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
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80 results found

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, 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

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

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

Renny M, Cristina Acosta M, Cofre N, Dominguez LS, Bidartondo MI, Sersic ANet al., 2017, Genetic diversity patterns of arbuscular mycorrhizal fungi associated with the mycoheterotroph Arachnitis uniflora Phil. (Corsiaceae), Annals of Botany, Vol: 119, Pages: 1279-1294, ISSN: 0305-7364

Background and AimsArachnitis 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.MethodsArachnitis 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.

Journal article

Schiebold JM-I, Bidartondo MI, Karasch P, Gravendeel B, Gebauer Get al., 2017, You are what you get from your fungi: nitrogen stable isotope patterns in Epipactis species, ANNALS OF BOTANY, Vol: 119, Pages: 1085-1095, ISSN: 0305-7364

Background and Aims: Partially mycoheterotrophic plants are enriched in 13C and 15N compared to autotrophic plants. Here, it is hypothesized that the type of mycorrhizal fungi found in orchid roots is responsible for variation in 15N 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 15N 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 15N than ectomycorrhizal (5·2 ± 4·0 ‰) and saprotrophic basidiomycetes (3·3 ± 2·1 ‰).Conclusions: As hypothesized, it is suggested that the observed gradient in 15N enrichment of Epipactis species is strongly driven by 15N abundance of their mycorrhizal fungi; i.e. ɛ15N in Epipactis spp. associated with rhizoctonias < ɛ15N in Epipactis spp. with ectomycorrhizal basidiomycetes < ɛ15N in Epipactis spp. with ectomycorrhizal ascomycetes and basidiomycetes < ɛ15N in Epipactis spp. with ectomycorrhizal ascomycetes.

Journal article

Rimington WR, Pressel S, Field KJ, Strullu-Derrien C, Duckett JG, Bidartondo MIet al., 2017, Reapprasing the origins of mycorrhizas, Molecular Mycorrhizal Symbiosis, Editors: Martin, Publisher: John Wiley & Sons, Pages: 21-32, ISBN: 9781118951415

Book chapter

Pressel S, Bidartondo MI, Field KJ, Rimington WR, Duckett JGet al., 2016, Pteridophyte fungal associations: Current knowledge and future perspectives, Journal of Systematics and Evolution, Vol: 54, Pages: 666-678, ISSN: 1674-4918

Current understanding of the nature and function of fungal associations in pteridophytes is surprisinglypatchy given their key evolutionary position, current research foci on other early-branching plant clades, and majorefforts at unravelling mycorrhizal evolution and the mechanisms underlying this key interaction between plants andfungi. Here we provide a critical review of current knowledge of fungal associations across pteridophytes andconsider future directions making recommendations along the way. From a comprehensive survey of the literature,a confused picture emerges: suggestions that members of the Lycopsida harbour Basidiomycota fungi contrastsharply with extensive cytological and recent molecular evidence pointing to exclusively Glomeromycota and/orMucoromycotina associations in this group. Similarly, reports of dark septate, assumingly ascomycetous, hyphae ina range of pteridophytes, advocating a mutualistic relationship, are not backed by functional evidence and thefact that the fungus invariably occupies dead host tissue points to saprotrophy and not mutualism. The bestconclusion that can be reached based on current evidence is that the fungal symbionts of pteridophytes belong tothe two fungal lineages Mucoromycotina and Glomeromycota. Do symbiotic fungi and host pteridophytes engagein mutually beneficial partnerships? To date, only two pioneering studies have addressed this key questiondemonstrating reciprocal exchange of nutrients between the sporophytes of Ophioglossum vulgatum and Osmundaregalis and their fungal symbionts. There is a pressing need for more functional investigations also extending to thegametophyte generation and coupled with in vitro isolation and resynthesis studies to unravel the effect of thefungi on their host.

Journal article

Gomes SIF, Aguirre-Gutierrez J, Bidartondo MI, Merckx VSFTet al., 2016, Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants, New Phytologist, Vol: 213, Pages: 1418-1427, ISSN: 0028-646X

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.

Journal article

Spake R, van der Linde S, Newton AC, Suz LM, Bidartondo MI, Doncaster CPet al., 2015, Similar biodiversity of ectomycorrhizal fungi in set-aside plantations and ancient old-growth broadleaved forests, Biological Conservation, Vol: 194, Pages: 71-79, ISSN: 1873-2917

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.

Journal article

Hynson NA, Bidartondo MI, Read DJ, 2015, Are there geographic mosaics of mycorrhizal specificity and partial mycoheterotrophy? A case study in Moneses uniflora (Ericaceae)., New Phytol, Vol: 208, Pages: 1003-1007

Journal article

Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel Set al., 2015, Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline, ISME Journal, Vol: 10, Pages: 1514-1526, ISSN: 1751-7362

Journal article

Kowal J, Pressel S, Duckett JG, Bidartondo MIet al., 2015, Liverworts to the rescue: an investigation of their efficacy as mycorrhizal inoculum for vascular plants, Functional Ecology, Vol: 30, Pages: 1014-1023, ISSN: 1365-2435

1. Pezoloma ericae (D.J. Read) Baral, a widespread mycorrhizal fungus of plants in the Ericales,is known to form intracellular associations with several families of leafy liverworts(Schistochilaceae, Lepidoziaceae, Cephaloziaceae, Cephaloziellaceae) in vitro. The ecologicalsignificance of this link between vascular and non-vascular plants is unknown.2. Fungal symbionts were isolated from rhizoids of the leafy liverworts Cephalozia connivens(Dicks.) Lindb. and C. bicuspidata (L.) Dum. (Cephaloziaceae), as well as from the hair rootsof two dominant ericoid mycorrhiza-forming species of European heathlands, Erica tetralix(L.) and Calluna vulgaris (L.).3. Using pure cultures of P. ericae, we resynthesized liverwort–fungus associations to use colonizedliverworts as inoculum which was applied to substrates supporting the growth of heatherseedlings and cuttings. Effects were quantified using germination, rooting, plant colonization,plant survival under waterlogging stress and growth in height in experimental systems withand without liverworts and/or fungi.4. Fungal symbionts growing from liverwort rhizoids readily colonized the hair roots of ericaceousplants to form typical ericoid mycorrhizas.5. The presence of inoculum-bearing liverworts led to significant increases in plant growth.Erica tetralix was more responsive to inoculation than C. vulgaris.6. Ericaceous cuttings rooted and survived more successfully when they were coplanted withpreviously colonized liverwort stems.7. We demonstrate, under realistic ecological circumstances, that liverworts can deliver mycorrhizalinoculum and improve the establishment of vascular plants. We propose that by providingsources of mycorrhizal inoculum, symbiotic non-vascular plants can contribute to therestoration of plant communities dominated by Ericales plants. This research leads to broaderknowledge about the function of ericoid mycorrhizas in ecosystems.

Journal article

Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MIet al., 2015, Symbiotic options for the conquest of land, Trends in Ecology & Evolution, Vol: 30, Pages: 477-486, ISSN: 0169-5347

The domination of the landmasses of Earth by plants starting during the Ordovician Period drastically altered the development of the biosphere and the composition of the atmosphere, with far-reaching consequences for all life ever since. It is widely thought that symbiotic soil fungi facilitated the colonization of the terrestrial environment by plants. However, recent discoveries in molecular ecology, physiology, cytology, and paleontology have brought into question the hitherto-assumed identity and biology of the fungi engaged in symbiosis with the earliest-diverging lineages of extant land plants. Here, we reconsider the existing paradigm and show that the symbiotic options available to the first plants emerging onto the land were more varied than previously thought.

Journal article

Yokoya K, Zettler LW, Kendon JP, Bidartondo MI, Stice AL, Skarha S, Corey LL, Knight AC, Sarasan Vet al., 2015, Preliminary findings on identification of mycorrhizal fungi from diverse orchids in the Central Highlands of Madagascar, Mycorrhiza, Vol: 25, Pages: 611-625, ISSN: 1432-1890

The Orchid flora of Madagascar is one of the most diverse with nearly 1000 orchid taxa, of which about 90 % are endemic to this biodiversity hotspot. The Itremo Massif in the Central Highlands of Madagascar with a Highland Subtropical climate range encompasses montane grassland, igneous and metamorphic rock outcrops, and gallery and tapia forests. Our study focused on identifying culturable mycorrhizae from epiphytic, lithophytic, and terrestrial orchid taxa to understand their diversity and density in a spatial matrix that is within the protected areas. We have collected both juvenile and mature roots from 41 orchid taxa for isolating their orchid mycorrhizal fungi (OMF), and to culture, identify, and store in liquid nitrogen for future studies. Twelve operational taxonomic units (OTUs), of three known orchid mycorrhizal genera, were recognized by analysis of internal transcribed spacer (ITS) sequences of 85 isolates, and, by comparing with GenBank database entries, each OTU was shown to have closely related fungi that were also found as orchid associates. Orchid and fungal diversity were greater in gallery forests and open grasslands, which is very significant for future studies and orchid conservation. As far as we know, this is the first ever report of detailed identification of mycorrhizal fungi from Madagascar. This study will help start to develop a programme for identifying fungal symbionts from this unique biodiversity hotspot, which is undergoing rapid ecosystem damage and species loss. The diversity of culturable fungal associates, their density, and distribution within the Itremo orchid hotspot areas will be discussed.

Journal article

Desiro A, Faccio A, Kaech A, Bidartondo MI, Bonfante Pet al., 2015, Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria, NEW PHYTOLOGIST, Vol: 205, Pages: 1464-1472, ISSN: 0028-646X

Journal article

Field KJ, Leake JR, Tille S, Allinson KE, Rimington WR, Bidartondo MI, Beerling DJ, Cameron DDet al., 2015, From mycoheterotrophy to mutualism: mycorrhizal specificity and functioning in Ophioglossum vulgatum sporophytes, NEW PHYTOLOGIST, Vol: 205, Pages: 1492-1502, ISSN: 0028-646X

Journal article

Rimington WR, Pressel S, Duckett JG, Bidartondo MIet al., 2015, Fungal associations of basal vascular plants: reopening a closed book?, NEW PHYTOLOGIST, Vol: 205, Pages: 1394-1398, ISSN: 0028-646X

Journal article

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