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1.
New Phytol ; 243(1): 398-406, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38757767

ABSTRACT

The minute 'dust seeds' of some terrestrial orchids preferentially germinate and develop as mycoheterotrophic protocorms near conspecific adult plants. Here we test the hypothesis that mycorrhizal mycelial connections provide a direct pathway for transfer of recent photosynthate from conspecific green orchids to achlorophyllous protocorms. Mycelial networks of Ceratobasidium cornigerum connecting green Dactylorhiza fuchsii plants with developing achlorophyllous protocorms of the same species were established on oatmeal or water agar before the shoots of green plants were exposed to 14CO2. After incubation for 48 h, the pattern of distribution of fixed carbon was visualised in intact entire autotrophic/protocorm systems using digital autoradiography and quantified in protocorms by liquid scintillation counting. Both methods of analysis revealed accumulation of 14C above background levels in protocorms, confirming that autotrophic plants supply carbon to juveniles via common mycorrhizal networks. Despite some accumulation of plant-fixed carbon in the fungal mycelium grown on oatmeal agar, a greater amount of carbon was transferred to protocorms growing on water agar, indicating that the polarity of transfer may be influenced by sink strength. We suggest this transfer pathway may contribute significantly to the pattern and processes determining localised orchid establishment in nature, and that 'parental nurture' via common mycelial networks may be involved in these processes.


Subject(s)
Autotrophic Processes , Heterotrophic Processes , Mycorrhizae , Orchidaceae , Photosynthesis , Mycorrhizae/physiology , Orchidaceae/microbiology , Mycelium , Carbon/metabolism , Carbon Radioisotopes
2.
Glob Chang Biol ; 30(1): e17104, 2024 Jan.
Article in English | MEDLINE | ID: mdl-38273555

ABSTRACT

Globally pervasive increases in atmospheric CO2 and nitrogen (N) deposition could have substantial effects on plant communities, either directly or mediated by their interactions with soil nutrient limitation. While the direct consequences of N enrichment on plant communities are well documented, potential interactions with rising CO2 and globally widespread phosphorus (P) limitation remain poorly understood. We investigated the consequences of simultaneous elevated CO2 (eCO2 ) and N and P additions on grassland biodiversity, community and functional composition in P-limited grasslands. We exposed soil-turf monoliths from limestone and acidic grasslands that have received >25 years of N additions (3.5 and 14 g m-2 year-1 ) and 11 (limestone) or 25 (acidic) years of P additions (3.5 g m-2 year-1 ) to eCO2 (600 ppm) for 3 years. Across both grasslands, eCO2 , N and P additions significantly changed community composition. Limestone communities were more responsive to eCO2 and saw significant functional shifts resulting from eCO2 -nutrient interactions. Here, legume cover tripled in response to combined eCO2 and P additions, and combined eCO2 and N treatments shifted functional dominance from grasses to sedges. We suggest that eCO2 may disproportionately benefit P acquisition by sedges by subsidising the carbon cost of locally intense root exudation at the expense of co-occurring grasses. In contrast, the functional composition of the acidic grassland was insensitive to eCO2 and its interactions with nutrient additions. Greater diversity of P-acquisition strategies in the limestone grassland, combined with a more functionally even and diverse community, may contribute to the stronger responses compared to the acidic grassland. Our work suggests we may see large changes in the composition and biodiversity of P-limited grasslands in response to eCO2 and its interactions with nutrient loading, particularly where these contain a high diversity of P-acquisition strategies or developmentally young soils with sufficient bioavailable mineral P.


Subject(s)
Carbon Dioxide , Grassland , Carbon Dioxide/analysis , Phosphorus , Plants , Poaceae , Nitrogen , Soil/chemistry , Calcium Carbonate
3.
Sci Total Environ ; 852: 158358, 2022 Dec 15.
Article in English | MEDLINE | ID: mdl-36049686

ABSTRACT

Conventional arable cropping with annual crops established by ploughing and harrowing degrades larger soil aggregates that contribute to storing soil organic carbon (SOC). The urgent need to increase SOC content of arable soils to improve their functioning and sequester atmospheric CO2 has motivated studies into the effects of reintroducing leys into long-term conventional arable fields. However, effects of short-term leys on total SOC accumulation have been equivocal. As soil aggregation may be important for carbon storage, we investigated the effects of arable-to-ley conversion on cambisol soil after three years of ley, on concentrations and stocks of SOC, nitrogen and their distributions in different sized water-stable aggregates. These values were benchmarked against soil from beneath hedgerow margins. SOC stocks (0-7 cm depth) rose from 20.3 to 22.6 Mg ha-1 in the arable-to-ley conversion, compared to 30 Mg ha-1 in hedgerows, but this 2.3 Mg ha-1 difference (or 0.77 Mg C ha-1 yr-1) was not significant). However, the proportion of large macroaggregates (> 2000 µm) increased 5.4-fold in the arable-to-ley conversion, recovering to similar abundance as hedgerow soils, driving near parallel increases in SOC and nitrogen within large macroaggregates (5.1 and 5.7-fold respectively). The total SOC (0-7 cm depth) stored in large macroaggregates increased from 2.0 to 9.6 Mg ha-1 in the arable-to-ley conversion, which no longer differed significantly from the 12.1 Mg ha-1 under hedgerows. The carbon therefore accumulated three times faster, at 2.53 Mg C ha-1 yr-1, in the large macroaggregates compared to the bulk soil. These findings highlight the value of monitoring large macroaggregate-bound SOC as a key early indicator of shifts in soil quality in response to change in field management, and the benefits of leys in soil aggregation, carbon accumulation, and soil functioning, providing justification for fiscal incentives that encourage wider use of leys in arable rotations.


Subject(s)
Soil , Trifolium , Carbon , Nitrogen , Carbon Sequestration , Poaceae , Medicago , Carbon Dioxide , Agriculture , Water
4.
Front Plant Sci ; 13: 955985, 2022.
Article in English | MEDLINE | ID: mdl-36092419

ABSTRACT

Wheat yields have plateaued in the UK over the last 25 years, during which time most arable land has been annually cropped continuously with short rotations dominated by cereals. Arable intensification has depleted soil organic matter and biology, including mycorrhizas, which are affected by tillage, herbicides, and crop genotype. Here, we test whether winter wheat yields, mycorrhization, and shoot health can be improved simply by adopting less intensive tillage and adding commercial mycorrhizal inoculum to long-term arable fields, or if 3-year grass-clover leys followed direct drilling is more effective for biological regeneration of soil with reduced N fertiliser. We report a trial of mycorrhization, ear pathology, and yield performance of the parents and four double haploid lines from the Avalon x Cadenza winter wheat population in a long-term arable field that is divided into replicated treatment plots. These plots comprised wheat lines grown using ploughing or disc cultivation for 3 years, half of which received annual additions of commercial arbuscular mycorrhizal (AM) inoculum, compared to 3-year mown grass-clover ley plots treated with glyphosate and direct-drilled. All plots annually received 35 kg of N ha-1 fertiliser without fungicides. The wheat lines did not differ in mycorrhization, which averaged only 34% and 40% of root length colonised (RLC) in the ploughed and disc-cultivated plots, respectively, and decreased with inoculation. In the ley, RLC increased to 52%. Two wheat lines were very susceptible to a sooty ear mould, which was lowest in the ley, and highest with disc cultivation. AM inoculation reduced ear infections by >50% in the susceptible lines. In the ley, yields ranged from 7.2 to 8.3 t ha-1, achieving 92 to 106% of UK average wheat yield in 2018 (7.8 t ha-1) but using only 25% of average N fertiliser. Yields with ploughing and disc cultivation averaged only 3.9 and 3.4 t ha-1, respectively, with AM inoculum reducing yields from 4.3 to 3.5 t ha-1 in ploughed plots, with no effect of disc cultivation. The findings reveal multiple benefits of reintegrating legume-rich leys into arable rotations as part of a strategy to regenerate soil quality and wheat crop health, reduce dependence on nitrogen fertilisers, enhance mycorrhization, and achieve good yields.

5.
Proc Natl Acad Sci U S A ; 118(11)2021 03 16.
Article in English | MEDLINE | ID: mdl-33836596

ABSTRACT

Legume trees form an abundant and functionally important component of tropical forests worldwide with N2-fixing symbioses linked to enhanced growth and recruitment in early secondary succession. However, it remains unclear how N2-fixers meet the high demands for inorganic nutrients imposed by rapid biomass accumulation on nutrient-poor tropical soils. Here, we show that N2-fixing trees in secondary Neotropical forests triggered twofold higher in situ weathering of fresh primary silicates compared to non-N2-fixing trees and induced locally enhanced nutrient cycling by the soil microbiome community. Shotgun metagenomic data from weathered minerals support the role of enhanced nitrogen and carbon cycling in increasing acidity and weathering. Metagenomic and marker gene analyses further revealed increased microbial potential beneath N2-fixers for anaerobic iron reduction, a process regulating the pool of phosphorus bound to iron-bearing soil minerals. We find that the Fe(III)-reducing gene pool in soil is dominated by acidophilic Acidobacteria, including a highly abundant genus of previously undescribed bacteria, Candidatus Acidoferrum, genus novus. The resulting dependence of the Fe-cycling gene pool to pH determines the high iron-reducing potential encoded in the metagenome of the more acidic soils of N2-fixers and their nonfixing neighbors. We infer that by promoting the activities of a specialized local microbiome through changes in soil pH and C:N ratios, N2-fixing trees can influence the wider biogeochemical functioning of tropical forest ecosystems in a manner that enhances their ability to assimilate and store atmospheric carbon.


Subject(s)
Fabaceae/microbiology , Forests , Microbiota/physiology , Minerals/metabolism , Nutrients/metabolism , Tropical Climate , Acidobacteria/classification , Acidobacteria/genetics , Acidobacteria/metabolism , Biomass , Carbon/analysis , Fabaceae/growth & development , Fabaceae/metabolism , Ferric Compounds/metabolism , Hydrogen-Ion Concentration , Microbiota/genetics , Minerals/analysis , Nitrogen/analysis , Nitrogen/metabolism , Nitrogen Fixation , Nutrients/analysis , Panama , Phosphorus/metabolism , Silicates/analysis , Silicates/metabolism , Soil/chemistry , Soil Microbiology , Symbiosis , Trees/growth & development , Trees/metabolism , Trees/microbiology
6.
Mycorrhiza ; 31(1): 69-83, 2021 Jan.
Article in English | MEDLINE | ID: mdl-33200348

ABSTRACT

Many plant species form symbioses with ectomycorrhizal fungi, which help them forage for limiting nutrients in the soil such as inorganic phosphate (Pi). The transcriptional responses to symbiosis and nutrient-limiting conditions in ectomycorrhizal fungal hyphae, however, are largely unknown. An artificial system was developed to study ectomycorrhizal basidiomycete Paxillus involutus growth in symbiosis with its host tree Pinus sylvestris at different Pi concentrations. RNA-seq analysis was performed on P. involutus hyphae growing under Pi-limiting conditions, either in symbiosis or alone. We show that Pi starvation and ectomycorrhizal symbiosis have an independent effect on the P. involutus transcriptome. Notably, low Pi availability induces expression of newly identified putative high-affinity Pi transporter genes, while reducing the expression of putative organic acid transporters. Additionally, low Pi availability induces a close transcriptional interplay between P and N metabolism. GTP-related signalling was found to have a positive effect in the maintenance of ectomycorrhizal symbiosis, whereas multiple putative cytochrome P450 genes were found to be downregulated, unlike arbuscular mycorrhizal fungi. We provide the first evidence of global transcriptional changes induced by low Pi availability and ectomycorrhizal symbiosis in the hyphae of P. involutus, revealing both similarities and differences with better-characterized arbuscular mycorrhizal fungi.


Subject(s)
Mycorrhizae , Pinus sylvestris , Pinus , Basidiomycota , Mycorrhizae/genetics , Phosphates , Pinus sylvestris/genetics , Symbiosis , Transcriptome
7.
Glob Chang Biol ; 26(6): 3658-3676, 2020 06.
Article in English | MEDLINE | ID: mdl-32314496

ABSTRACT

Land-based enhanced rock weathering (ERW) is a biogeochemical carbon dioxide removal (CDR) strategy aiming to accelerate natural geological processes of carbon sequestration through application of crushed silicate rocks, such as basalt, to croplands and forested landscapes. However, the efficacy of the approach when undertaken with basalt, and its potential co-benefits for agriculture, require experimental and field evaluation. Here we report that amending a UK clay-loam agricultural soil with a high loading (10 kg/m2 ) of relatively coarse-grained crushed basalt significantly increased the yield (21 ± 9.4%, SE) of the important C4 cereal Sorghum bicolor under controlled environmental conditions, without accumulation of potentially toxic trace elements in the seeds. Yield increases resulted from the basalt treatment after 120 days without P- and K-fertilizer addition. Shoot silicon concentrations also increased significantly (26 ± 5.4%, SE), with potential benefits for crop resistance to biotic and abiotic stress. Elemental budgets indicate substantial release of base cations important for inorganic carbon removal and their accumulation mainly in the soil exchangeable pools. Geochemical reactive transport modelling, constrained by elemental budgets, indicated CO2 sequestration rates of 2-4 t CO2 /ha, 1-5 years after a single application of basaltic rock dust, including via newly formed soil carbonate minerals whose long-term fate requires assessment through field trials. This represents an approximately fourfold increase in carbon capture compared to control plant-soil systems without basalt. Our results build support for ERW deployment as a CDR technique compatible with spreading basalt powder on acidic loamy soils common across millions of hectares of western European and North American agriculture.


Subject(s)
Soil , Sorghum , Agriculture , Carbon Dioxide , Dust , Edible Grain , Silicates
8.
Nat Plants ; 6(4): 349-354, 2020 04.
Article in English | MEDLINE | ID: mdl-32203292

ABSTRACT

How species coexist despite competing for the same resources that are in limited supply is central to our understanding of the controls on biodiversity1,2. Resource partitioning may facilitate coexistence, as co-occurring species use different sources of the same limiting resource3,4. In plant communities, however, direct evidence for partitioning of the commonly limiting nutrient, phosphorus (P), has remained scarce due to the challenges of quantifying P acquisition from its different chemical forms present in soil5. To address this, we used 33P to directly trace P uptake from DNA, orthophosphate and calcium phosphate into monocultures and mixed communities of plants growing in grassland soil. We show that co-occurring plants acquire P from these important organic and mineral sources in different proportions, and that differences in P source use are consistent with the species' root adaptations for P acquisition. Furthermore, the net benefit arising from niche plasticity (the gain in P uptake for a species in a mixed community compared to monoculture) correlates with species abundance in the wild, suggesting that niche plasticity for P is a driver of community structure. This evidence for P resource partitioning and niche plasticity may explain the high levels of biodiversity frequently found in P-limited ecosystems worldwide6,7.


Subject(s)
Phosphorus/metabolism , Plants/metabolism , Soil/chemistry , Biodiversity , DNA, Plant/metabolism , Ecosystem , Phosphorus Compounds/metabolism
9.
Sci Rep ; 10(1): 5141, 2020 03 20.
Article in English | MEDLINE | ID: mdl-32198435

ABSTRACT

There is increasing interest in urban food production for reasons of food security, environmental sustainability, social and health benefits. In developed nations urban food growing is largely informal and localised, in gardens, allotments and public spaces, but we know little about the magnitude of this production. Here we couple own-grown crop yield data with garden and allotment areal surveys and urban fruit tree occurrence to provide one of the first estimates for current and potential food production in a UK urban setting. Current production is estimated to be sufficient to supply the urban population with fruit and vegetables for about 30 days per year, while the most optimistic model results suggest that existing land cultivated for food could supply over half of the annual demand. Our findings provide a baseline for current production whilst highlighting the potential for change under the scaling up of cultivation on existing land.


Subject(s)
Food Supply/methods , Gardening/statistics & numerical data , Gardens/statistics & numerical data , Urban Population/statistics & numerical data , Crop Production/methods , Fruit/growth & development , Humans , United Kingdom , Vegetables/growth & development
10.
Sci Total Environ ; 713: 136491, 2020 Apr 15.
Article in English | MEDLINE | ID: mdl-31962242

ABSTRACT

Effects of earthworms on soil physico-hydraulic and chemical properties, herbage production and wheat growth in long-term arable soils following conversion to ley were investigated. Seven intact soil monoliths were collected from each of four arable fields. One monolith per field served as a control. The other six were defaunated by deep-freezing; three were left defaunated (DeF) and three (DeF+E) were repopulated with earthworms to mimic pasture field density and diversity. The monoliths were planted with a grass-clover ley and inserted into pre-established ley strips in their original fields for 12 months. Hydraulic conductivity measurements at -0.5 cm tension (K0.5) were taken five times over the year. K0.5 significantly increased in summer 2017 and spring 2018 and decreased in winter 2017-18. K0.5 was significantly greater (47%) for DeF+E than DeF monoliths. By the end of the experiment, pores >1 mm diameter made a significantly greater contribution to water flow in DeF+E (98%) than DeF (95%) monoliths. After only a year of arable to ley conversion, soil bulk density significantly decreased (by 6%), and organic matter (OM) content increased (by 29%) in the DeF treatments relative to the arable soil. Earthworms improved soil quality further. Compared to DeF monoliths, DeF+E monoliths had significantly increased water-holding capacity (by 9%), plant-available water (by 21%), OM content (by 9%), grass-clover shoot dry biomass (by 58%), water-stable aggregates >250 µm (by 15%) and total N (by 3.5%). In a wheat bioassay following the field experiment, significantly more biomass (20%) was produced on DeF+E than DeF monolith soil, likely due to the changed soil physico-hydraulic properties. Our results show that earthworms play a significant role in improvements to soil quality and functions brought about by arable to ley conversion, and that augmenting depleted earthworm populations can help the restoration of soil qualities adversely impacted by intensive agriculture.


Subject(s)
Oligochaeta , Soil , Agriculture , Animals , Poaceae , Triticum
11.
Sci Total Environ ; 705: 135930, 2020 Feb 25.
Article in English | MEDLINE | ID: mdl-31837547

ABSTRACT

The process of urbanization has detached a large proportion of the global population from involvement with food production. However, there has been a resurgence in interest in urban agriculture and there is widespread recognition by policy-makers of its potential contribution to food security. Despite this, there is little data on urban agricultural production by non-commercial small-scale growers. We combine citizen science data for self-provisioning crop yields with field-mapping and GIS-based analysis of allotments in Leicester, UK, to provide an estimate of allotment fruit and vegetable production at a city-scale. In addition, we examine city-scale changes in allotment land provision on potential crop production over the past century. The average area of individual allotment plots used to grow crops was 52%. Per unit area yields for the majority of crops grown in allotments were similar to those of UK commercial horticulture. We estimate city-wide allotment production of >1200 t of fruit and vegetables and 200 t of potatoes per annum, equivalent to feeding >8500 people. If the 13% of plots that are completely uncultivated were used this could increase production to >1400 t per annum, feeding ~10,000 people, however this production may not be located in areas where there is greatest need for increased access to fresh fruits and vegetables. The citywide contribution of allotment cultivation peaked in the 1950s when 475 ha of land was allotments, compared to 97 ha currently. This suggests a decline from >45,000 to <10,000 of people fed per annum. We demonstrate that urban allotments make a small but important contribution to the fruit and vegetable diet of a UK city. However, further urban population expansion will exert increasing development pressure on allotment land. Policy-makers should both protect allotments within cities, and embed urban agricultural land within future developments to improve local food security.


Subject(s)
Agriculture , Vegetables , Cities , Crops, Agricultural , United Kingdom , Urbanization
12.
Curr Biol ; 30(3): 421-431.e2, 2020 02 03.
Article in English | MEDLINE | ID: mdl-31866369

ABSTRACT

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.


Subject(s)
Biological Evolution , Embryophyta/anatomy & histology , Fossils/anatomy & histology , Trees/anatomy & histology , Embryophyta/physiology , New York , Trees/physiology
13.
New Phytol ; 223(2): 908-921, 2019 07.
Article in English | MEDLINE | ID: mdl-30919981

ABSTRACT

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 15 N-labelled algal necromass and 33 P orthophosphate. Photosynthate allocation to fungi was traced using 14 CO2 . Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15 N, irrespective of atmospheric CO2 concentration. Both symbionts increased 33 P 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.


Subject(s)
Carbon/metabolism , Glomeromycota/physiology , Hepatophyta/microbiology , Mucor/physiology , Nitrogen/metabolism , Phosphorus/metabolism , Plants/microbiology , Symbiosis , Biomass , Endophytes/ultrastructure , Glomeromycota/ultrastructure , Linear Models , Mucor/ultrastructure , Mycelium/metabolism
14.
Nat Plants ; 4(6): 392, 2018 Jun.
Article in English | MEDLINE | ID: mdl-29802316

ABSTRACT

In the version of this Perspective originally published, 'acidification' was incorrectly spelt as 'adification' in Fig. 4. This has now been corrected.

15.
Nat Plants ; 4(3): 138-147, 2018 03.
Article in English | MEDLINE | ID: mdl-29459727

ABSTRACT

The magnitude of future climate change could be moderated by immediately reducing the amount of CO2 entering the atmosphere as a result of energy generation and by adopting strategies that actively remove CO2 from it. Biogeochemical improvement of soils by adding crushed, fast-reacting silicate rocks to croplands is one such CO2-removal strategy. This approach has the potential to improve crop production, increase protection from pests and diseases, and restore soil fertility and structure. Managed croplands worldwide are already equipped for frequent rock dust additions to soils, making rapid adoption at scale feasible, and the potential benefits could generate financial incentives for widespread adoption in the agricultural sector. However, there are still obstacles to be surmounted. Audited field-scale assessments of the efficacy of CO2 capture are urgently required together with detailed environmental monitoring. A cost-effective way to meet the rock requirements for CO2 removal must be found, possibly involving the recycling of silicate waste materials. Finally, issues of public perception, trust and acceptance must also be addressed.


Subject(s)
Climate Change , Crop Production , Food Supply , Soil , Soil/standards
16.
Proc Biol Sci ; 284(1860)2017 Aug 16.
Article in English | MEDLINE | ID: mdl-28814651

ABSTRACT

Fossil and phylogenetic evidence indicates legume-rich modern tropical forests replaced Late Cretaceous palm-dominated tropical forests across four continents during the early Cenozoic (58-42 Ma). Tropical legume trees can transform ecosystems via their ability to fix dinitrogen (N2) and higher leaf N compared with non-legumes (35-65%), but it is unclear how their evolutionary rise contributed to silicate weathering, the long-term sink for atmospheric carbon dioxide (CO2). Here we hypothesize that the increasing abundance of N2-fixing legumes in tropical forests amplified silicate weathering rates by increased input of fixed nitrogen (N) to terrestrial ecosystems via interrelated mechanisms including increasing microbial respiration and soil acidification, and stimulating forest net primary productivity. We suggest the high CO2 early Cenozoic atmosphere further amplified legume weathering. Evolution of legumes with high weathering rates was probably driven by their high demand for phosphorus and micronutrients required for N2-fixation and nodule formation.


Subject(s)
Biological Evolution , Fabaceae/physiology , Forests , Nitrogen Fixation , Tropical Climate , Atmosphere/chemistry , Carbon Dioxide/chemistry , Fabaceae/classification , Nitrogen/chemistry , Phylogeny , Soil/chemistry , Trees/classification , Trees/physiology
17.
ISME J ; 10(6): 1514-26, 2016 06.
Article in English | MEDLINE | ID: mdl-26613340

ABSTRACT

Most land plants form mutualistic associations with arbuscular mycorrhizal fungi of the Glomeromycota, but recent studies have found that ancient plant lineages form mutualisms with Mucoromycotina fungi. Simultaneous associations with both fungal lineages have now been found in some plants, necessitating studies to understand the functional and evolutionary significance of these tripartite associations for the first time. We investigate the physiology and cytology of dual fungal symbioses in the early-diverging liverworts Allisonia and Neohodgsonia at modern and Palaeozoic-like elevated atmospheric CO2 concentrations under which they are thought to have evolved. We found enhanced carbon cost to liverworts with simultaneous Mucoromycotina and Glomeromycota associations, greater nutrient gain compared with those symbiotic with only one fungal group in previous experiments and contrasting responses to atmospheric CO2 among liverwort-fungal symbioses. In liverwort-Mucoromycotina symbioses, there is increased P-for-C and N-for-C exchange efficiency at 440 p.p.m. compared with 1500 p.p.m. CO2. In liverwort-Glomeromycota symbioses, P-for-C exchange is lower at ambient CO2 compared with elevated CO2. No characteristic cytologies of dual symbiosis were identified. We provide evidence of a distinct physiological niche for plant symbioses with Mucoromycotina fungi, giving novel insight into why dual symbioses with Mucoromycotina and Glomeromycota fungi persist to the present day.


Subject(s)
Carbon Dioxide/pharmacology , Fungi/physiology , Glomeromycota/physiology , Hepatophyta/microbiology , Mycorrhizae/physiology , Symbiosis , Biological Evolution , Carbon/metabolism , Fungi/drug effects , Fungi/ultrastructure , Glomeromycota/drug effects , Glomeromycota/ultrastructure , Hepatophyta/drug effects , Hepatophyta/ultrastructure , Mycorrhizae/drug effects , Mycorrhizae/ultrastructure , Phylogeny , Plant Roots/microbiology
18.
Proc Biol Sci ; 282(1813): 20151115, 2015 Aug 22.
Article in English | MEDLINE | ID: mdl-26246550

ABSTRACT

How the colonization of terrestrial environments by early land plants over 400 Ma influenced rock weathering, the biogeochemical cycling of carbon and phosphorus, and climate in the Palaeozoic is uncertain. Here we show experimentally that mineral weathering by liverworts­an extant lineage of early land plants­partnering arbuscular mycorrhizal (AM) fungi, like those in 410 Ma-old early land plant fossils, amplified calcium weathering from basalt grains threefold to sevenfold, relative to plant-free controls. Phosphate weathering by mycorrhizal liverworts was amplified 9-13-fold over plant-free controls, compared with fivefold to sevenfold amplification by liverworts lacking fungal symbionts. Etching and trenching of phyllosilicate minerals increased with AM fungal network size and atmospheric CO2 concentration. Integration of grain-scale weathering rates over the depths of liverwort rhizoids and mycelia (0.1 m), or tree roots and mycelia (0.75 m), indicate early land plants with shallow anchorage systems were probably at least 10-fold less effective at enhancing the total weathering flux than later-evolving trees. This work challenges the suggestion that early land plants significantly enhanced total weathering and land-to-ocean fluxes of calcium and phosphorus, which have been proposed as a trigger for transient dramatic atmospheric CO2 sequestration and glaciations in the Ordovician.


Subject(s)
Biological Evolution , Carbon Dioxide/analysis , Climate Change , Marchantia/growth & development , Mycorrhizae/growth & development , Evolution, Planetary
19.
Environ Sci Technol ; 49(14): 8339-46, 2015 Jul 21.
Article in English | MEDLINE | ID: mdl-26114917

ABSTRACT

Soil holds 75% of the total organic carbon (TOC) stock in terrestrial ecosystems. This comprises ecosystem-derived organic carbon (OC) and black carbon (BC), a recalcitrant product of the incomplete combustion of fossil fuels and biomass. Urban topsoils are often enriched in BC from historical emissions of soot and have high TOC concentrations, but the contribution of BC to TOC throughout the urban soil profile, at a regional scale is unknown. We sampled 55 urban soil profiles across the North East of England, a region with a history of coal burning and heavy industry. Through combined elemental and thermogravimetic analyses, we found very large total soil OC stocks (31-65 kg m(-2) to 1 m), exceeding typical values reported for UK woodland soils. BC contributed 28-39% of the TOC stocks, up to 23 kg C m(-2) to 1 m, and was affected by soil texture. The proportional contribution of the BC-rich fraction to TOC increased with soil depth, and was enriched in topsoil under trees when compared to grassland. Our findings establish the importance of urban ecosystems in storing large amounts of OC in soils and that these soils also capture a large proportion of BC particulates emitted within urban areas.


Subject(s)
Carbon/analysis , Cities , Organic Chemicals/analysis , Soil/chemistry , Soot/analysis , England , Grassland , Soil Pollutants/analysis
20.
New Phytol ; 205(4): 1492-1502, 2015 Mar.
Article in English | MEDLINE | ID: mdl-25615559

ABSTRACT

Mycorrhizal functioning in the fern Ophioglossum is complex and poorly understood. It is unknown whether mature O. vulgatum sporophytes form mutualistic associations with fungi of the Glomeromycota and with what specificity. Are green sporophytes able to 'repay' fungal carbon (C) invested in them by mycorrhizal partners during the initially heterotrophic gametophyte and early sporophyte stages of the lifecycle? We identified fungal partners of O. vulgatum sporophytes using molecular techniques and supplied them with (33) P-orthophosphate and O. vulgatum sporophytes with (14) CO2 . We traced the movement of fungal-acquired nutrients and plant-fixed C between symbionts and analysed natural abundance (13) C and (15) N isotope signatures to assess nutritional interactions. We found fungal specificity of O. vulgatum sporophytes towards a mycorrhizal fungus closely related to Glomus macrocarpum. Our radioisotope tracers revealed reciprocal C-for-phosphorus exchange between fern sporophytes and fungal partners, despite competition from surrounding vegetation. Monocultures of O. vulgatum were enriched in (13) C and (15) N, providing inconclusive evidence of mycoheterotrophy when experiencing competition from the surrounding plant community. We show mutualistic and specific symbiosis between a eusporangiate fern and fungi of the Glomeromycota. Our findings suggest a 'take now, pay later' strategy of mycorrhizal functioning through the lifecycle O. vulgatum, from mycoheterotrophic gametophyte to mutualistic aboveground sporophyte.


Subject(s)
Ferns/microbiology , Glomeromycota/physiology , Heterotrophic Processes/physiology , Mycorrhizae/physiology , Symbiosis/physiology , Analysis of Variance , Biological Evolution , Biomass , Carbon/metabolism , Colony Count, Microbial , Glomeromycota/growth & development , Molecular Sequence Data , Mycorrhizae/growth & development , Nitrogen/metabolism , Phosphorus/metabolism , Plant Roots/metabolism , Plant Shoots/metabolism , Soil/chemistry , Species Specificity
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