Unity in diversity Field, Katie J.; Pressel, Silvia
The New phytologist,
12/2018, Letnik:
220, Številka:
4
Journal Article
Recenzirano
Odprti dostop
Mycorrhizal symbiosis is an ancient and widespread mutualism between plants and fungi that facilitated plant terrestrialisation > 500 million years ago, with key roles in ecosystem functioning at ...multiple scales. Central to the symbiosis is the bidirectional exchange of plant-fixed carbon for fungal-acquired nutrients. Within this unifying role of mycorrhizas, considerable diversity in structure and function reflects the diversity of the partners involved. Early diverging plants form mutualisms not only with arbuscular mycorrhizal Glomeromycotina fungi, but also with poorly characterised Mucoromycotina, which may also colonise the roots of ‘higher’ plants as fine root endophytes. Functional diversity in these symbioses depends on both fungal and plant life histories and is influenced by the environment. Recent studies have highlighted the roles of lipids/fatty acids in plant-to-fungus carbon transport and potential contributions of Glomeromycotina fungi to plant nitrogen nutrition. Together with emerging appreciation of mycorrhizal networks as multi-species resource-sharing systems, these insights are broadening our views on mycorrhizas and their roles in nutrient cycling. It is crucial that the diverse array of biotic and abiotic factors that together shape the dynamics of carbon-for-nutrient exchange between plants and fungi are integrated, in addition to embracing the unfolding and potentially key role of Mucoromycotina fungi in these processes.
The timescale of early land plant evolution Morris, Jennifer L.; Puttick, Mark N.; Clark, James W. ...
Proceedings of the National Academy of Sciences - PNAS,
03/2018, Letnik:
115, Številka:
10
Journal Article
Recenzirano
Odprti dostop
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.
Cryo-scanning electron microscopy shows that nascent intercellular spaces (ICSs) in bryophytes are liquid-filled, whereas these are gas-filled from the outset in tracheophytes except in the ...gametophytes of Lycopodiales. ICSs are absent in moss gametophytes and remain liquid-filled in hornwort gametophytes and in both generations in liverworts. Liquid is replaced by gas following stomatal opening in hornworts and is ubiquitous in moss sporophytes even in astomate taxa. New data on moss water relations and sporophyte weights indicate that the latter are homiohydric while X-ray microanalysis reveals an absence of potassium pumps in the stomatal apparatus. The distribution of ICSs in bryophytes is strongly indicative of very ancient multiple origins. Inherent in this scenario is either the dual or triple evolution of stomata. The absence, in mosses, of any relationship between increases in sporophyte biomass and stomata numbers and absences, suggests that CO2 entry through the stomata, possible only after fluid replacement by gas in the ICSs, makes but a minor contribution to sporophyte nutrition. Save for a single claim of active regulation of aperture dimensions in mosses, all other functional and structural data point to the sporophyte desiccation, leading to spore discharge, as the primeval role of the stomatal apparatus.
This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.
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.
Display omitted
•Early land plant relationships are extremely uncertain•We resolve the “Setaphyta” clade of liverworts plus mosses•The simple body plan of liverworts results from loss of ancestral characters•The ancestral land plant was more complex
Puttick et al. resolve a “Setaphyta” clade uniting liverworts and mosses and support for bryophyte monophyly. Their results indicate that the ancestral land plant was more complex than has been envisaged based on phylogenies recognizing liverworts as the sister lineage to all other embryophytes.
Introduction Though used as the model liverwort in culture for several decades, the biology of Marchantia polymorpha subsp. ruderalis in nature has never been documented in detail in a single ...account. Methods Here we synthesize routine field observations documented with hundreds of images of M. ruderalis colonies (or groups) showing sex differentiation over 3 years on two populations of M. ruderalis after major heathland fires in 2020. Results Initial post-fire establishment is from airborne spores rather than a spore bank but thereafter spread is via gemmae which have less exacting germination requirements. Young sporelings are highly gemmiferous but gemmae production becomes less frequent after sex organ formation. Over the course of a year there are up to three waves of carpocephalum production with the overwhelming majority of antheridiophores appearing 2-3 months ahead of the archegoniophores though no differences in growth rates were apparent between male and female thalli. Spermatozoids are produced almost continuously throughout the year, whilst sporophyte maturation is restricted to the summer months. Discussion Because of the asynchrony between antheridiophore and archegoniophore production a 1:1 sex ratio is only apparent over this period. The spring months see an excess of males with more females in the summer. An almost 100% fertilization rate, with fertilization distances of up to 19 m far exceeding those in all other bryophytes, is attributed to vast spermatozoid production for most of the year, dispersal on surface oil films between thalli and highly effective intra-thallus spermatozoid transport via the pegged-rhizoid water-conducting system. Archegoniophores do develop on female-only populations but have shorter stalks than those where fertilization has occurred. Eventual disappearance post fires is attributed to a fall in topsoil nutrient levels preventing new sporeling establishment and competition from Ceratodon purpureus and Polytrichum spp. A major drought in the summer of 2022 almost wiped out the heathland Marchantia populations but all the other bryophytes survived.
Fungi (Eumycota) form close associations with plants, with which they have co‐existed since the dawn of life on land, but their diversity in early terrestrial ecosystems is still poorly understood. ...We studied petrographic sections of exceptionally well‐preserved petrified plants from the 407 million yr‐old Rhynie Chert (Scotland, UK). For comparative purposes, we illustrate fungal associations in four extant lower land plants. We document two new endophytes in the plant Horneophyton lignieri: Palaeoglomus boullardii (sp. nov. Glomeromycota) colonizes parenchyma in a discontinuous zone of the outer cortex of the aerial axes, forming arbuscule‐like structures, vesicles and spores; Palaeoendogone gwynne‐vaughaniae (gen. nov., sp. nov. Mucoromycotina) colonizes parenchyma in the basal part of the plant, where it is present in intercellular spaces and as intracellular coils but absent from rhizoids. Critical comparisons between the newly discovered Horneophyton endophytes, fungi previously described from the Rhynie Chert and fungal colonization in extant lower land plants reveal several features characteristic of both Mucoromycotina and Glomeromycota. A reappraisal of fungal associations in early land plants indicates that they are more diverse than assumed hitherto, overturning the long‐held paradigm that the early endophytes were exclusively Glomeromycota.
The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that ...Glomeromycota formed the sole ancestral plant–fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO₂concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon‐for‐nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid‐Palaeozoic (1500 ppm) and near‐contemporary (440 ppm) CO₂concentrations using isotope tracers, and analysed cytological differences in plant–fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort–Mucoromycotina symbiosis is mutualistic and mycorrhiza‐like, but differs from liverwort–Glomeromycota symbiosis in maintaining functional efficiency of carbon‐for‐nutrient exchange between partners across CO₂concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild‐collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO₂, we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.
• Liverworts, which are amongst the earliest divergent plant lineages and important ecosystem pioneers, often form nutritional mutualisms with arbuscular mycorrhiza-forming Glomeromycotina and ...fine-root endophytic Mucoromycotina fungi, both of which coevolved with early land plants. Some liverworts, in common with many later divergent plants, harbour both fungal groups, suggesting these fungi may complementarily improve plant access to different soil nutrients.
• We tested this hypothesis by growing liverworts in single and dual fungal partnerships under a modern atmosphere and under 1500 ppm CO₂, as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with 15N-labelled algal necromass and 33P orthophosphate. Photosynthate allocation to fungi was traced using 14CO₂.
• Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15N, irrespective of atmospheric CO₂ concentration. Both symbionts increased 33P uptake, but Glomeromycotina were often more effective. Dual partnerships showed complementarity of nutrient pool use and greatest photosynthate allocation to symbiotic fungi.
• We show there are important functional differences between the plant–fungal symbioses tested, providing new insights into the functional biology of Glomeromycotina and Mucoromycotina fungal groups that form symbioses with plants. This may explain the persistence of the two fungal lineages in symbioses across the evolution of land plants.
PDF
