Imperial College London

ProfessorMartinBidartondo

Faculty of Natural SciencesDepartment of Life Sciences (Silwood Park)

Professor of Molecular Ecology
 
 
 
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Contact

 

+44 (0)20 8332 5382m.bidartondo Website

 
 
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Location

 

Jodrell GateRoyal Botanic GardensRoyal Botanic Gardens

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Summary

 

Publications

Publication Type
Year
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94 results found

Sinanaj B, Hoysted GA, Pressel S, Bidartondo MI, Field KJet al., 2021, Critical research challenges facing Mucoromycotina 'fine root endophytes'., New Phytologist, ISSN: 0028-646X

Mucoromycotina 'Fine Root Endophytes' (MFRE), referred to previously as Glomus tenue (Greenall) or more recently Planticonsortium tenue (Walker et al., 2018), are a globally distributed group of soil fungi (Orchard et al., 2017a) that form endosymbioses with plants from across most of the land plant phylogeny (Rimington et al., 2019; Hoysted et al., 2018; 2019). Despite much progress having been made in characterising plant-MFRE symbioses in the last decade, significant challenges remain.

Journal article

Suz LM, Bidartondo MI, van der Linde S, Kuyper TWet al., 2021, Ectomycorrhizas and tipping points in forest ecosystems, NEW PHYTOLOGIST, ISSN: 0028-646X

Journal article

PRESSEL S, BIDARTONDO MI, FIELD KJ, DUCKETT JGet al., 2021, Advances in understanding of mycorrhizal-like associations in bryophytes, Bryophyte Diversity and Evolution, Vol: 43, ISSN: 2381-9677

<jats:p>Mutually beneficial associations between plants and soil fungi, mycorrhizas, are one of the most important terrestrial symbioses. These partnerships are thought to have propelled plant terrestrialisation some 500 million years ago and today they play major roles in ecosystem functioning. It has long been known that bryophytes harbour, in their living tissues, fungal symbionts, recently identified as belonging to the three mycorrhizal fungal lineages Glomeromycotina, Ascomycota and Basidiomycota. Latest advances in understanding of fungal associations in bryophytes have been largely driven by the discovery, nearly a decade ago, that early divergent liverwort clades, including the most basal Haplomitriopsida, and some hornworts, engage with a wider repertoire of fungal symbionts than previously thought, including endogonaceous members of the ancient sub-phylum Mucoromycotina. Subsequent global molecular and cytological studies have revealed that Mucoromycotina symbionts, alongside Glomeromycotina, are widespread in both complex and simple thalloid liverworts and throughout hornworts, with physiological studies confirming that, in liverworts at least, these associations are mycorrhizal-like, and highlighting important functional differences between Mucoromycotina and Glomeromycotina symbioses. Whether a more prominent role of Mucoromycotina symbionts in plant nitrogen nutrition, as identified in liverworts, extends to other plant lineages, including the flowering plants, is a major topic for future research.&#x0D;         The latest finding that ascomycete symbionts of leafy liverworts are not restricted to one fungus, Rhizoscyphus ericae, but include species in the genus Meliniomyces, as shown here in Mylia anomala, together with the recent demonstration that R. ericae forms nutritional mutualisms with the rhizoids of Cephalozia bicuspidata, fill other major gaps in our growing knowledge of fungal associations

Journal article

Hoysted GA, Kowal J, Pressel S, Duckett JG, Bidartondo MI, Field KJet al., 2021, Carbon for nutrient exchange between Lycopodiella inundata and Mucoromycotina fine root endophytes is unresponsive to high atmospheric CO2, Mycorrhiza, Vol: 31, Pages: 431-440, ISSN: 0940-6360

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 [CO2] (a[CO2]) than ambient; however, nothing is known about how changes in a[CO2] 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 33P-orthophosphate, 15 N-ammonium chloride and 14CO2 isotope tracers under ambient and elevated a[CO2] concentrations of 440 and 800 ppm, respectively. Transfers of 33P and 15 N from MFRE to plants were unaffected by changes in a[CO2]. There was a slight increase in C transfer from plants to MFRE under elevated a[CO2]. Our results demonstrate that the exchange of C-for-nutrients between a vascular plant and Mucoromycotina FRE is largely unaffected by changes in a[CO2]. 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.

Journal article

Arribas P, Andujar C, Bidartondo MI, Bohmann K, Coissac E, Creer S, deWaard JR, Elbrecht V, Ficetola GF, Goberna M, Kennedy S, Krehenwinkel H, Leese F, Novotny V, Ronquist F, Yu DW, Zinger L, Creedy TJ, Meramveliotakis E, Noguerales V, Overcast I, Morlon H, Vogler AP, Papadopoulou A, Emerson BCet al., 2021, Connecting high-throughput biodiversity inventories: Opportunities for a site-based genomic framework for global integration and synthesis, Molecular Ecology, Vol: 30, Pages: 1120-1135, ISSN: 0962-1083

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.

Journal article

Arraiano-Castilho R, Bidartondo M, Niskanen T, Clarkson JJ, Brunner I, Zimmermann S, Senn-Irlet B, Frey B, Peintner U, Mrak T, Suz LMet al., 2020, Habitat specialisation controls ectomycorrhizal fungi above the treeline in the European Alps, NEW PHYTOLOGIST, Vol: 229, Pages: 2901-2916, ISSN: 0028-646X

Journal article

Hoysted GA, Bidartondo MI, Duckett JG, Pressel S, Field KJet al., 2020, Phenology and function in lycopod-Mucoromycotina symbiosis, NEW PHYTOLOGIST, Vol: 229, Pages: 2389-2394, ISSN: 0028-646X

Journal article

Stevenson PC, Bidartondo M, Blackhall-Miles R, Cavagnaro TR, Cooper A, Geslin B, Koch H, Lee MA, Moat J, O'Hanlon R, Sjoman H, Sofo A, Stara K, Suz LMet al., 2020, The state of the world's urban ecosystems: What can we learn from trees, fungi, and bees?, PLANTS PEOPLE PLANET, Vol: 2, Pages: 482-498

Journal article

Kowal J, Arrigoni E, Serra J, Bidartondo Met al., 2020, Prevalence and phenology of fine root endophyte colonization across populations ofLycopodiella inundata, MYCORRHIZA, Vol: 30, Pages: 577-587, ISSN: 0940-6360

Journal article

Kendon JP, Yokoya K, Zettler LW, Jacob AS, McDiarmid F, Bidartondo MI, Sarasan Vet al., 2020, Recovery of mycorrhizal fungi from wild collected protocorms of Madagascan endemic orchidAerangis ellisii(BS Williams) Schltr. and their use in seed germination in vitro, MYCORRHIZA, Vol: 30, Pages: 567-576, ISSN: 0940-6360

Journal article

Arraiano-Castilho R, Bidartondo M, Niskanen T, Zimmermann S, Frey B, Brunner I, Senn-Irlet B, Hoerandl E, Gramlich S, Suz LMet al., 2020, Plant-fungal interactions in hybrid zones: Ectomycorrhizal communities of willows (Salix) in an alpine glacier forefield, Fungal Ecology, Vol: 45, Pages: 1-13, ISSN: 1754-5048

Ectomycorrhizal (EcM) fungi are essential for the establishment of woody perennial plants in the European Alps. From continental to local scales, environmental conditions and plant host characteristics can predict EcM community structure and composition. However, it is unclear whether EcM communities of congeneric host species and their hybrids are differentially structured at local scales. We aimed to i) characterize EcM communities of Salix helvetica, Salix purpurea and their hybrids and ii) elucidate the abiotic and biotic factors affecting EcM communities in hybrid zones. We analysed the EcM communities associated with willows in a glacier valley by combining molecular identification of fungi from individual ectomycorrhizas and from soil. We detected diverse EcM fungi forming non-modular and unnested networks, but we did not find significant differences in the overall EcM fungal community richness or composition among parental species and hybrids. Nevertheless, individual fungi differed regarding host preference. Our results demonstrate that in a sub-alpine hybrid zone with heterogeneous geomorphology, host genotype was not a strong predictor of overall EcM fungal community, but it influenced the occurrence of particular fungi.

Journal article

Rimington WR, Duckett JG, Field KJ, Bidartondo MI, Pressel Set al., 2020, The distribution and evolution of fungal symbioses in ancient lineages of land plants., Mycorrhiza, Vol: 30, Pages: 23-49, ISSN: 0940-6360

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.

Journal article

Rimington WR, Pressel S, Duckett JG, Field KJ, Bidartondo Met al., 2019, Evolution and networks in ancient and widespread symbioses between Mucoromycotina and liverworts, Mycorrhiza, Vol: 29, Pages: 551-565, ISSN: 0940-6360

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.

Journal article

Hoysted GA, Jacob AS, Kowal J, Giesemann P, Bidartondo M, Duckett JG, Gebauer G, Rimington WR, Schornack S, Pressel S, Field KJet al., 2019, Mucoromycotina fine root endophyte fungi form nutritional mutualisms with vascular plants, Plant Physiology, Vol: 181, Pages: 565-577, ISSN: 0032-0889

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 (Lycopodiella inundata) 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.

Journal article

Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel Set al., 2019, Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts., New Phytologist, Vol: 223, Pages: 908-921, ISSN: 0028-646X

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 endophyte Mucoromycotina fungi, both of which co-evolved 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 both fungal lineages in symbioses across the evolution of land plants.

Journal article

Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EAet al., 2019, Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review, Environmental Pollution, Vol: 246, Pages: 148-162, ISSN: 0269-7491

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−1 yr−1 for the former and 10–20 kg ha−1 yr−1 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

Journal article

Schweiger JM-I, Kemnade C, Bidartondo MI, Gebauer Get al., 2019, Light limitation and partial mycoheterotrophy in rhizoctonia-associated orchids, Oecologia, Vol: 189, Pages: 375-383, ISSN: 0029-8549

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 (δ13C, δ15N, δ2H, δ18O) and C and N concentrations. We found significant 13C enrichment in both orchids relative to autotrophic references at the forest but not the grassland, and significant 2H enrichment at both sites. The 13C 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.

Journal article

Bidartondo MI, Rimington W, Pressel S, Duckett J, Field KJ, Read DJet al., 2018, Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi, Proceedings of the Royal Society of London. Series B, Containing papers of a Biological character. Royal Society (Great Britain), Vol: 285, ISSN: 0950-1193

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.

Journal article

Berdeni D, Cotton TEA, Daniell TJ, Bidartondo M, Cameron DD, Evans KLet al., 2018, The effects of arbuscular mycorrhizal fungal colonisation on nutrient status, growth, productivity, and canker resistance of apple (Malus pumila), Frontiers in Microbiology, Vol: 9, ISSN: 1664-302X

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 (Malus pumila) as a study system. In a fully factorial experiment, young trees were grown for 3 years with or without AMF (Funneliformis mosseae and Rhizophagus irregularis), 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 Neonectria ditissima, 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.

Journal article

van der Linde S, Suz LM, Orme CDL, Cox F, Andreae H, Asi E, Atkinson B, Benham S, Carroll C, Cools N, De Vos B, Dietrich H-P, Eichhorn J, Gehrmann J, Grebenc T, Gweon HS, Hansen K, Jacob F, Kristöfel F, Lech P, Manninger M, Martin J, Meesenburg H, Merilä P, Nicolas M, Pavlenda P, Rautio P, Schaub M, Schröck H-W, Seidling W, Šrámek V, Thimonier A, Thomsen IM, Titeux H, Vanguelova E, Verstraeten A, Vesterdal L, Waldner P, Wijk S, Zhang Y, Žlindra D, Bidartondo MIet al., 2018, Environment and host as large-scale controls of ectomycorrhizal fungi, Nature, Vol: 558, Pages: 243-248, ISSN: 0028-0836

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.

Journal article

Schweiger JM-I, Bidartondo MI, Gebauer G, 2018, Stable isotope signatures of underground seedlings reveal the organic matter gained by adult orchids from mycorrhizal fungi, Functional Ecology, Vol: 32, Pages: 870-881, ISSN: 0269-8463

Orchids produce dust seeds dependent on the provision of organic carbon by mycorrhizal fungi for their early development stages. Hence, all chlorophyllous orchids experience a dramatic switch in trophic strategies from initial mycoheterotrophy to either autotrophy or partial mycoheterotrophy during ontogeny. Yet, the degree to which partially mycoheterotrophic orchids gain carbon from their mycorrhizal fungi is unclear based on existing approaches. Here, we propose a novel approach to quantify the fungal‐derived organic matter gain of chlorophyllous mature orchids mycorrhizal with rhizoctonia fungi, using the stable isotope signatures of their fully mycoheterotrophic (FMH) seedlings in a linear two‐source mixing model. We conducted a field germination experiment with seven orchid species and measured carbon, nitrogen and hydrogen stable isotope natural abundances and nitrogen concentrations of mature orchids, underground seedlings, and autotrophic references. After in situ burial for 19–30 months, germination rates varied considerably among five orchid species and failed for two. On average, underground seedlings were enriched in 13C and 15N relative to mature orchids and had higher nitrogen concentrations. Using the mean enrichment factors ε13C and ε2H of seedlings as FMH endpoint, the organic matter gain derived by mature orchids from mycorrhizas was c. 20%. Chlorophyllous orchids mycorrhizal with rhizoctonias are predisposed to partially mycoheterotrophic nutrition due to their initially mycoheterotrophic seedling stage. We show that the carbon and hydrogen isotope abundances of underground seedlings can be used in an improved mixing‐model to identify a significant proportion of fungal‐derived organic matter in mature orchids.

Journal article

Kowal J, Pressel S, Duckett JG, Bidartondo MI, Field KJet al., 2018, From rhizoids to roots? Experimental evidence of mutualism between liverworts and ascomycete fungi., Annals of Botany, Vol: 121, Pages: 221-227, ISSN: 0305-7364

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.

Journal article

Hoysted GA, Kowal J, Jacob A, Rimington WR, Duckett JG, Pressel S, Orchard S, Ryan MH, Field KJ, Bidartondo MIet al., 2017, A mycorrhizal revolution., Current Opinion in Plant Biology, Vol: 44, Pages: 1-6, ISSN: 1369-5266

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 CO2 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.

Journal article

Desirò A, Rimington WR, Jacob A, Pol NV, Smith ME, Trappe JM, Bidartondo MI, Bonito Get al., 2017, Multigene phylogeny of Endogonales, an early diverging lineage of fungi associated with plants., IMA Fungus, Vol: 8, Pages: 245-257, ISSN: 2210-6340

Endogonales is a lineage of early diverging fungi within Mucoromycota. 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 in vitro, 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 Endogonales using sporophores collected over the past three decades from four continents. Our results show that Endogonales harbour significant undescribed diversity and form two deeply divergent and well-supported phylogenetic clades, which we delimit as the families Endogonaceae and Densosporaceae fam. nov. The family Densosporaceae consists of the genus Densospora,Sphaerocreas pubescens, and many diverse lineages known only from environmental DNA sequences of plant-endosymbiotic fungi. Within Endogonaceae there are two clades. One corresponds to Endogone and includes the type species, E. pisiformis. Species of Endogone 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, Jimgerdemannia gen. nov. Members of that genus (J. flammicorona and J. lactiflua 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 Densosporaceae and Endogonaceae will be important for understanding fungal innovations including evolution of macroscopic sporophores and symbioses with pl

Journal article

Bidartondo MI, Hijri M, 2017, The Ninth International Conference on Mycorrhiza in Prague: across mycorrhizal symbioses from molecules to global scales., Mycorrhiza, Vol: 28, Pages: 203-205, ISSN: 0940-6360

Journal article

Brunner I, Frey B, Hartmann M, Zimmermann S, Graf F, Suz LM, Niskanen T, Bidartondo MI, Senn-Irlet Bet al., 2017, Ecology of Alpine Macrofungi - Combining Historical with Recent Data, Frontiers in Microbiology, Vol: 8, ISSN: 1664-302X

Historical datasets of living communities are important because they can be used todocument creeping shifts in species compositions. Such a historical data set exists foralpine fungi. From 1941 to 1953, the Swiss geologist Jules Favre visited yearly the regionof 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 pioneersof alpine fungal ecology not least because he noted location, elevation, geology, andassociated plants during his numerous excursions. However, some relevant informationis only available in his unpublished field-book. Overall, Favre listed 204 fungal species in26 sampling sites, with 46 species being previously unknown. The analysis of his datarevealed that the macrofungi recorded belong to two major ecological groups, either theyare symbiotrophs and live in ectomycorrhizal associations with alpine plant hosts, or theyare saprotrophs and decompose plant litter and soil organic matter. The most frequentfungi were members of Inocybe and Cortinarius, which form ectomycorrhizas with Dryasoctopetala or the dwarf alpine Salix species. The scope of the present study was tocombine 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 thedata from novel high-throughput DNA sequencing techniques of soils from the SwissAlps. Results of the latter application revealed, that problems associated with these newtechniques are manifold and species determination remains often unclear. At this point,the fungal taxa collected by Favre and deposited as exsiccata at the “Conservatoire etJardin Botaniques de la Ville de Genève” could be used as a reference sequence datasetfor alpine fungal studies. In conclusion, it can be postulated that new improved databasesare urgently necessary for the near future, partic

Journal article

Suz LM, Kallow S, Reed K, Bidartondo MI, Barsoum Net al., 2017, Pine mycorrhizal communities in pure and mixed pine-oak forests: Abiotic environment trumps neighboring oak host effects, Forest Ecology and Management, Vol: 406, Pages: 370-380, ISSN: 0378-1127

Scots pine (Pinus sylvestris) is frequently planted as a monoculture, but it is also grown in mixed plantations with other native trees such as pedunculate oak (Quercus robur). Both pine and oak form ectomycorrhizas that cover their roots and extend into the soil, facilitating tree water and nutrient uptake in exchange for photosynthetic carbon. Forming the interface between the soil and tree roots, mycorrhizal fungi are key drivers of biogeochemical cycling in terrestrial ecosystems and play an important role in the successful establishment of tree seedlings. They can, however, be susceptible to changes in the soil environment and in their hosts. Both environment and neighboring hosts affect how fungi colonize roots and may affect their host preference. Despite the importance of mycorrhizal fungi in forest ecosystems, little is known about the biodiversity and functional effects of mycorrhizal communities in mixed compared with monoculture plantations. Changes in mycorrhizal richness and composition can result in changes in functional groups with consequences for forest ecosystem stability and functioning. We compared pine mycorrhizas in eight mixed plantations of pine and oak and eight pine monocultures in two forests in England, and we investigated the main factors driving their taxonomic and functional composition. Geographical location and litter pH explained over 50% of the variation in pine mycorrhizal communities. Different environmental factors affected taxonomic and functional composition across stands, indicating functional redundancy. Pine tended to associate with more fungi in the presence of oak, but the abiotic environment exerted a stronger influence than oak presence on pine mycorrhizal diversity.

Journal article

Osborne OG, De-Kayne R, Bidartondo MI, Hutton I, Baker WJ, Turnbull CGN, Savolainen Vet al., 2017, Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island, New Phytologist, Vol: 217, Pages: 1254-1266, ISSN: 0028-646X

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.

Journal article

Schiebold JM-I, Bidartondo MI, Lenhard F, Makiola A, Gebauer Get al., 2017, Exploiting mycorrhizas in broad daylight: Partial mycoheterotrophy is a common nutritional strategy in meadow orchids, Journal of Ecology, Vol: 106, Pages: 168-178, ISSN: 0022-0477

Partial mycoheterotrophy (PMH) is a nutritional mode in which plants utilize organic matter, i.e. carbon, both from photosynthesis and a fungal source. The latter reverses the direction of plant-to-fungus carbon flow as usually assumed in mycorrhizal mutualisms. Based on significant enrichment in the heavy isotope 13C, a growing number of PMH orchid species have been identified. These PMH orchids are mostly associated with fungi simultaneously forming ectomycorrhizas with forest trees. In contrast, the much more common orchids that associate with rhizoctonia fungi, which are decomposers, have stable isotope profiles most often characterized by high 15N enrichment and high nitrogen concentrations but either an insignificant 13C enrichment or depletion relative to autotrophic plants. Using hydrogen stable isotope abundances recent investigations showed PMH in rhizoctonia-associated orchids growing under light-limited conditions. Hydrogen isotope abundances can be used as substitute for carbon isotope abundances in cases where autotrophic and heterotrophic carbon sources are insufficiently distinctive to indicate PMH.To determine whether rhizoctonia-associated orchids growing in habitats with high irradiance feature PMH as a nutritional mode, we sampled 13 orchid species growing in montane meadows, four forest orchid species and 34 autotrophic reference species. We analysed δ2H, δ13C, δ15N and δ18O and determined nitrogen concentrations. Orchid mycorrhizal fungi were identified by DNA sequencing.As expected, we found high enrichments in 2H, 13C, 15N and nitrogen concentrations in the ectomycorrhiza-associated forest orchids, and the rhizoctonia-associated Neottia cordata from a forest site was identified as PMH. Most orchids inhabiting sunny meadows lacked 13C enrichment or were even significantly depleted in 13C relative to autotrophic references. However, we infer PMH for the majority of these meadow orchids due to both significant 2H and 15N

Journal article

Merckx VSFT, Gomes SIF, Wapstra M, Hunt C, Steenbeecke G, Mennes CB, Walsh N, Smissen R, Hsieh TH, Smets EF, Bidartondo MIet al., 2017, The biogeographical history of the interaction between mycoheterotrophic Thismia (Thismiaceae) plants and mycorrhizal Rhizophagus (Glomeraceae) fungi, Journal of Biogeography, Vol: 44, Pages: 1869-1879, ISSN: 1365-2699

AimAchlorophyllous mycoheterotrophic plants and mycorrhizal fungi often have highly specific interactions that potentially limit the plants’ distribution and diversification potential. However, specificity in biotic interactions may differ considerably over a species’ distribution range and therefore interactions need to be studied over their entire range to assess their evolution in space and time. The present study investigates the biogeographical history of the interaction between five closely related mycoheterotrophic Thismia species and arbuscular mycorrhizal fungi over the distribution range of the plant species.LocationTemperate south-east Australia and New Zealand.MethodsPhylogenetic relationships of Thismia (nrITS and mtcob) and their arbuscular mycorrhizal fungi (partial nrSSU) were reconstructed based on data from 65 plant specimens. The diversification times in Thismia were estimated with a Bayesian relaxed clock approach using a Dioscoreales framework (nrSSU, mtatp1, mtmatR, mtnad1 b-c). Ancestral geographical ranges were reconstructed using a maximum likelihood approach. The same approach was used to reconstruct ancestral mycorrhizal associations.ResultsOur analysis shows that Thismia plants have highly specific, phylogenetically conserved and evolutionarily persistent interactions with Rhizophagus fungi. Nevertheless, Thismia was able to diversify and radiate recently due to the wide geographical distribution of the host fungi. In addition, we find that although the mycorrhizal interactions of this clade of mycoheterotrophs are strictly bound to a fungal lineage, host switches remain possible.Main conclusionsIn this clade of closely related mycoheterotrophs, dependency on highly specific fungal interactions is the result of phylogenetic niche conservatism, acting over at least 12 million years. Nevertheless, plants that are dependent on highly specific fungal interactions have ample opportunities to disperse and radiate over the geographic

Journal article

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