Early Colonization Of Land Research Articles

Chemical and elementary characterization of Spongiophyton nanum: Understanding the phylogeny, paleoenvironment, and fossilization processes of an enigmatic flora

The record of thalloid macrofossils in the North-Northwest region of the Paraná Basin is less studied compared to that of invertebrate paleofauna in the same area. Consequently, the lack of important information regarding the niches occupied by thalloid embryophytes during early land colonization in this coastal paleoenvironment is evident. This study presents the first chemical and elemental data on Spongiophyton for this region of the basin, offering insights into its paleoenvironment and fossilization processes and providing considerations about the phylogeny of this enigmatic assemblage Spongiophyton nanum Kräusel emend. Chaloner et al. (1974) collected fragments from an outcropping rock in Jaciara, Mato Grosso, Brazil, and studied them using scanning electron microscope/energy X-ray dispersive spectrometer (EDS) and Fourier transform infrared (FTIR) spectroscopy techniques. The EDS analysis showed the highest elemental concentration of carbon, oxygen, and calcium as the main elements of the cuticle composition. Silicon and aluminum were better represented inside the pores than in other areas of the cuticle. The high carbon concentration in the cuticle suggested an anoxic condition prevalent during the deposition of the fine-grained sediments, which prevented its oxidation before and during diagenesis. The carbon present in the EDS spectra was restricted to the cuticle area, and the FTIR spectra indicated the presence of some functional groups, both related to the original organic matter, possibly cutin. Based on elemental characterization, the fossilization of S. nanum may involve more than one process, such as carbonification and mineralization, and S. nanum has more affinities with lichen groups.

Phenoloxidases: catechol oxidase - the temporary employer and laccase - the rising star of vascular plants.

Phenolics are vital for the adaptation of plants to terrestrial habitats and for species diversity. Phenoloxidases (catechol oxidases, COs, and laccases, LACs) are responsible for the oxidation and polymerization of phenolics. However, their origin, evolution, and differential roles during plant development and land colonization are unclear. We performed the phylogeny, domain, amino acids, compositional biases, and intron analyses to clarify the origin and evolution of COs and LACs, and analysed the structure, selective pressure, and chloroplast targeting to understand the species-dependent distribution of COs. We found that Streptophyta COs were not homologous to the Chlorophyta tyrosinases (TYRs), and might have been acquired by horizontal gene transfer from bacteria. COs expanded in bryophytes. Structural-functionality and selective pressure were partially responsible for the species-dependent retention of COs in embryophytes. LACs emerged in Zygnemaphyceae, having evolved from ascorbate oxidases (AAOs), and prevailed in the vascular plants and strongly expanded in seed plants. COs and LACs coevolved with the phenolic metabolism pathway genes. These results suggested that TYRs and AAOs were the first-stage phenoloxidases in Chlorophyta. COs might be the second key for the early land colonization. LACs were the third one (dominating in the vascular plants) and might be advantageous for diversified phenol substrates and the erect growth of plants. This work provided new insights into how phenoloxidases evolved and were devoted to plant evolution.

When Phased without Water: Biophysics of Cellular Desiccation, from Biomolecules to Condensates.

The molecular machinery that enables life has evolved in water, yet many of the organisms around us are able to survive even extreme desiccation. Especially remarkable are single-cell and sedentary organisms that rely on specialized biomolecular machinery to survive in environments that are routinely subjected to a near-complete lack of water. In this review, we zoom in on the molecular level of what is happening in the cellular environment under water stress. We cover the various mechanisms by which biochemical components of the cell can dysfunction in dehydrated cells and detail the different strategies that organisms have evolved to eliminate or cope with these desiccation-induced perturbations. We specifically focus on two survival strategies: (1) the use of disordered proteins to protect the cellular environment before, during, and in the recovery from desiccation, and (2) the use of biomolecular condensates as a self-assembly mechanism that can sequester or protect specific cellular machinery in times of water stress. We provide a summary of experimental work describing the critical contributions of disordered proteins and biomolecular condensates to the cellular response to water loss and highlight their role in desiccation tolerance. Desiccation biology is an exciting area of cell biology, still far from being completely explored. Understanding it on the molecular level is bound to give us critical new insights in how life adapted/can adapt to the loss of water, spanning from the early colonization of land to how we can deal with climate change in our future.

Sequence stratigraphy and carbon isotopes from the Trenton and Black River Groups near Union Furnace, PA: Constraining the role of land plants in the Ordovician world

Sea-level change influences carbon isotopic trends in both modern and ancient carbonate depositional environments. Generally, this relationship is manifested as a positive carbon isotopic excursion where the rising limb of the excursion is associated with transgression. These excursions exist because sea level can influence 1) local/regional/global carbon cycling, 2) basin restriction and meteoric influence, and 3) carbonate sedimentation. The first two processes are influenced, in part, by the large carbon reservoir represented by the terrestrial biosphere. Our goal is to explore the relationship between carbon isotopes and sea level prior to the evolution of vascular plants at a time when the terrestrial carbon reservoir was far smaller.This study focuses on the Upper Ordovician Union Furnace section in Pennsylvania, where a previously documented ~1‰ increase in δ13C values in the upper Sandbian (458.4–453.0 Ma; referred to as the “baseline shift”) has been interpreted to reflect a perturbation to the global carbon cycle due to the proliferation of non-vascular plants. By focusing on the interval deposited before the “baseline shift”, we were able to examine the relationship between sea level, carbon isotopes, and some of the earliest terrestrial ecosystems. We present a high-resolution δ13C record directly tied to the sedimentological and sequence stratigraphic framework. By sampling genetically related packages of rock we were able to document a relationship between carbon isotopes and sea level at the sequence and parasequence level. Our results show that carbon isotopic values decreased during transgressions and increased during regressions. This seemingly inverse relationship between δ13C values and sea level is interpreted to reflect increased terrestrial fluxes during regression in a world devoid of vascular plants. Our results suggest that the early colonization of land by non-vascular plants impacted regional carbon cycling in the Appalachian Basin and eventually the global carbon cycle in the Late Ordovician.

Mycorrhizal symbioses and the evolution of trophic modes in plants

Abstract Since the early colonization of land, plants depend, to various extents, on mycorrhizal fungi to meet their nutrient demands. In most mycorrhizal symbioses, plants provide sugars derived from photosynthesis to the fungi, whereas the fungi provide essential minerals to the plant. However, in some plants, the flow of carbon has reversed and the fungi provide carbon to the plants. These plants are called mycoheterotrophs. However, it remains unclear how and under which circumstances trophic modes change and whether transitions in trophic modes are associated with changes in mycorrhizal communities. Here, we review the available literature on mycorrhizal associations and trophic modes in plants. We first outline how trophic modes can be determined and how they differ across plants. We then investigate the evolutionary context under which mycoheterotrophy originated. We also examine the mycorrhizal communities associating with autotrophic, partially mycoheterotrophic and fully mycoheterotrophic plants within different plant families and investigate whether commonalities can be observed. Our overview shows that mycoheterotrophy has originated more than 40 times through evolutionary time and can be found in a wide range of plant groups, including liverworts, lycophytes, ferns, monocots and dicots. Partial mycoheterotrophy appears to be much more common than previously anticipated and represents an almost continuous gradient between autotrophy and full mycoheterotrophy. Comparison of the mycorrhizal communities associating with autotrophic, partial and full mycoheterotrophic plants indicates that, although they share some commonalities, shifts from autotrophy to full mycoheterotrophy are accompanied by either losses or shifts in mycorrhizal partners, suggesting that full or partial loss of photosynthesis selects for different mycorrhizal communities. Synthesis. Partial mycoheterotrophy appears to be much more common than previously thought and represents an almost continuous gradient from autotrophy to full mycoheterotrophy. Evolution to full mycoheterotrophy is challenging as it requires specific adaptations and often a switch to other mycorrhizal partners. More detailed analyses of the functionality of different mycorrhizal systems co‐occurring in the roots of a single plant and the costs of mycorrhizal switching are needed to understand the precise mechanisms leading to full mycoheterotrophy.

Genome-wide organellar analyses from the hornwort Leiosporoceros dussii show low frequency of RNA editing.

Because hornworts occupy a pivotal position in early land colonization as sister to other bryophytes, sister to tracheophytes, or sister to all other land plants, a renewed interest has arisen in their phylogenetic diversity, morphology, and genomes. To date, only five organellar genome sequences are available for hornworts. We sequenced the plastome (155,956 bp) and mitogenome (212,153 bp) of the hornwort Leiosporoceros dussii, the sister taxon to all hornworts. The Leiosporoceros organellar genomes show conserved gene structure and order with respect to the other hornworts and other bryophytes. Additionally, using RNA-seq data we quantified the frequency of RNA-editing events (the canonical C-to-U and the reverse editing U-to-C) in both organellar genomes. In total, 109 sites were found in the plastome and 108 in the mitogenome, respectively. The proportion of edited sites corresponds to 0.06% of the plastome and 0.05% of the mitogenome (in reference to the total genome size), in contrast to 0.58% of edited sites in the plastome of Anthoceros angustus (161,162 bp). All edited sites in the plastome and 88 of 108 sites in the mitogenome are C-to-U conversions. Twenty reverse edited sites (U-to-C conversions) were found in the mitogenome (17.8%) and none in the plastome. The low frequency of RNA editing in Leiosporoceros, which is nearly 88% less than in the plastome of Anthoceros and the mitogenome of Nothoceros, indicates that the frequency of RNA editing has fluctuated during hornwort diversification. Hornworts are a pivotal land plant group to unravel the genomic implications of RNA editing and its maintenance despite the evident evolutionary disadvantages.

An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion

Thermobia domestica belongs to an ancient group of insects and has a remarkable ability to digest crystalline cellulose without microbial assistance. By investigating the digestive proteome of Thermobia, we have identified over 20 members of an uncharacterized family of lytic polysaccharide monooxygenases (LPMOs). We show that this LPMO family spans across several clades of the Tree of Life, is of ancient origin, and was recruited by early arthropods with possible roles in remodeling endogenous chitin scaffolds during development and metamorphosis. Based on our in-depth characterization of Thermobia’s LPMOs, we propose that diversification of these enzymes toward cellulose digestion might have endowed ancestral insects with an effective biochemical apparatus for biomass degradation, allowing the early colonization of land during the Paleozoic Era. The vital role of LPMOs in modern agricultural pests and disease vectors offers new opportunities to help tackle global challenges in food security and the control of infectious diseases.

Ultrastructural study on the interaction between Physcomitrella patens and Botrytis cinerea

Little is known about the interactions of bryophytes with their pathogens compared with those of flowering plants. This study used the moss Physcomitrella patens and fungal pathogen Botrytis cinerea to investigate their interaction at the ultrastructural level. Infection behaviour of B. cinerea in moss tissues was observed for 1–7 days after inoculation. Some appressoria directly penetrated P. patens cytoplasm through leaf cell walls, and others entered the intercellular spaces of leaves and infected cytoplasm. Infection hyphae were observed in sclerenchyma cells of P. patens stems for the first time. The results demonstrated that the ratio of hyphae‐inoculated leaf cells to leaf numbers could be used to quantify the disease development process at 24 h after inoculation. The ultrastructural studies revealed two responses of P. patens to B. cinerea inoculation: reinforcement of cell walls, including papillae formation; and cell death. This was the first observation of papillae for P. patens–B. cinerea interaction at the ultrastructural level. Papillae in P. patens had a similar ultrastructure to those of higher plants, and may be involved in the defence response to B. cinerea infection. Thus papillae formation is probably an evolutionarily conserved defence mechanism from the early land colonization by plants. Cell death during the P. patens–B. cinerea interaction had some features of programmed cell death, with hydrogen peroxide produced in cytoplasm membranes, suggesting something like a hypersensitive response. These ultrastructural studies suggest that P. patens could be a useful system for studying phytopathogens and could provide theoretical bases for defence mechanisms in evolutionary development.

Plant microbiomes and sustainable agriculture: Deciphering the plant microbiome and its role in nutrient supply and plant immunity has great potential to reduce the use of fertilizers and biocides in agriculture.

Bacteria had been around long before multi‐cellular eukaryotes evolved and quickly began to colonize these new life forms as another suitable habitat and potential source of nutrients. Nearly all higher organisms across taxa now have bacterial communities living on and within them—from mutually beneficial symbioses to antagonistic parasitic conflicts. They have co‐evolved with their microbiota and come to depend on it for a range of functions in immunity, metabolism and nutrient absorption. In humans, the microbiota, especially bacteria in the gut, play important roles in all areas, by breaking down indigestible polysaccharides, providing vitamins, mediating nutrient absorption in the gut and helping train the immune system. While research on the human microbiome has stolen the limelight, plant scientists have also been making progress towards elucidating the composition and function of plant microbiomes. Their work has great potential for the future of humanity, as it could help to establish more sustainable agriculture with less dependence on fertilizers, pesticides and herbicides, while increasing yield and nutrient content. Research on the plant microbiome actually predates the animal and human counterparts because microorganisms play an obvious and crucial role in fixing nutrients for the plant, especially nitrogen and phosphorus. Given their vital importance for protein and DNA synthesis and energy production, many plants have evolved close symbiotic relationships with soil bacteria and fungi that supply them with both elements in convenient forms with minimum energy expenditure. Indeed, the close relationships with two specific families of microorganisms set apart the plant microbiome from its animal counterpart: rhizobia nitrogen‐fixing bacteria and mycorrhizal fungi, which greatly enhance the ability of roots to extract various nutrients from the soil. Neither group can survive without the host plant that in return supplies oxygen and products of photosynthesis, mainly proteins and carbohydrates. ### A three‐way relationship The relationship with mycorrhizal fungi seems to be …

Enhancement of Non-Photochemical Quenching in the Bryophyte Physcomitrella patens During Acclimation to Salt and Osmotic Stress

Drought and salt stress are major abiotic constraints affecting plant growth worldwide. Under these conditions, the production of reactive oxygen species (ROS) is a common phenomenon taking place mainly in chloroplasts, peroxisomes, mitochondria and apoplasts, especially when associated with high light stress. ROS are harmful because of their high reactivity to cell components, thereby leading to cytotoxicity and cell death. During the Ordovician and early Devonian period, photosynthetic organisms colonized terrestrial habitats, and the acquisition of desiccation tolerance has been a major component of their evolution. We have studied the capacity for acclimation to drought and salt stress of the moss Physcomitrella patens, a representative of the early land colonization stage. Exposure to high concentrations of NaCl and sorbitol strongly affects chloroplast development, the Chl content and the thylakoid protein composition in this moss. Under sublethal conditions (0.2 M NaCl and 0.4 M sorbitol), the photosynthetic apparatus of P. patens responds to oxidative stress by increasing non-photochemical quenching (NPQ). Surprisingly, the accumulation of PSBS and LHCSR, the two polypeptides essential for NPQ in P. patens, was not up-regulated in these conditions. Rather, an increased NPQ amplitude correlated with the overaccumulation of zeaxanthin and the presence of the enzyme violaxanthin de-epoxidase. These results suggest that the regulation of excess energy dissipation through control of PSBS and LHCSR is mainly driven by light conditions, while osmotic and salt stress act through acclimative regulation of the xanthophyll cycle. We conclude that regulation of the xanthophyll cycle is an important anticipatory strategy against photoinhibition by high light.

Early land colonization conference (November 17–19, 2010)

Early land colonization conference (November 17–19, 2010)

Structure and evolution of the plant cation diffusion facilitator family of ion transporters

BackgroundMembers of the cation diffusion facilitator (CDF) family are integral membrane divalent cation transporters that transport metal ions out of the cytoplasm either into the extracellular space or into internal compartments such as the vacuole. The spectrum of cations known to be transported by proteins of the CDF family include Zn, Fe, Co, Cd, and Mn. Members of this family have been identified in prokaryotes, eukaryotes, and archaea, and in sequenced plant genomes. CDF families range in size from nine members in Selaginella moellendorffii to 19 members in Populus trichocarpa. Phylogenetic analysis suggests that the CDF family has expanded within plants, but a definitive plant CDF family phylogeny has not been constructed.ResultsRepresentative CDF members were annotated from diverse genomes across the Viridiplantae and Rhodophyta lineages and used to identify phylogenetic relationships within the CDF family. Bayesian phylogenetic analysis of CDF amino acid sequence data supports organizing land plant CDF family sequences into 7 groups. The origin of the 7 groups predates the emergence of land plants. Among these, 5 of the 7 groups are likely to have originated at the base of the tree of life, and 2 of 7 groups appear to be derived from a duplication event prior to or coincident with land plant evolution. Within land plants, local expansion continues within select groups, while several groups are strictly maintained as one gene copy per genome.ConclusionsDefining the CDF gene family phylogeny contributes to our understanding of this family in several ways. First, when embarking upon functional studies of the members, defining primary groups improves the predictive power of functional assignment of orthologous/paralogous genes and aids in hypothesis generation. Second, defining groups will allow a group-specific sequence motif to be generated that will help define future CDF family sequences and aid in functional motif identification, which currently is lacking for this family in plants. Third, the plant-specific expansion resulting in Groups 8 and 9 evolved coincident to the early primary radiation of plants onto land, suggesting these families may have been important for early land colonization.

Arthropod colonization of land – Linking molecules and fossils in oribatid mites (Acari, Oribatida)

Terrestrial fossils that document the early colonization of land are scarce for >100 my after the Cambrian explosion. This raises the question whether life on land did not exist or just did not fossilize. With a molecular dating technique, we analyzed the origin of terrestrial chelicerate microarthropods (Acari, Oribatida) which have a fossil record since the Middle Devonian that is exceptional among soil animals. Our results suggest that oribatid mites originated in the Precambrian (571±37mya) and that the radiation of basal groups coincides with the gap in the terrestrial fossil record between the Cambrian explosion and the earliest fossilized records of continental ecosystems. Further, they suggest that the colonization of land started via the interstitial, ∼150 my earlier than the oldest fossils of terrestrial ecosystems. Overall, the results imply that omnivorous and detritivorous arthropods formed a major component in early terrestrial food webs, thereby facilitating the invasion of terrestrial habitats by later colonizers of higher trophic levels.

Microbiology of the Atmosphere-Rock Interface: How Biological Interactions and Physical Stresses Modulate a Sophisticated Microbial Ecosystem

Life at the atmosphere-lithosphere boundary is an ancient terrestrial niche that is sparsely covered by thin subaerial biofilms. The microbial inhabitants of these biofilms (a) have adapted to all types of terrestrial/subaerial stresses (e.g., desiccation, extreme temperatures, low nutrient availability, intense solar radiation), (b) interact with minerals that serve as both a dwelling and a source of mineral nutrients, and (c) provoke weathering of rocks and soil formation. Subaerial communities comprise heterotrophic and phototrophic microorganisms that support each other's lifestyle. Major lineages of eubacteria associated with the early colonization of land (e.g., Actinobacteria, Cyanobacteria) are present in these habitats along with eukaryotes such as microscopic green algae and ascomycetous fungi. The subaerial biofilm inhabitants have adapted to desiccation, solar radiation, and other environmental challenges by developing protective, melanized cell walls, assuming microcolonial architectures and symbiotic lifestyles. How these changes occurred, their significance in soil formation, and their potential as markers of climate change are discussed below.

Bryophyte phylogeny: Advancing the molecular and morphological frontiers

Abstract Revolutionary new concepts of bryophyte relationships have emerged from molecular phylogenetic analyses conducted since the onset of the 21st century. For example, sequence data contradict the historical notion that isophylly in leafy liverworts is plesiomorphic and that simple thalloid liverworts are monophyletic. Also contrary to traditional views are the concepts that Leiosporoceros is genetically distinct from other hornworts and that Oedipodium is sister to the peristomate mosses. Substantial increases in ultrastructural and anatomical data likewise have provided new insights on interrelationships. Because of this recent deluge in evolutionary studies on bryophytes, it is an opportune time to co-examine contemporary morphological knowledge and novel molecular hypotheses. An understanding of bryophyte evolution and biology is essential to identify structural innovations that accompanied early land colonization and to illuminate the evolution of more complicated body plans in tracheophytes. In...

A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land

BackgroundThe timescale of prokaryote evolution has been difficult to reconstruct because of a limited fossil record and complexities associated with molecular clocks and deep divergences. However, the relatively large number of genome sequences currently available has provided a better opportunity to control for potential biases such as horizontal gene transfer and rate differences among lineages. We assembled a data set of sequences from 32 proteins (~7600 amino acids) common to 72 species and estimated phylogenetic relationships and divergence times with a local clock method.ResultsOur phylogenetic results support most of the currently recognized higher-level groupings of prokaryotes. Of particular interest is a well-supported group of three major lineages of eubacteria (Actinobacteria, Deinococcus, and Cyanobacteria) that we call Terrabacteria and associate with an early colonization of land. Divergence time estimates for the major groups of eubacteria are between 2.5–3.2 billion years ago (Ga) while those for archaebacteria are mostly between 3.1–4.1 Ga. The time estimates suggest a Hadean origin of life (prior to 4.1 Ga), an early origin of methanogenesis (3.8–4.1 Ga), an origin of anaerobic methanotrophy after 3.1 Ga, an origin of phototrophy prior to 3.2 Ga, an early colonization of land 2.8–3.1 Ga, and an origin of aerobic methanotrophy 2.5–2.8 Ga.ConclusionsOur early time estimates for methanogenesis support the consideration of methane, in addition to carbon dioxide, as a greenhouse gas responsible for the early warming of the Earths' surface. Our divergence times for the origin of anaerobic methanotrophy are compatible with highly depleted carbon isotopic values found in rocks dated 2.8–2.6 Ga. An early origin of phototrophy is consistent with the earliest bacterial mats and structures identified as stromatolites, but a 2.6 Ga origin of cyanobacteria suggests that those Archean structures, if biologically produced, were made by anoxygenic photosynthesizers. The resistance to desiccation of Terrabacteria and their elaboration of photoprotective compounds suggests that the common ancestor of this group inhabited land. If true, then oxygenic photosynthesis may owe its origin to terrestrial adaptations.

Molecular evidence for the early colonization of land by fungi and plants.

The colonization of land by eukaryotes probably was facilitated by a partnership (symbiosis) between a photosynthesizing organism (phototroph) and a fungus. However, the time when colonization occurred remains speculative. The first fossil land plants and fungi appeared 480 to 460 million years ago (Ma), whereas molecular clock estimates suggest an earlier colonization of land, about 600 Ma. Our protein sequence analyses indicate that green algae and major lineages of fungi were present 1000 Ma and that land plants appeared by 700 Ma, possibly affecting Earth's atmosphere, climate, and evolution of animals in the Precambrian.