Publications by authors named "Martin Bidartondo"

66 Publications

Critical research challenges facing Mucoromycotina 'fine root endophytes'.

New Phytol 2021 11 13;232(4):1528-1534. Epub 2021 Sep 13.

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK.

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http://dx.doi.org/10.1111/nph.17684DOI Listing
November 2021

Ectomycorrhizas and tipping points in forest ecosystems.

New Phytol 2021 09 8;231(5):1700-1707. Epub 2021 Jul 8.

Soil Biology Group, Wageningen University & Research, Wageningen, 6700 AA, the Netherlands.

The resilience of forests is compromised by human-induced environmental influences pushing them towards tipping points and resulting in major shifts in ecosystem state that might be difficult to reverse, are difficult to predict and manage, and can have vast ecological, economic and social consequences. The literature on tipping points has grown rapidly, but almost exclusively based on aquatic and aboveground systems. So far little effort has been made to make links to soil systems, where change is not as drastically apparent, timescales may differ and recovery may be slower. Predicting belowground ecosystem state transitions and recovery, and their impacts on aboveground systems, remains a major scientific, practical and policy challenge. Recently observed major changes in aboveground tree condition across European forests are probably causally linked to ectomycorrhizal (EM) fungal changes belowground. Based on recent breakthroughs in data collection and analysis, we apply tipping point theory to forests, including their belowground component, focusing on EM fungi; link environmental thresholds for EM fungi with nutrient imbalances in forest trees; explore the role of phenotypic plasticity in EM fungal adaptation to, and recovery from, environmental change; and propose major positive feedback mechanisms to understand, address and predict forest ecosystem tipping points.
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http://dx.doi.org/10.1111/nph.17547DOI Listing
September 2021

Carbon for nutrient exchange between Lycopodiella inundata and Mucoromycotina fine root endophytes is unresponsive to high atmospheric CO.

Mycorrhiza 2021 Jul 21;31(4):431-440. Epub 2021 Apr 21.

Deparment of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK.

Non-vascular plants associating with arbuscular mycorrhizal (AMF) and Mucoromycotina 'fine root endophyte' (MFRE) fungi derive greater benefits from their fungal associates under higher atmospheric [CO] (a[CO]) than ambient; however, nothing is known about how changes in a[CO] affect MFRE function in vascular plants. We measured movement of phosphorus (P), nitrogen (N) and carbon (C) between the lycophyte Lycopodiella inundata and Mucoromycotina fine root endophyte fungi using P-orthophosphate,  N-ammonium chloride and CO isotope tracers under ambient and elevated a[CO] concentrations of 440 and 800 ppm, respectively. Transfers of P and  N from MFRE to plants were unaffected by changes in a[CO]. There was a slight increase in C transfer from plants to MFRE under elevated a[CO]. Our results demonstrate that the exchange of C-for-nutrients between a vascular plant and Mucoromycotina FRE is largely unaffected by changes in a[CO]. Unravelling the role of MFRE in host plant nutrition and potential C-for-N trade changes between symbionts under different abiotic conditions is imperative to further our understanding of the past, present and future roles of plant-fungal symbioses in ecosystems.
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http://dx.doi.org/10.1007/s00572-021-01033-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8266774PMC
July 2021

Connecting high-throughput biodiversity inventories: Opportunities for a site-based genomic framework for global integration and synthesis.

Mol Ecol 2021 03 2;30(5):1120-1135. Epub 2021 Feb 2.

Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de la Laguna, Spain.

High-throughput sequencing (HTS) is increasingly being used for the characterization and monitoring of biodiversity. If applied in a structured way, across broad geographical scales, it offers the potential for a much deeper understanding of global biodiversity through the integration of massive quantities of molecular inventory data generated independently at local, regional and global scales. The universality, reliability and efficiency of HTS data can potentially facilitate the seamless linking of data among species assemblages from different sites, at different hierarchical levels of diversity, for any taxonomic group and regardless of prior taxonomic knowledge. However, collective international efforts are required to optimally exploit the potential of site-based HTS data for global integration and synthesis, efforts that at present are limited to the microbial domain. To contribute to the development of an analogous strategy for the nonmicrobial terrestrial domain, an international symposium entitled "Next Generation Biodiversity Monitoring" was held in November 2019 in Nicosia (Cyprus). The symposium brought together evolutionary geneticists, ecologists and biodiversity scientists involved in diverse regional and global initiatives using HTS as a core tool for biodiversity assessment. In this review, we summarize the consensus that emerged from the 3-day symposium. We converged on the opinion that an effective terrestrial Genomic Observatories network for global biodiversity integration and synthesis should be spatially led and strategically united under the umbrella of the metabarcoding approach. Subsequently, we outline an HTS-based strategy to collectively build an integrative framework for site-based biodiversity data generation.
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http://dx.doi.org/10.1111/mec.15797DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7986105PMC
March 2021

Habitat specialisation controls ectomycorrhizal fungi above the treeline in the European Alps.

New Phytol 2021 03 30;229(5):2901-2916. Epub 2020 Nov 30.

Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, TW9 3DS, UK.

Alpine habitats are one of the most vulnerable ecosystems to environmental change, however, little information is known about the drivers of plant-fungal interactions in these ecosystems and their resilience to climate change. We investigated the influence of the main drivers of ectomycorrhizal (EM) fungal communities along elevation and environmental gradients in the alpine zone of the European Alps and measured their degree of specialisation using network analysis. We sampled ectomycorrhizas of Dryas octopetala, Bistorta vivipara and Salix herbacea, and soil fungal communities at 28 locations across five countries, from the treeline to the nival zone. We found that: (1) EM fungal community composition, but not richness, changes along elevation, (2) there is no strong evidence of host specialisation, however, EM fungal networks in the alpine zone and within these, EM fungi associated with snowbed communities, are more specialised than in other alpine habitats, (3) plant host population structure does not influence EM fungal communities, and (4) most variability in EM fungal communities is explained by fine-scale changes in edaphic properties, like soil pH and total nitrogen. The higher specialisation and narrower ecological niches of these plant-fungal interactions in snowbed habitats make these habitats particularly vulnerable to environmental change in alpine ecosystems.
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http://dx.doi.org/10.1111/nph.17033DOI Listing
March 2021

Phenology and function in lycopod-Mucoromycotina symbiosis.

New Phytol 2021 03 28;229(5):2389-2394. Epub 2020 Nov 28.

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK.

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http://dx.doi.org/10.1111/nph.17009DOI Listing
March 2021

Prevalence and phenology of fine root endophyte colonization across populations of Lycopodiella inundata.

Mycorrhiza 2020 Sep 30;30(5):577-587. Epub 2020 Jul 30.

Department of Comparative Plant & Fungal Biology, Royal Botanic Gardens, Kew, London, TW9 3AB, UK.

Mycorrhizal fungi are critical components of terrestrial habitats and agroecosystems. Recently, Mucoromycotina fine root endophyte fungi (MucFRE) were found to engage in nutritional mutualism with Lycopodiella inundata, which belongs to one of the earliest vascular plant lineages known to associate with MucFRE. The extent to which this mutualism plays a role in resilient plant populations can only be understood by examining its occurrence rate and phenological patterns. To test for prevalence and seasonality in colonization, we examined 1305 individual L. inundata roots from 275 plants collected during spring and autumn 2019 across 11 semi-natural heathlands in Britain and the Netherlands. We quantified presence/absence of fine root endophyte (FRE) hyphae and vesicles and explored possible relationships between temperature and precipitation in the months immediately before sampling. Fine root endophyte hyphae were dominant in all of the examined heathlands, and every colonized root had FRE in both cortical cells and root hairs. However, we found significant differences in colonization between the two seasons at every site. Overall, 14% of L. inundata roots were colonized in spring (2.4% with vesicles) compared with 86% in autumn (7.6% with vesicles). Colonization levels between populations were also significantly different, correlating with temperature and precipitation, suggesting some local environments may be more conducive to root and related hyphal growth. These marked seasonal differences in host-plant colonization suggest that results about FRE from single time point collections should be carefully interpreted. Our findings are relevant to habitat restoration, species conservation plans, agricultural bio-inoculation treatments, and microbial diversity studies.
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http://dx.doi.org/10.1007/s00572-020-00979-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7392370PMC
September 2020

Recovery of mycorrhizal fungi from wild collected protocorms of Madagascan endemic orchid Aerangis ellisii (B.S. Williams) Schltr. and their use in seed germination in vitro.

Mycorrhiza 2020 Sep 14;30(5):567-576. Epub 2020 Jun 14.

Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK.

Orchid mycorrhizal fungi (OMF) are critical for seed germination and maintaining natural populations of orchids, yet the degree of specificity of most orchids to their mycorrhizal associates remains unknown. Many orchids are at risk of extinction, whether generalists or specialists, but orchid species of narrow fungal specificity are arguably under increased threat due to their requirement for specific fungal symbionts. This study characterises the fungi associated with Aerangis ellisii, a lithophytic orchid from a site in the Central Highlands of Madagascar. Culturable OMF isolated from spontaneous protocorms of this species from the wild were used for seed germination. In vitro germination and seedling development of A. ellisii were achieved with fungi derived from A. ellisii and an isolate from a different Aerangis species 30 km away. The significance of these findings and their importance to conservation strategies for this species and other Aerangis spp. is discussed. These results have important implications for the conservation of A. ellisii populations in Madagascar.
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http://dx.doi.org/10.1007/s00572-020-00971-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7410863PMC
September 2020

The distribution and evolution of fungal symbioses in ancient lineages of land plants.

Mycorrhiza 2020 Jan 4;30(1):23-49. Epub 2020 Mar 4.

Department of Life Sciences, Algae, Fungi and Plants Division, Natural History Museum, London, London, SW7 5BD, UK.

An accurate understanding of the diversity and distribution of fungal symbioses in land plants is essential for mycorrhizal research. Here we update the seminal work of Wang and Qiu (Mycorrhiza 16:299-363, 2006) with a long-overdue focus on early-diverging land plant lineages, which were considerably under-represented in their survey, by examining the published literature to compile data on the status of fungal symbioses in liverworts, hornworts and lycophytes. Our survey combines data from 84 publications, including recent, post-2006, reports of Mucoromycotina associations in these lineages, to produce a list of at least 591 species with known fungal symbiosis status, 180 of which were included in Wang and Qiu (Mycorrhiza 16:299-363, 2006). Using this up-to-date compilation, we estimate that fewer than 30% of liverwort species engage in symbiosis with fungi belonging to all three mycorrhizal phyla, Mucoromycota, Basidiomycota and Ascomycota, with the last being the most widespread (17%). Fungal symbioses in hornworts (78%) and lycophytes (up to 100%) appear to be more common but involve only members of the two Mucoromycota subphyla Mucoromycotina and Glomeromycotina, with Glomeromycotina prevailing in both plant groups. Our fungal symbiosis occurrence estimates are considerably more conservative than those published previously, but they too may represent overestimates due to currently unavoidable assumptions.
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http://dx.doi.org/10.1007/s00572-020-00938-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7062687PMC
January 2020

Evolution and networks in ancient and widespread symbioses between Mucoromycotina and liverworts.

Mycorrhiza 2019 Nov 13;29(6):551-565. Epub 2019 Nov 13.

Department of Life Sciences, Imperial College London, London, SW7 2AZ, UK.

Like the majority of land plants, liverworts regularly form intimate symbioses with arbuscular mycorrhizal fungi (Glomeromycotina). Recent phylogenetic and physiological studies report that they also form intimate symbioses with Mucoromycotina fungi and that some of these, like those involving Glomeromycotina, represent nutritional mutualisms. To compare these symbioses, we carried out a global analysis of Mucoromycotina fungi in liverworts and other plants using species delimitation, ancestral reconstruction, and network analyses. We found that Mucoromycotina are more common and diverse symbionts of liverworts than previously thought, globally distributed, ancestral, and often co-occur with Glomeromycotina within plants. However, our results also suggest that the associations formed by Mucoromycotina fungi are fundamentally different because, unlike Glomeromycotina, they may have evolved multiple times and their symbiotic networks are un-nested (i.e., not forming nested subsets of species). We infer that the global Mucoromycotina symbiosis is evolutionarily and ecologically distinctive.
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http://dx.doi.org/10.1007/s00572-019-00918-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6890582PMC
November 2019

Mucoromycotina Fine Root Endophyte Fungi Form Nutritional Mutualisms with Vascular Plants.

Plant Physiol 2019 10 29;181(2):565-577. Epub 2019 Jul 29.

Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, LS2 9JT, United Kingdom

Fungi and plants have engaged in intimate symbioses that are globally widespread and have driven terrestrial biogeochemical processes since plant terrestrialization >500 million years ago. Recently, hitherto unknown nutritional mutualisms involving ancient lineages of fungi and nonvascular plants have been discovered, although their extent and functional significance in vascular plants remain uncertain. Here, we provide evidence of carbon-for-nitrogen exchange between an early-diverging vascular plant () and Mucoromycotina (Endogonales) fine root endophyte fungi. Furthermore, we demonstrate that the same fungal symbionts colonize neighboring nonvascular and flowering plants. These findings fundamentally change our understanding of the physiology, interrelationships, and ecology of underground plant-fungal symbioses in modern terrestrial ecosystems by revealing the nutritional role of Mucoromycotina fungal symbionts in vascular plants.
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http://dx.doi.org/10.1104/pp.19.00729DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776871PMC
October 2019

Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts.

New Phytol 2019 07 5;223(2):908-921. Epub 2019 May 5.

Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK.

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 [CO ], as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with N-labelled algal necromass and P orthophosphate. Photosynthate allocation to fungi was traced using CO . Only Mucoromycotina fungal partners provided liverworts with substantial access to algal N, irrespective of atmospheric CO concentration. Both symbionts increased 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.
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http://dx.doi.org/10.1111/nph.15819DOI Listing
July 2019

Light limitation and partial mycoheterotrophy in rhizoctonia-associated orchids.

Oecologia 2019 Feb 23;189(2):375-383. Epub 2019 Jan 23.

Laboratory of Isotope Biogeochemistry, Bayreuth Center of Ecology and Environmental Research (BayCEER), University of Bayreuth, 95440, Bayreuth, Germany.

Partially mycoheterotrophic (PMH) plants obtain organic molecules from their mycorrhizal fungi in addition to carbon (C) fixed by photosynthesis. Some PMH orchids associated with ectomycorrhizal fungi have been shown to flexibly adjust the proportion of organic molecules obtained from fungi according to the habitat's light level. We hypothesise that Neottia ovata and Ophrys insectifera, two orchids associated with saprotrophic rhizoctonia fungi, are also able to increase uptake of organic molecules from fungi as irradiance levels decrease. We continuously measured light availability for individuals of N. ovata and O. insectifera at a grassland and a forest during orchid flowering and fruiting. We repeatedly sampled leaves of N. ovata, O. insectifera and autotrophic reference species for stable isotope natural abundances (δC, δN, δH, δO) and C and N concentrations. We found significant C enrichment in both orchids relative to autotrophic references at the forest but not the grassland, and significant H enrichment at both sites. The C enrichment in O. insectifera was linearly correlated with the habitat's irradiance levels. We conclude that both species can be considered as PMH and at least in O. insectifera, the degree of partial mycoheterotrophy can be fine-tuned according to light availability. However, exploitation of mycorrhizal fungi appears less flexible in saprotroph-associated orchids than in orchids associated with ectomycorrhizal fungi.
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http://dx.doi.org/10.1007/s00442-019-04340-0DOI Listing
February 2019

Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: A review.

Environ Pollut 2019 Mar 28;246:148-162. Epub 2018 Nov 28.

Earth Systems Research Center, University of New Hampshire, 8 College Road, Durham, NH, 03824-0322, USA. Electronic address:

Humans have dramatically increased atmospheric nitrogen (N) deposition globally. At the coarsest resolution, N deposition is correlated with shifts from ectomycorrhizal (EcM) to arbuscular mycorrhizal (AM) tree dominance. At finer resolution, ectomycorrhizal fungal (EcMF) and arbuscular mycorrhizal fungal (AMF) communities respond strongly to long-term N deposition with the disappearance of key taxa. Conifer-associated EcMF are more sensitive than other EcMF, with current estimates of critical loads at 5-6 kg ha yr for the former and 10-20 kg ha yr for the latter. Where loads are exceeded, strong plant-soil and microbe-soil feedbacks may slow recovery rates after abatement of N deposition. Critical loads for AMF and tropical EcMF require additional study. In general, the responses of EcMF to N deposition are better understood than those of AMF because of methodological tractability. Functional consequences of EcMF community change are linked to decreases by fungi with medium-distance exploration strategies, hydrophobic walls, proteolytic capacity, and perhaps peroxidases for acquiring N from soil organic matter. These functional losses may contribute to declines in forest floor decomposition under N deposition. For AMF, limited capacity to directly access complexed organic N may reduce functional consequences, but research is needed to test this hypothesis. Mycorrhizal biomass often declines with N deposition, but the relative contributions of alternate mechanisms for this decline (lower C supply, higher C cost, physiological stress by N) have not been quantified. Furthermore, fungal biomass and functional responses to N inputs probably depend on ecosystem P status, yet how N deposition-induced P limitation interacts with belowground C flux and mycorrhizal community structure and function is still unclear. Current 'omic analyses indicate potential functional differences among fungal lineages and should be integrated with studies of physiology, host nutrition, growth and health, fungal and plant community structure, and ecosystem processes.
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http://dx.doi.org/10.1016/j.envpol.2018.11.074DOI Listing
March 2019

Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi.

Proc Biol Sci 2018 10 10;285(1888). Epub 2018 Oct 10.

Department of Life Sciences, Imperial College London, London SW7 2AZ, UK.

Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest living relatives of the first plants to colonize land 500 million years ago (MYA). Previous investigations reported near-exclusive colonization of liverworts by the most recently evolved arbuscular mycorrhizal fungi, the Glomeraceae, indicating a recent acquisition from flowering plants at odds with the widely held notion that arbuscular mycorrhizal-like associations in liverworts represent the ancestral symbiotic condition in land plants. We performed an analysis of symbiotic fungi in 674 globally collected liverworts using molecular phylogenetics and electron microscopy. Here, we show every order of arbuscular mycorrhizal fungi colonizes early-diverging liverworts, with non-Glomeraceae being at least 10 times more common than in flowering plants. Arbuscular mycorrhizal fungi in liverworts and other ancient plant lineages (hornworts, lycopods, and ferns) were delimited into 58 taxa and 36 singletons, of which at least 43 are novel and specific to liverworts. The discovery that early plant lineages are colonized by early-diverging fungi supports the hypothesis that arbuscular mycorrhizas are an ancestral symbiosis for all land plants.
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http://dx.doi.org/10.1098/rspb.2018.1600DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6191707PMC
October 2018

The Effects of Arbuscular Mycorrhizal Fungal Colonisation on Nutrient Status, Growth, Productivity, and Canker Resistance of Apple ().

Front Microbiol 2018 3;9:1461. Epub 2018 Jul 3.

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom.

We assess whether arbuscular mycorrhizal fungi (AMF) improve growth, nutritional status, phenology, flower and fruit production, and disease resistance in woody perennial crops using apple ( as a study system. In a fully factorial experiment, young trees were grown for 3 years with or without AMF ( and ), and with industrial standard fertiliser applications or restricted fertiliser (10% of standard). We use two commercial scions (Dabinett and Michelin) and rootstocks (MM111 and MM106). Industrial standard fertiliser applications reduced AMF colonisation and root biomass, potentially increasing drought sensitivity. Mycorrhizal status was influenced by above ground genotypes (scion type) but not rootstocks, indicating strong interactions between above and below ground plant tissue. The AMF inoculation significantly increased resistance to , a globally economically significant fungal pathogen of apple orchards, but did not consistently alter leaf nutrients, growth, phenology or fruit and flower production. This study significantly advances understanding of AMF benefits to woody perennial crops, especially increased disease resistance which we show is not due to improved tree nutrition or drought alleviation. Breeding programmes and standard management practises can limit the potential for these benefits.
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http://dx.doi.org/10.3389/fmicb.2018.01461DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6037770PMC
July 2018

Author Correction: Environment and host as large-scale controls of ectomycorrhizal fungi.

Nature 2018 09;561(7724):E42

Thünen Institute of Forest Ecosystems, Eberswalde, Germany.

Change history: In the HTML version of this Article, author 'Filipa Cox' had no affiliation in the author list, although she was correctly associated with affiliation 3 in the PDF. In addition, the blue circles for 'oak' were missing from Extended Data Fig. 1. These errors have been corrected online.
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http://dx.doi.org/10.1038/s41586-018-0312-yDOI Listing
September 2018

Environment and host as large-scale controls of ectomycorrhizal fungi.

Nature 2018 06 6;558(7709):243-248. Epub 2018 Jun 6.

Thünen Institute of Forest Ecosystems, Eberswalde, Germany.

Explaining the large-scale diversity of soil organisms that drive biogeochemical processes-and their responses to environmental change-is critical. However, identifying consistent drivers of belowground diversity and abundance for some soil organisms at large spatial scales remains problematic. Here we investigate a major guild, the ectomycorrhizal fungi, across European forests at a spatial scale and resolution that is-to our knowledge-unprecedented, to explore key biotic and abiotic predictors of ectomycorrhizal diversity and to identify dominant responses and thresholds for change across complex environmental gradients. We show the effect of 38 host, environment, climate and geographical variables on ectomycorrhizal diversity, and define thresholds of community change for key variables. We quantify host specificity and reveal plasticity in functional traits involved in soil foraging across gradients. We conclude that environmental and host factors explain most of the variation in ectomycorrhizal diversity, that the environmental thresholds used as major ecosystem assessment tools need adjustment and that the importance of belowground specificity and plasticity has previously been underappreciated.
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http://dx.doi.org/10.1038/s41586-018-0189-9DOI Listing
June 2018

From rhizoids to roots? Experimental evidence of mutualism between liverworts and ascomycete fungi.

Ann Bot 2018 02;121(2):221-227

Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, UK.

Background And Aims: The rhizoids of leafy liverworts (Jungermanniales, Marchantiophyta) are commonly colonized by the ascomycete fungus Pezoloma ericae. These associations are hypothesized to be functionally analogous to the ericoid mycorrhizas (ErMs) formed by P. ericae with the roots of Ericaceae plants in terms of bi-directional phosphorus for carbon exchange; however, this remains unproven. Here, we test whether associations between the leafy liverwort Cephalozia bicuspidata and P. ericae are mutualistic.

Methods: We measured movement of phosphorus and carbon between C. bicuspidata and P. ericae using [33P]orthophosphate and 14CO2 isotope tracers in monoxenic cultures. We also measured leafy liverwort growth, with and without P. ericae.

Key Results: We present the first demonstration of nutritionally mutualistic symbiosis between a non-vascular plant and an ErM-forming fungus, showing transfer of fungal-acquired P to the liverwort and of liverwort-fixed C to the fungus alongside increased growth in fungus-colonized liverworts.

Conclusions: Thus, this ascomycete-liverwort symbiosis can now be described as mycorrhiza-like, providing further insights into ericoid mycorrhizal evolution and adding Ascomycota fungi to mycorrhizal fungal groups engaging in mutualisms with plants across the land plant phylogeny. As P. ericae also colonizes the rhizoids of Schistochilaceae liverworts, which originated in the Triassic and are sister to all other jungermannialean liverworts associated with fungi, our findings point toward an early origin of ascomycete-liverwort symbioses, possibly pre-dating their evolution in the Ericales by some 150 million years.
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http://dx.doi.org/10.1093/aob/mcx126DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5808786PMC
February 2018

A mycorrhizal revolution.

Curr Opin Plant Biol 2018 08 29;44:1-6. Epub 2017 Dec 29.

Comparative Plant & Fungal Biology, Royal Botanic Gardens, Kew, Richmond TW9 3DS, UK; Department of Life Sciences, Imperial College London, London SW7 2AZ, UK.

It has long been postulated that symbiotic fungi facilitated plant migrations onto land through enhancing the scavenging of mineral nutrients and exchanging these for photosynthetically fixed organic carbon. Today, land plant-fungal symbioses are both widespread and diverse. Recent discoveries show that a variety of potential fungal associates were likely available to the earliest land plants, and that these early partnerships were probably affected by changing atmospheric CO concentrations. Here, we evaluate current hypotheses and knowledge gaps regarding early plant-fungal partnerships in the context of newly discovered fungal mutualists of early and more recently evolved land plants and the rapidly changing views on the roles of plant-fungal symbioses in the evolution and ecology of the terrestrial biosphere.
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http://dx.doi.org/10.1016/j.pbi.2017.12.004DOI Listing
August 2018

Multigene phylogeny of , an early diverging lineage of fungi associated with plants.

IMA Fungus 2017 Dec 3;8(2):245-257. Epub 2017 Oct 3.

Department of Plant Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, USA.

is a lineage of early diverging fungi within . Many species in this order produce small sporophores ("sporocarps") containing a large number of zygospores, and many species form symbioses with plants. However, due to limited collections, subtle morphological differentiation, difficulties in growing these organisms , and idiosyncrasies in their rDNA that make PCR amplification difficult, the systematics and character evolution of these fungi have been challenging to resolve. To overcome these challenges we generated a multigene phylogeny of using sporophores collected over the past three decades from four continents. Our results show that harbour significant undescribed diversity and form two deeply divergent and well-supported phylogenetic clades, which we delimit as the families and fam. nov. The family consists of the genus , and many diverse lineages known only from environmental DNA sequences of plant-endosymbiotic fungi. Within there are two clades. One corresponds to and includes the type species, . Species of are characterized by above- and below-ground sporophores, a hollow and infolded sporophore form, a loose zygosporangial hyphal mantle, homogeneous gametangia, and an enigmatic trophic mode with no evidence of ectomycorrhizal association for most species. For the other clade we introduce a new generic name, gen. nov. Members of that genus ( and species complexes, and an undescribed species) are characterized by hypogeous sporophores with a solid gleba, a well-developed zygosporangial hyphal mantle, heterogeneous gametangia, and an ectomycorrhizal trophic mode. Future studies on and will be important for understanding fungal innovations including evolution of macroscopic sporophores and symbioses with plants.
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http://dx.doi.org/10.5598/imafungus.2017.08.02.03DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5729711PMC
December 2017

The Ninth International Conference on Mycorrhiza in Prague: across mycorrhizal symbioses from molecules to global scales.

Mycorrhiza 2018 02;28(2):203-205

Plant Biology Research Institute, University of Montreal, 4101, 11 Sherbrooke Street East, Montreal, QC, H1X 2B2, Canada.

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http://dx.doi.org/10.1007/s00572-017-0804-xDOI Listing
February 2018

Ecology of Alpine Macrofungi - Combining Historical with Recent Data.

Front Microbiol 2017 26;8:2066. Epub 2017 Oct 26.

Biodiversity and Conservation Biology, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland.

Historical datasets of living communities are important because they can be used to document creeping shifts in species compositions. Such a historical data set exists for alpine fungi. From 1941 to 1953, the Swiss geologist Jules Favre visited yearly the region of the Swiss National Park and recorded the occurring fruiting bodies of fungi >1 mm (so-called "macrofungi") in the alpine zone. Favre can be regarded as one of the pioneers of alpine fungal ecology not least because he noted location, elevation, geology, and associated plants during his numerous excursions. However, some relevant information is only available in his unpublished field-book. Overall, Favre listed 204 fungal species in 26 sampling sites, with 46 species being previously unknown. The analysis of his data revealed that the macrofungi recorded belong to two major ecological groups, either they are symbiotrophs and live in ectomycorrhizal associations with alpine plant hosts, or they are saprotrophs and decompose plant litter and soil organic matter. The most frequent fungi were members of and , which form ectomycorrhizas with or the dwarf alpine species. The scope of the present study was to combine Favre's historical dataset with more recent data, either with the "SwissFungi" database or with data from major studies of the French and German Alps, and with the data from novel high-throughput DNA sequencing techniques of soils from the Swiss Alps. Results of the latter application revealed, that problems associated with these new techniques are manifold and species determination remains often unclear. At this point, the fungal taxa collected by Favre and deposited as exsiccata at the "Conservatoire et Jardin Botaniques de la Ville de Genève" could be used as a reference sequence dataset for alpine fungal studies. In conclusion, it can be postulated that new improved databases are urgently necessary for the near future, particularly, with regard to investigating fungal communities from alpine regions using new techniques.
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http://dx.doi.org/10.3389/fmicb.2017.02066DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5662630PMC
October 2017

Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island.

New Phytol 2018 02 16;217(3):1254-1266. Epub 2017 Oct 16.

Department of Life Sciences, Imperial College London, Ascot, SL5 7PY, UK.

Microbes can have profound effects on their hosts, driving natural selection, promoting speciation and determining species distributions. However, soil-dwelling microbes are rarely investigated as drivers of evolutionary change in plants. We used metabarcoding and experimental manipulation of soil microbiomes to investigate the impact of soil and root microbes in a well-known case of sympatric speciation, the Howea palms of Lord Howe Island (Australia). Whereas H. forsteriana can grow on both calcareous and volcanic soils, H. belmoreana is restricted to, but more successful on, volcanic soil, indicating a trade-off in adaptation to the two soil types. We suggest a novel explanation for this trade-off. Arbuscular mycorrhizal fungi (AMF) are significantly depleted in H. forsteriana on volcanic soil, relative to both H. belmoreana on volcanic soil and H. forsteriana on calcareous soil. This is mirrored by the results of survival experiments, where the sterilization of natural soil reduces Howea fitness in every soil-species combination except H. forsteriana on volcanic soil. Furthermore, AMF-associated genes exhibit evidence of divergent selection between Howea species. These results show a mechanism by which divergent adaptation can have knock-on effects on host-microbe interactions, thereby reducing interspecific competition and promoting the coexistence of plant sister species.
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http://dx.doi.org/10.1111/nph.14850DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5813143PMC
February 2018

Genetic diversity patterns of arbuscular mycorrhizal fungi associated with the mycoheterotroph Arachnitis uniflora Phil. (Corsiaceae).

Ann Bot 2017 06;119(8):1279-1294

Instituto Multidisciplinario de Biología Vegetal, IMBIV, UNC-CONICET, Edificio de Investigaciones Biológicas y Tecnológicas, Vélez Sársfield 1611, 5000 Córdoba, Argentina.

Background And Aims: Arachnitis uniflora is a mycoheterotrophic plant that exploits arbuscular mycorrhizal fungi of neighbouring plants. We tested A. uniflora 's specificity towards fungi across its large latitudinal range, as well as the role of historical events and current environmental, geographical and altitudinal variables on fungal genetic diversity.

Methods: Arachnitis uniflora mycorrhizas were sampled at 25 sites. Fungal phylogenetic relationships were reconstructed, genetic diversity was calculated and the main divergent lineages were dated. Phylogeographical analysis was performed with the main fungal clade. Fungal diversity correlations with environmental factors were investigated.

Key Results: Glomeraceae fungi dominated, with a main clade that likely originated in the Upper Cretaceous and diversified in the Miocene. Two other arbuscular mycorrhizal fungal families not previously known to be targeted by A. uniflora were detected rarely and appear to be facultative associations. High genetic diversity, found in Bolivia and both northern and southern Patagonia, was correlated with temperature, rainfall and soil features.

Conclusions: Fungal genetic diversity and its distribution can be explained by the ancient evolutionary history of the target fungi and by micro-scale environmental conditions with a geographical mosaic pattern.
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http://dx.doi.org/10.1093/aob/mcx023DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5604589PMC
June 2017

You are what you get from your fungi: nitrogen stable isotope patterns in Epipactis species.

Ann Bot 2017 05;119(7):1085-1095

Laboratory of Isotope Biogeochemistry, Bayreuth Center of Ecology and Environmental Research (BayCEER), University of Bayreuth, 95440 Bayreuth, Germany.

Background And Aims: Partially mycoheterotrophic plants are enriched in 13 C and 15 N compared to autotrophic plants. Here, it is hypothesized that the type of mycorrhizal fungi found in orchid roots is responsible for variation in 15 N enrichment of leaf tissue in partially mycoheterotrophic orchids.

Methods: The genus Epipactis was used as a case study and carbon and nitrogen isotope abundances of eight Epipactis species, fungal sporocarps of four Tuber species and autotrophic references were measured. Mycorrhizal fungi were identified using molecular methods. Stable isotope data of six additional Epipactis taxa and ectomycorrhizal and saprotrophic basidiomycetes were compiled from the literature.

Key Results: The 15 N enrichment of Epipactis species varied between 3·2 ± 0·8 ‰ ( E. gigantea ; rhizoctonia-associated) and 24·6 ± 1·6 ‰ ( E. neglecta ; associated with ectomycorrhizal ascomycetes). Sporocarps of ectomycorrhizal ascomycetes (10·7 ± 2·2 ‰) were significantly more enriched in 15 N than ectomycorrhizal (5·2 ± 4·0 ‰) and saprotrophic basidiomycetes (3·3 ± 2·1 ‰).

Conclusions: As hypothesized, it is suggested that the observed gradient in 15 N enrichment of Epipactis species is strongly driven by 15 N abundance of their mycorrhizal fungi; i.e. ɛ 15 N in Epipactis spp. associated with rhizoctonias < ɛ 15 N in Epipactis spp. with ectomycorrhizal basidiomycetes < ɛ 15 N in Epipactis spp. with ectomycorrhizal ascomycetes and basidiomycetes < ɛ 15 N in Epipactis spp. with ectomycorrhizal ascomycetes.
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http://dx.doi.org/10.1093/aob/mcw265DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5604585PMC
May 2017

Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants.

New Phytol 2017 Feb 14;213(3):1418-1427. Epub 2016 Oct 14.

Naturalis Biodiversity Center, postbus 9517, Leiden, 2300 RA, the Netherlands.

In general, plants and arbuscular mycorrhizal (AM) fungi exchange photosynthetically fixed carbon for soil nutrients, but occasionally nonphotosynthetic plants obtain carbon from AM fungi. The interactions of these mycoheterotrophic plants with AM fungi are suggested to be more specialized than those of green plants, although direct comparisons are lacking. We investigated the mycorrhizal interactions of both green and mycoheterotrophic plants. We used next-generation DNA sequencing to compare the AM communities from roots of five closely related mycoheterotrophic species of Thismia (Thismiaceae), roots of surrounding green plants, and soil, sampled over the entire temperate distribution of Thismia in Australia and New Zealand. We observed that the fungal communities of mycoheterotrophic and green plants are phylogenetically more similar within than between these groups of plants, suggesting a specific association pattern according to plant trophic mode. Moreover, mycoheterotrophic plants follow a more restricted association with their fungal partners in terms of phylogenetic diversity when compared with green plants, targeting more clustered lineages of fungi, independent of geographic origin. Our findings demonstrate that these mycoheterotrophic plants target more narrow lineages of fungi than green plants, despite the larger fungal pool available in the soil, and thus they are more specialized towards mycorrhizal fungi than autotrophic plants.
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http://dx.doi.org/10.1111/nph.14249DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5248637PMC
February 2017

Similar biodiversity of ectomycorrhizal fungi in set-aside plantations and ancient old-growth broadleaved forests.

Biol Conserv 2016 Feb;194:71-79

Centre for Biological Sciences, Institute for Life Sciences Building 85, University of Southampton, Southampton, SO17 1BJ, UK.

Setting aside overmature planted forests is currently seen as an option for preserving species associated with old-growth forests, such as those with dispersal limitation. Few data exist, however, on the utility of set-aside plantations for this purpose, or the value of this habitat type for biodiversity relative to old-growth semi-natural ecosystems. Here, we evaluate the contribution of forest type relative to habitat characteristics in determining species richness and composition in seven forest blocks, each containing an ancient old-growth stand (> 1000 yrs) paired with a set-aside even-aged planted stand (ca. 180 yrs). We investigated the functionally important yet relatively neglected ectomycorrhizal fungi (EMF), a group for which the importance of forest age has not been assessed in broadleaved forests. We found that forest type was not an important determinant of EMF species richness or composition, demonstrating that set-aside can be an effective option for conserving ancient EMF communities. Species richness of above-ground EMF fruiting bodies was principally related to the basal area of the stand (a correlate of canopy cover) and tree species diversity, whilst richness of below-ground ectomycorrhizae was driven only by tree diversity. Our results suggest that overmature planted forest stands, particularly those that are mixed-woods with high basal area, are an effective means to connect and expand ecological networks of ancient old-growth forests in historically deforested and fragmented landscapes for ectomycorrhizal fungi.
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http://dx.doi.org/10.1016/j.biocon.2015.12.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4730558PMC
February 2016

Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline.

ISME J 2016 06 27;10(6):1514-26. Epub 2015 Nov 27.

Department of Life Sciences, Natural History Museum, London, UK.

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.
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http://dx.doi.org/10.1038/ismej.2015.204DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5029179PMC
June 2016

Are there geographic mosaics of mycorrhizal specificity and partial mycoheterotrophy? A case study in Moneses uniflora (Ericaceae).

New Phytol 2015 Dec 23;208(4):1003-7. Epub 2015 Jul 23.

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK.

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http://dx.doi.org/10.1111/nph.13587DOI Listing
December 2015
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