Evolution of phenotypic disparity in the plant kingdom.

The plant kingdom exhibits diverse bodyplans, from single-celled algae to complex multicellular land plants, but it is unclear how this phenotypic disparity was achieved. Here we show that the living divisions comprise discrete clusters within morphospace, separated largely by reproductive innovations, the extinction of evolutionary intermediates and lineage-specific evolution. Phenotypic complexity correlates not with disparity but with ploidy history, reflecting the role of genome duplication in plant macroevolution. Overall, the plant kingdom exhibits a pattern of episodically increasing disparity throughout its evolutionary history that mirrors the evolutionary floras and reflects ecological expansion facilitated by reproductive innovations. This pattern also parallels that seen in the animal and fungal kingdoms, suggesting a general pattern for the evolution of multicellular bodyplans.

Low tropical diversity during the adaptive radiation of early land plants.

The latitudinal biodiversity gradient, with tropical regions acting as 'evolutionary cradles', is a cornerstone of current biogeographical and ecological theory1. In the modern world floral biodiversity and biomass are overwhelmingly concentrated in the tropics, and it is often assumed that the tropics were evolutionary cradles throughout land plant evolutionary history. For example, the origination and diversification of angiosperms is believed to have taken place in the Cretaceous tropics2 and modern gymnosperms in the Permian tropics3. Here, we show that during the first major diversification of land plants, in the Late Silurian-Early Devonian, land plant biodiversity was much lower at the equator compared to medium-high southern latitudes. Throughout this crucial interval of plant evolution, tropical vegetation remained depauperate and of very low taxonomic biodiversity, although with similar morphological disparity to the more diverse higher latitude floras. Possible explanations for this low tropical floral biodiversity include palaeocontinental configuration or adverse palaeotropical environmental conditions. We discount the possibility that it was simply a fortuitous feature of the biogeographical spread of the earliest vascular land plants.

A possible billion-year-old holozoan with differentiated multicellularity.

Sediments of the Torridonian sequence of the Northwest Scottish Highlands contain a wide array of microfossils, documenting life in a non-marine setting a billion years ago (1 Ga).1-4 Phosphate nodules from the Diabaig Formation at Loch Torridon preserve microorganisms with cellular-level fidelity,5,6 allowing for partial reconstruction of the developmental stages of a new organism, Bicellum brasieri gen. et sp. nov. The mature form of Bicellum consists of a solid, spherical ball of tightly packed cells (a stereoblast) of isodiametric cells enclosed in a monolayer of elongated, sausage-shaped cells. However, two populations of naked stereoblasts show mixed cell shapes, which we infer to indicate incipient development of elongated cells that were migrating to the periphery of the cell mass. These simple morphogenetic movements could be explained by differential cell-cell adhesion.7,8 In fact, the basic morphology of Bicellum is topologically similar to that of experimentally produced cell masses that were shown to spontaneously segregate into two distinct domains based on differential cadherin-based cell adhesion.9 The lack of rigid cell walls in the stereoblast renders an algal affinity for Bicellum unlikely: its overall morphology is more consistent with a holozoan origin. Unicellular holozoans are known today to form multicellular stages within complex life cycles,10-13 so the occurrence of such simple levels of transient multicellularity seen here is consistent with a holozoan affinity. Regardless of precise phylogenetic placement, these fossils demonstrate simple cell differentiation and morphogenic processes that are similar to those seen in some metazoans today.

A novel reproductive strategy in an Early Devonian plant.

Bonacorsi et al. describe a new fossil from the Early Devonian that provides the earliest clear evidence for more advanced reproductive biology in land plants. The plant produced multiple spore size classes, which is an essential innovation necessary for all advanced plant reproductive strategies, including seeds and flowers.

Mid-Devonian Archaeopteris Roots Signal Revolutionary Change in Earliest Fossil Forests.

The origin of trees and forests in the Mid Devonian (393-383 Ma) was a turning point in Earth history, marking permanent changes to terrestrial ecology, geochemical cycles, atmospheric CO2 levels, and climate. However, how all these factors interrelate remains largely unknown. From a fossil soil (palaeosol) in the Catskill region near Cairo NY, USA, we report evidence of the oldest forest (mid Givetian) yet identified worldwide. Similar to the famous site at Gilboa, NY, we find treefern-like Eospermatopteris (Cladoxylopsida). However, the environment at Cairo appears to have been periodically drier. Along with a single enigmatic root system potentially belonging to a very early rhizomorphic lycopsid, we see spectacularly extensive root systems here assigned to the lignophyte group containing the genus Archaeopteris. This group appears pivotal to the subsequent evolutionary history of forests due to possession of multiple advanced features and likely relationship to subsequently dominant seed plants. Here we show that Archaeopteris had a highly advanced root system essentially comparable to modern seed plants. This suggests a unique ecological role for the group involving greatly expanded energy and resource utilization, with consequent influence on global processes much greater than expected from tree size or rooting depth alone.

Palaeontology: The Rhynie Chert Is the Gift that Keeps on Giving.

The earliest record of a terrestrial testate amoeba is reported. This provides further evidence that early terrestrial ecosystems were more complex and modern in aspect than previously considered, in terms of biota, ecological interactions and biogeochemical cycling.

The Interrelationships of Land Plants and the Nature of the Ancestral Embryophyte.

The evolutionary emergence of land plant body plans transformed the planet. However, our understanding of this formative episode is mired in the uncertainty associated with the phylogenetic relationships among bryophytes (hornworts, liverworts, and mosses) and tracheophytes (vascular plants). Here we attempt to clarify this problem by analyzing a large transcriptomic dataset with models that allow for compositional heterogeneity between sites. Zygnematophyceae is resolved as sister to land plants, but we obtain several distinct relationships between bryophytes and tracheophytes. Concatenated sequence analyses that can explicitly accommodate site-specific compositional heterogeneity give more support for a mosses-liverworts clade, "Setaphyta," as the sister to all other land plants, and weak support for hornworts as the sister to all other land plants. Bryophyte monophyly is supported by gene concatenation analyses using models explicitly accommodating lineage-specific compositional heterogeneity and analyses of gene trees. Both maximum-likelihood analyses that compare the fit of each gene tree to proposed species trees and Bayesian supertree estimation based on gene trees support bryophyte monophyly. Of the 15 distinct rooted relationships for embryophytes, we reject all but three hypotheses, which differ only in the position of hornworts. Our results imply that the ancestral embryophyte was more complex than has been envisaged based on topologies recognizing liverworts as the sister lineage to all other embryophytes. This requires many phenotypic character losses and transformations in the liverwort lineage, diminishes inconsistency between phylogeny and the fossil record, and prompts re-evaluation of the phylogenetic affinity of early land plant fossils, the majority of which are considered stem tracheophytes.

The timescale of early land plant evolution.

Establishing the timescale of early land plant evolution is essential for testing hypotheses on the coevolution of land plants and Earth's System. The sparseness of early land plant megafossils and stratigraphic controls on their distribution make the fossil record an unreliable guide, leaving only the molecular clock. However, the application of molecular clock methodology is challenged by the current impasse in attempts to resolve the evolutionary relationships among the living bryophytes and tracheophytes. Here, we establish a timescale for early land plant evolution that integrates over topological uncertainty by exploring the impact of competing hypotheses on bryophyte-tracheophyte relationships, among other variables, on divergence time estimation. We codify 37 fossil calibrations for Viridiplantae following best practice. We apply these calibrations in a Bayesian relaxed molecular clock analysis of a phylogenomic dataset encompassing the diversity of Embryophyta and their relatives within Viridiplantae. Topology and dataset sizes have little impact on age estimates, with greater differences among alternative clock models and calibration strategies. For all analyses, a Cambrian origin of Embryophyta is recovered with highest probability. The estimated ages for crown tracheophytes range from Late Ordovician to late Silurian. This timescale implies an early establishment of terrestrial ecosystems by land plants that is in close accord with recent estimates for the origin of terrestrial animal lineages. Biogeochemical models that are constrained by the fossil record of early land plants, or attempt to explain their impact, must consider the implications of a much earlier, middle Cambrian-Early Ordovician, origin.

Palaeoecology and palaeophytogeography of the Rhynie chert plants: further evidence from integrated analysis of in situ and dispersed spores.

The remarkably preserved Rhynie chert plants remain pivotal to our understanding of early land plants. The extraordinary anatomical detail they preserve is a consequence of exceptional preservation, by silicification, in the hot-springs environment they inhabited. However, this has prompted questions as to just how typical of early land plants the Rhynie chert plants really are. Some have suggested that they were highly adapted to the unusual hot-springs environment and are unrepresentative of 'normal' plants of the regional flora. New quantitative analysis of dispersed spore assemblages from the stratigraphical sequence of the Rhynie outlier, coupled with characterization of the in situ spores of the Rhynie chert plants, permits investigation of their palaeoecology and palaeophytogeography. It is shown that the Rhynie inland intermontane basin harboured a relatively diverse flora with only a small proportion of these plants actually inhabiting the hot-springs environment. However, the flora of the Rhynie basin differed from coeval lowland floodplain deposits on the same continent, as it was less diverse, lacked some important spore groups and contained some unique elements. At least some of the Rhynie plants (e.g. Horneophyton lignieri) existed outside the hot-springs environment, inhabiting the wider basin, and were indeed palaeogeographically widespread. They probably existed in the hot-springs environment because they were preadapted to this unstable and harsh setting.This article is part of a discussion meeting issue 'The Rhynie cherts: our earliest terrestrial ecosystem revisited'.

Palaeoecology of a billion-year-old non-marine cyanobacterium from the Torridon Group and Nonesuch Formation.

A new chroococcalean cyanobacterium is described from approximately 1-billion-year-old non-marine deposits of the Torridonian Group of Scotland and the Nonesuch Formation of Michigan, USA. Individual cells of the new microfossil, Eohalothece lacustrina gen. et sp. nov., are associated with benthic microbial biofilms, but the majority of samples are recovered in palynological preparations in the form of large, apparently planktonic colonies, similar to extant species of Microcystis. In the Torridonian, Eohalothece is associated with phosphatic nodules, and we have developed a novel hypothesis linking Eohalothece to phosphate deposition in ancient freshwater settings. Extant cyanobacteria can be prolific producers of extracellular microcystins, which are non-ribosomal polypeptide phosphatase inhibitors. Microcystins may have promoted the retention and concentration of sedimentary organic phosphate prior to mineralization of francolite and nodule formation. This has a further implication that the Torridonian lakes were nitrogen limited as the release of microcystins is enhanced under such conditions today. The abundance and wide distribution of Eohalothece lacustrina attests to the importance of cyanobacteria as oxygen-producing photoautotrophs in lacustrine ecosystems at the time of the Mesoproterozoic-Neoproterozoic transition.

Conservation of Male Sterility 2 function during spore and pollen wall development supports an evolutionarily early recruitment of a core component in the sporopollenin biosynthetic pathway.

The early evolution of plants required the acquisition of a number of key adaptations to overcome physiological difficulties associated with survival on land. One of these was a tough sporopollenin wall that enclosed reproductive propagules and provided protection from desiccation and UV-B radiation. All land plants possess such walled spores (or their derived homologue, pollen). We took a reverse genetics approach, consisting of knock-out and complementation experiments to test the functional conservation of the sporopollenin-associated gene MALE STERILTY 2 (which is essential for pollen wall development in Arabidopsis thaliana) in the bryophyte Physcomitrella patens. Knock-outs of a putative moss homologue of the A. thaliana MS2 gene, which is highly expressed in the moss sporophyte, led to spores with highly defective walls comparable to that observed in the A. thaliana ms2 mutant, and extremely compromised germination. Conversely, the moss MS2 gene could not rescue the A. thaliana ms2 phenotype. The results presented here suggest that a core component of the biochemical and developmental pathway required for angiosperm pollen wall development was recruited early in land plant evolution but the continued increase in pollen wall complexity observed in angiosperms has been accompanied by divergence in MS2 gene function.

Lacustrine Nostoc (Nostocales) and associated microbiome generate a new type of modern clotted microbialite.

Microbialites are mineral formations formed by microbial communities that are often dominated by cyanobacteria. Carbonate microbialites, known from Proterozoic times through the present, are recognized for sequestering globally significant amounts of inorganic carbon. Recent ecological work has focused on microbial communities dominated by cyanobacteria that produce microbial mats and laminate microbialites (stromatolites). However, the taxonomic composition and functions of microbial communities that generate distinctive clotted microbialites (thrombolites) are less well understood. Here, microscopy and deep shotgun sequencing were used to characterize the microbiome (microbial taxa and their genomes) associated with a single cyanobacterial host linked by 16S sequences to Nostoc commune Vaucher ex Bornet & Flahault, which dominates abundant littoral clotted microbialites in shallow, subpolar, freshwater Laguna Larga in southern Chile. Microscopy and energy-dispersive X-ray spectroscopy suggested the hypothesis that adherent hollow carbonate spheres typical of the clotted microbialite begin development on the rigid curved outer surfaces of the Nostoc balls. A surface biofilm included >50 nonoxygenic bacterial genera (taxa other than Nostoc) that indicate diverse ecological functions. The Laguna Larga Nostoc microbiome included the sulfate reducers Desulfomicrobium and Sulfospirillum and genes encoding all known proteins specific to sulfate reduction, a process known to facilitate carbonate deposition by increasing pH. Sequences indicating presence of nostocalean and other types of nifH, nostocalean sulfide:ferredoxin oxidoreductase (indicating anoxygenic photosynthesis), and biosynthetic pathways for the secondary products scytonemin, mycosporine, and microviridin toxin were identified. These results allow comparisons with microbiota and microbiomes of other algae and illuminate biogeochemical roles of ancient microbialites.

A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic.

The geochemical carbon cycle is strongly influenced by life on land, principally through the effects of carbon sequestration and the weathering of calcium and magnesium silicates in surface rocks and soils. Knowing the time of origin of land plants and animals and also of key organ systems (e.g. plant vasculature, roots, wood) is crucial to understand the development of the carbon cycle and its effects on other Earth systems. Here, we compare evidence from fossils with calibrated molecular phylogenetic trees (timetrees) of living plants and arthropods. We show that different perspectives conflict in terms of the relative timing of events, the organisms involved and the pattern of diversification of various groups. Focusing on the fossil record, we highlight a number of key biases that underpin some of these conflicts, the most pervasive and far-reaching being the extent and nature of major facies changes in the rock record. These effects probably mask an earlier origin of life on land than is evident from certain classes of fossil data. If correct, this would have major implications in understanding the carbon cycle during the Early Palaeozoic.

Earth's earliest non-marine eukaryotes.

The existence of a terrestrial Precambrian (more than 542 Myr ago) biota has been largely inferred from indirect chemical and geological evidence associated with palaeosols, the weathering of clay minerals and microbially induced sedimentary structures in siliciclastic sediments. Direct evidence of fossils within rocks of non-marine origin in the Precambrian is exceedingly rare. The most widely cited example comprises a single report of morphologically simple mineralized tubes and spheres interpreted as cyanobacteria, obtained from 1,200-Myr-old palaeokarst in Arizona. Organic-walled microfossils were first described from the non-marine Torridonian (1.2-1.0 Gyr ago) sequence of northwest Scotland in 1907. Subsequent studies found few distinctive taxa-a century later, the Torridonian microflora is still being characterized as primarily nondescript "leiospheres". We have comprehensively sampled grey shales and phosphatic nodules throughout the Torridonian sequence. Here we report the recovery of large populations of diverse organic-walled microfossils extracted by acid maceration, complemented by studies using thin sections of phosphatic nodules that yield exceptionally detailed three-dimensional preservation. These assemblages contain multicellular structures, complex-walled cysts, asymmetric organic structures, and dorsiventral, compressed organic thalli, some approaching one millimetre in diameter. They offer direct evidence of eukaryotes living in freshwater aquatic and subaerially exposed habitats during the Proterozoic era. The apparent dominance of eukaryotes in non-marine settings by 1 Gyr ago indicates that eukaryotic evolution on land may have commenced far earlier than previously thought.

Evolutionary development of the plant and spore wall.

BACKGROUND AND AIMS: Many key innovations were required to enable plants to colonize terrestrial habitats successfully. One of these was the acquisition of a durable spore/pollen wall capable of withstanding the harsh desiccating and UV-B-rich environment encountered on land. The spores of 'lower' spore-bearing plants and the pollen of 'higher' seed plants are homologous. In recent years, researchers have begun to investigate the molecular genetics of pollen wall development in angiosperms (including the model organism Arabidopsis thaliana). However, research into the molecular genetics of spore wall development in more basal plants has thus far been extremely limited. This review summarizes the literature on spore/pollen wall development, including the molecular genetics associated with pollen wall development in angiosperms, in a preliminary attempt to identify possible candidate genes involved in spore wall development in more basal plants. PRESENCE IN MOSS OF GENES INVOLVED IN POLLEN WALL DEVELOPMENT: Bioinformatic studies have suggested that genes implicated in pollen wall development in angiosperms are also present in moss and lycopsids, and may therefore be involved in spore wall development in basal plants. This suggests that the molecular genetics of spore/pollen development are highly conserved, despite the large morphological and functional differences between spores and pollen. FUTURE WORK: The use of high-throughput sequencing strategies and/or microarray experiments at an appropriate stage of 'lower' land plant sporogenesis will allow the identification of candidate genes likely to be involved in the development of the spore wall by way of comparison with those genes known to be involved in pollen wall development. Additionally, by conducting gene knock-out and gene swap experiments between 'lower' land plant species, such as the moss model species Physcomitrella patens, and the angiosperm model species arabidopsis it will be possible to test the role of these candidate genes.

Origin and radiation of the earliest vascular land plants.

Colonization of the land by plants most likely occurred in a stepwise fashion starting in the Mid-Ordovician. The earliest flora of bryophyte-like plants appears to have been cosmopolitan and dominated the planet, relatively unchanged, for some 30 million years. It is represented by fossilized dispersed cryptospores and fragmentary plant remains. In the Early Silurian, cryptospore abundance and diversity diminished abruptly as trilete spores appeared, became abundant, and underwent rapid diversification. This change coincides approximately with the appearance of vascular plant megafossils and probably represents the origin and adaptive radiation of vascular plants. We have obtained a diverse trilete spore occurrence from the Late Ordovician that suggests that vascular plants originated and diversified earlier than previously hypothesized, in Gondwana, before migrating elsewhere and secondarily diversifying.

Spore wall ultrastructure in the early lycopsid Leclercqia (Protolepidodendrales) from the Lower Devonian of North America: Evidence for a fundamental division in the lycopsids.

Documenting the morphology and ultrastructure of spores from known Silurian-Devonian plants clarifies organization and probable affinities of dispersed spores and contributes to analyses of evolutionary changes and phylogenetic relationships in early plants. In this study of fossil in situ spores from the early protolepidodendralean lycopsid Leclercqia, we identified new characters including an additional synapomorphy of the ligulate lycopsid clade. A detailed light (LM), scanning electron (SEM), and transmission electron microscope (TEM) analysis of spores from two species of Leclercqia from the Lower Devonian (Emsian) of New Brunswick, eastern Canada, L. andrewsii and L. complexa, shows both are homosporous, yielding spores belonging to the dispersed spore form taxon Acinosporites lindlarensis. Important features of wall ultrastructure include the presence of a paraexospore, peculiar exospore-derived, peg-like structures located in the gap between the outer exospore/inner paraexospore, and multilamellate regions in the interradial areas of the proximal surface. Similar interradial multilamellate regions occur in other ligulate lycopsids (fossil and extant). This character is probably a further synapomorphy for the ligulate lycopsid clade, within which heterosporous lycopods form a monophyletic group. These data suggest the ligule and interradial multilamellate region appeared prior to heterospory.