Research Council, 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.

Asteroxylon mackiei was first described from the Rhynie Chert by Kidston and Lang1, but the nature of its reproductive region has remained uncertain, since the peculiar leafless axes and small pear-shaped sporangia, which they provisionally assigned to the plant, have never been found connected to its leafy stems.