Leaves and sporangia developed in rare non-Fibonacci spirals in early leafy plants.

Lateral plant organs, including leaves and reproductive structures, are arranged on stems in distinct patterns termed phyllotaxis. Most extant plants exhibit phyllotactic patterns that are mathematically described by the Fibonacci series. However, it remains unclear what lateral organ arrangements were present in early leafy plants. To investigate this, we quantified phyllotaxis in fossils of the Early Devonian lycopod Asteroxylon mackiei. We report diverse phyllotaxis in leaves, including whorls and spirals. Spirals were all n:(n+1) non-Fibonacci types. We also show that leaves and reproductive structures occurred in the same phyllotactic series, indicating developmental similarities between the organs. Our findings shed light on the long-standing debate about leaf origins and demonstrate the antiquity of non-Fibonacci spirals in plants.

An evidence-based 3D reconstruction of Asteroxylon mackiei, the most complex plant preserved from the Rhynie chert.

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.

Archaeosporites rhyniensis gen. et sp. nov. (Glomeromycota, Archaeosporaceae) from the Lower Devonian Rhynie chert: a fungal lineage morphologically unchanged for more than 400 million years.

BACKGROUND AND AIMS: Structurally preserved arbuscular mycorrhizas from the Lower Devonian Rhynie chert represent core fossil evidence of the evolutionary history of mycorrhizal systems. Moreover, Rhynie chert fossils of glomeromycotan propagules suggest that this lineage of arbuscular fungi was morphologically diverse by the Early Devonian; however, only a small fraction of this diversity has been formally described and critically evaluated. METHODS: Thin sections, previously prepared by grinding wafers of chert from the Rhynie beds, were studied by transmitted light microscopy. Fossils corresponding to the description of Archaeospora spp. occurred in 29 slides, and were measured, photographed and compared with modern-day species in that genus. KEY RESULTS: Sessile propagules <85 µm in diameter, some still attached to a sporiferous saccule, were found in early land plant axes and the chert matrix; they developed, in a similar manner to extant Archaeospora, laterally or centrally within the saccule neck. Microscopic examination and comparison with extant fungi showed that, morphologically, the fossils share the characters used to circumscribe the genus Archaeospora (Glomeromycota; Archaeosporales; Archaeosporaceae). CONCLUSIONS: The fossils can be assigned with confidence to the extant family Archaeosporaceae, but because molecular analysis is necessary to place organisms in these taxa to present-day genera and species, they are placed in a newly proposed fossil taxon, Archaeosporites rhyniensis.

A hidden cradle of plant evolution in Permian tropical lowlands.

The latitudinal biodiversity gradient today has deep roots in the evolutionary history of Earth's biota over geologic time. In the marine realm, earliest fossil occurrences at low latitudes reveal a tropical cradle for many animal groups. However, the terrestrial fossil record-especially from drier environments that are thought to drive evolutionary innovation-is sparse. We present mixed plant-fossil assemblages from Permian equatorial lowlands in present-day Jordan that harbor precocious records of three major seed-plant lineages that all became dominant during the Mesozoic, including the oldest representative of any living conifer family. These finds offer a glimpse of the early evolutionary origins of modern plant groups in disturbance-prone tropical habitats that are usually hidden from observation.

Organs and tissues of Rhynie chert plants.

The Early Devonian Rhynie chert and the nearby Windyfield chert contain the oldest in situ preserved terrestrial ecosystem. Two of the seven species of anatomically preserved land plants had naked axes, one an axis with a more or less regular pattern of short-longitudinal ribs, two species had spiny axes and one species had small leaf-like appendages. All plants mainly consist of parenchymatous tissues. In some species, conducting elements comprise uniformly thickened thick-walled cells resembling hydroids of larger bryophytes, whereas others have real tracheids with annular and/or spiral secondary wall thickenings. True phloem has never been demonstrated but in all species the thick-walled water-conducting cells are encircled by a zone of thin-walled cells without intercellular spaces. The cortex is differentiated into two or three zones and forms the major part of the axes; in one species the cells of the middle cortex are sclerified. Some species have a hypodermis. In all species the epidermis is covered by a well-developed cuticle. Sporangia are known from all species. Sporangia are spindle-shaped, lobed or kidney-shaped and attached terminally or laterally with a short stalk. Gametophytes of four species have been described. Gametophytes are unisexual, isomorphic but much smaller than the sporophytes.This article is part of a discussion meeting issue 'The Rhynie cherts: our earliest terrestrial ecosystem revisited'.

Leaf anatomy of a late Palaeozoic cycad.

Today, cycads are a small group of gymnospermous plants with a limited distribution in the (sub)tropics, but they were major constituents of Mesozoic floras. Fossil leaves sporadically found in latest Carboniferous and Permian floras have putatively been ascribed to cycads. However, their true affinity remains unclear due to the lack of anatomical evidence. Virtually all modern cycads have pinnate leaves, but this type of leaf morphology is by no means unique for cycads. Pinnate leaves of Plagiozamites oblongifolius Halle 1927 with well-preserved cuticles showing the epidermal anatomy are here described from the upper Permian Xuanwei Formation of Yunnan Province, Southwest China. The cuticles show a clear differentiation into costal and intercostal zones; stomata are confined to the intercostal zones on both the upper and lower leaf surfaces. The external morphology and the epidermal anatomy of these fossil leaves are closely comparable with those of extant cycads, particularly members of the family Zamiaceae.

Early Devonian (~410 mya) microfossils resembling Characiopsis (Tribophyceae) and Characium (Chlorophyceae).

Unusual microfossils that occurred associated with fungal spores in the Lower Devonian (~410 mya) Windyfield chert from Scotland were composed of a narrow stipe (2.5-9 µm long) to which was attached an obovoid or elongate drop-shaped cell up to 14 µm long; a basal attachment pad was present in several specimens. The fossils were strikingly similar morphologically to certain present-day unicellular freshwater Tribophyceae and Chlorophyceae, but affinities to the fungal phylum Chytridiomycota also cannot be ruled out. This discovery adds to the inventory of distinctive microbial morphologies in the early non-marine paleoecosystems.

Complete tylosis formation in a latest Permian conifer stem.

BACKGROUND AND AIMS: Our knowledge of tylosis formation is mainly based on observations of extant plants; however, its developmental and functional significance are less well understood in fossil plants. This study, for the first time, describes a complete tylosis formation in a fossil woody conifer and discusses its ecophysiological implications. METHODS: The permineralized stem of Shenoxylon mirabile was collected from the upper Permian (Changhsingian) Sunjiagou Formation of Shitanjing coalfield, northern China. Samples from different portions of the stem were prepared by using the standard thin-sectioning technique and studied in transmitted light. KEY RESULTS: The outgrowth of ray parenchyma cells protruded into adjacent tracheids through pits initially forming small pyriform or balloon-shaped structures, which became globular or slightly elongated when they reached their maximum size. The tracheid luminae were gradually occluded by densely spaced tyloses. The host tracheids are arranged in distinct concentric zones representing different growth phases of tylosis formation within a single growth ring. CONCLUSIONS: The extensive development of tyloses from the innermost heartwood (metaxylem) tracheids to the outermost sapwood tracheids suggests that the plant was highly vulnerable and reacted strongly to environmental stress. Based on the evidence available, the tyloses were probably not produced in response to wound reaction or pathogenic infection, since evidence of wood traumatic events or fungal invasion are not recognizable. Rather, they may represent an ecophysiological response to the constant environmental stimuli.

Triassic leech cocoon from Antarctica contains fossil bell animal.

Our understanding of the evolution of life on Earth is limited by the imperfection of the fossil record. One reason for this imperfect record is that organisms without hard parts, such as bones, shells, and wood, have a very low potential to enter the fossil record. Occasionally, however, exceptional fossil deposits that preserve soft-bodied organisms provide a rare glimpse of the true biodiversity during past periods of Earth history. We here present an extraordinary find of a fossil ciliate that is encased inside the wall layer of a more than 200 Ma leech cocoon from Antarctica. The microfossil consists of a helically contractile stalk that attaches to a main body with a peristomial feeding apparatus and a large C-shaped macronucleus. It agrees in every aspect with the living bell animals, such as Vorticella. Vorticellids and similar peritrichs are vital constituents of aquatic ecosystems worldwide, but so far have lacked any fossil record. This discovery offers a glimpse of ancient soft-bodied protozoan biotas, and also highlights the potential of clitellate cocoons as microscopic "conservation traps" comparable to amber.

Thalloid organisms and the fossil record: New perspectives from the Transantarctic Mountains.

Thalloid body plans occur in several groups of organisms, including bryophytes, lichens and algae. While many aspects of the biology and ecology of extant thalloid organisms are well understood today, knowledge about the evolutionary history, palaeobiology and palaeoecology of these life forms remains limited. The recently discovered thalloid fossil Litothallus ganovex from the Triassic of Antarctica consists of fused vertical cell filaments forming a pseudoparenchymatous crust-like body, and most likely represents a freshwater macroalga. Other cuticle fragments from Antarctica are tentatively interpreted as remains of thallose liverworts. These unexpected new finds indicate that thalloid organisms are more frequent in the fossil record than previously assumed, and contribute to a better understanding of the palaeobiodiversity of ancient non-marine ecosystems.

Microanatomy of Early Devonian book lungs.

The book lungs of an exceptionally preserved fossil arachnid (Trigonotarbida) from the Early Devonian (approx. 410 Myr ago) Rhynie cherts of Scotland were studied using a non-destructive imaging technique. Our three-dimensional modelling of fine structures, based on assembling successive images made at different focal planes through the translucent chert matrix, revealed for the first time fossil trabeculae: tiny cuticular pillars separating adjacent lung lamellae and creating a permanent air space. Trabeculae thus show unequivocally that trigonotarbids were fully terrestrial and that the microanatomy of the earliest known lungs is indistinguishable from that in modern Arachnida. A recurrent controversy in arachnid evolution is whether the similarity between the book lungs of Pantetrapulmonata (i.e. spiders, trigonotarbids, etc.) and those of scorpions is a result of convergence. Drawing on comparative studies of extant taxa, we have identified explicit characters (trabeculae, spines on the lamellar edge) shared by living and fossil arachnid respiratory organs, which support the hypothesis that book lungs were derived from a single, common, presumably terrestrial, ancestor.

Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses.

The Early Devonian Rhynie chert has been critical in documenting early land plant-fungal interactions. However, complex associations involving several fungi that enter into qualitatively different relationships with a single host plant and even interact with one another have not yet been detailed. Here, we studied petrographic thin sections of the Rhynie chert plant Nothia aphylla. Three fungal endophytes (co)occur in prostrate axes of this plant: narrow hyphae producing clusters of small spores; large spherical spores/zoosporangia; and wide aseptate hyphae that form intercellular vesicles in the cortex. Host responses on attack include bulging of infected rhizoids, formation of encasement layers around intracellular hyphae, and separation of infected from uninfected tissues by secondarily thickened cell walls. A complex simultaneous interaction of N. aphylla with three endophytic fungi was discovered. The host responses indicate that some of the mechanisms causing host responses in extant plants were in place 400 million yr ago. Anatomical and life history features of N. aphylla suggest that this plant may have been particularly susceptible to colonization by fungi.

An alternative mode of early land plant colonization by putative endomycorrhizal fungi.

Rhizomatous axes of Nothia aphylla, a land plant from the 400-myr-old Rhynie chert, host a fungus that closely resembles Glomites rhyniensis (Glomeromycota), the endomycorrhizal fungus of the Rhynie chert plant Aglaophyton major. However, G. rhyniensis is an intercellular endophyte that becomes intracellular exclusively within a well-defined region of the cortex, while the fungus in N. aphylla initially is intracellular but later becomes intercellular in the cortex. We hypothesize that N. aphylla displays an alternative mode of colonization by endomycorrhizal fungi, perhaps related to the peculiar internal anatomy of the lower portion of the rhizomatous axis, in which the radial arrangement of cells, along with the virtual absence of intercellular spaces, provides no intercellular infection pathway into the cortex.

Aromatized arborane/fernane hydrocarbons as biomarkers for cordaites.

Previous palaeobotanical and palynological studies on coals from Euramerican Pennsylvanian ( identical with Late Carboniferous) coal basins indicate a major change in coal-swamp floras, especially at the Westphalian-Stephanian ( approximately Kasimovian-Gzhelian, according to Geological Time Scale 2004) boundary. A flora dominated by arborescent lycophytes was replaced by a vegetation dominated by marattialean tree ferns in various Euramerican coal basins. Earlier combined palynological and organic geochemical studies on Westphalian/Stephanian coals and shales from the Saar-Nahe Basin (Germany) revealed that the distribution of aromatized arborane/fernane hydrocarbons in solvent extracts reflects the increasing importance of seed plants, especially cordaites (extinct group of gymnosperms), conifers and pteridosperms. However, the biological source of the precursor molecules could not be specified. To clarify if the arborane/fernane derivatives MATH, MAPH, DAPH 1, and DAPH 2 in Westphalian/Stephanian coals can be assigned to one of the three potential source plant groups, we analyzed coals, sediments and fossil plant remains from different Euramerican locations with respect to their biomarker composition and stable carbon isotopic composition. Thereby, stable carbon isotopic ratios showed only insignificant variations between Westphalian and Stephanian samples and proved to be an unsuitable tool to describe floral changes during the Westphalian/Stephanian of the Saar-Nahe Basin. In contrast, we were able to show for the first time that MATH, MAPH, DAPH 1 and DAPH 2 are prominent constituents only in extracts of cordaitean macrofossils and can therefore be regarded as biomarkers for this group of gymnosperms.

Hassiella monospora gen. et sp. nov., a microfungus from the 400 million year old Rhynie chert.

A new microfungus, Hassiella monospora gen. et sp. nov., consisting of coenocytic hyphae is associated with degraded plant material in the Early Devonian silicified Rhynie chert ecosystem. Some hyphae produce small bulb-like projections that subsequently develop into spherical, thick-walled and highly ornamented reproductive structures. Mature reproductive structures are characterized by a prominent, funnel-shaped appendage that is interpreted as an amphigynous antheridium. When combined, these features are suggestive of the oogonia/oosporangia in certain extant members of the Peronosporomycetes (Oomycota).

Life history biology of early land plants: deciphering the gametophyte phase.

The ca. 400-million-year-old Rhynie chert biota represents a benchmark for studies of early terrestrial ecosystems. The exquisite preservation of the organisms documents an ancient biodiversity that also includes various levels of biological interaction. Absent from the picture until recently has been detailed information about the development of the gametophyte phase and the alternation of generations of the macroplants in this ecosystem. Here, we trace the development of the gametophyte phase of Aglaophyton, an early land plant with an unusual complement of structural and morphological characters. Mature gametophytes consist of a fleshy protocorm attached to the substrate by basal rhizoids; arising from the upper surface are one to several upright gametangiophores bearing multiple gametangia. Stomata are present on the upper surface of the protocorm and gametangiophore, and endomycorrhizal fungi extend throughout the gametophyte. Gametophytes are unisexual, producing either antheridiophores or archegoniophores. There is no evidence that gametophytes later become hermaphroditic. The sexual dimorphism of the Rhynie chert gametophytes is inconsistent with theoretical ideas about the haploid phase of early land plants. The gametophyte phase of early land plants can now be considered within an ecological and evolutionary framework that, in turn, can be used to develop hypotheses about some aspects of the population dynamics and growth of these early land plants.

Atmospheric CO2 from fossil plant cuticles.

Plants respond to changes in atmospheric carbon dioxide levels by regulating the number of stomata in their leaves. In his reconstruction of a continuous, 300-million-year record of atmospheric CO2, Retallack bases his curve on stomatal counts of fossil plant cuticles taken from published micrographs. However, the preservation of cuticles from Permian times is generally too fragmentary for the stomatal index to be reliably determined, the micrographs used could have biased the results, and there are important errors in the supplementary data - all of which cast doubt on the Permian part of Retallack's record.