Tropical tree ectomycorrhiza are distributed independently of soil nutrients

. 2024 Mar ; 8 (3) : 400-410. [epub] 20240110

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38200369
Odkazy

PubMed 38200369
DOI 10.1038/s41559-023-02298-0
PII: 10.1038/s41559-023-02298-0
Knihovny.cz E-zdroje

Mycorrhizae, a form of plant-fungal symbioses, mediate vegetation impacts on ecosystem functioning. Climatic effects on decomposition and soil quality are suggested to drive mycorrhizal distributions, with arbuscular mycorrhizal plants prevailing in low-latitude/high-soil-quality areas and ectomycorrhizal (EcM) plants in high-latitude/low-soil-quality areas. However, these generalizations, based on coarse-resolution data, obscure finer-scale variations and result in high uncertainties in the predicted distributions of mycorrhizal types and their drivers. Using data from 31 lowland tropical forests, both at a coarse scale (mean-plot-level data) and fine scale (20 × 20 metres from a subset of 16 sites), we demonstrate that the distribution and abundance of EcM-associated trees are independent of soil quality. Resource exchange differences among mycorrhizal partners, stemming from diverse evolutionary origins of mycorrhizal fungi, may decouple soil fertility from the advantage provided by mycorrhizal associations. Additionally, distinct historical biogeographies and diversification patterns have led to differences in forest composition and nutrient-acquisition strategies across three major tropical regions. Notably, Africa and Asia's lowland tropical forests have abundant EcM trees, whereas they are relatively scarce in lowland neotropical forests. A greater understanding of the functional biology of mycorrhizal symbiosis is required, especially in the lowland tropics, to overcome biases from assuming similarity to temperate and boreal regions.

Asian School of the Environment Nanyang Technological University Singapore Singapore

Binatang Research Center Madang Papua New Guinea

Biology Centre Institute of Entomology of the Czech Academy of Sciences Ceske Budejovice Czech Republic

Center for Conservation and Sustainability Smithsonian National Zoo and Conservation Biology Institute Washington DC USA

Center for Plant Science Innovation University of Nebraska Lincoln NE USA

Coordenação de Dinâmica Ambiental Manaus Brazil

Departamento de Ciencias Forestales Universidad Nacional de Colombia Sede Medellín Medellín Colombia

Departamento de Ecologia Instituto de Biociências Universidade de São Paulo São Paulo Brazil

Department of Ecology and Evolutionary Biology University of California Los Angeles CA USA

Department of Ecology Evolution and Environmental Biology Columbia University New York NY USA

Department of Environmental Sciences University of Puerto Rico San Juan PR USA

Department of Plant Biology University of Illinois Urbana Champaign Urbana IL USA

Department of Science and Technology Uva Wellassa University Badulla Sri Lanka

Escuela de Ciencias Biológicas Pontificia Universidad Católica del Ecuador Quito Ecuador

Estación Experimental de Zonas Áridas Consejo Superior de Investigaciones Científicas Almería Spain

Faculty of Science and Technology Thammasat University Pathum Thani Thailand

Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic

Faculty of Sciences University of Kisangani Kisangani Democratic Republic of the Congo

Forest Global Earth Observatory Smithsonian Tropical Research Institute Washington DC USA

Forestry and Environment Division Forest Research Institute Malaysia Kepong Malaysia

Graduate School of Science Osaka Metropolitan University Osaka Japan

Herbario Amazónico Colombiano Instituto Amazónico de Investigaciones Científicas Sinchi Bogotá Colombia

Herbier National du Gabon Institut de Pharmacopée et de Médecine Traditionelle Libreville Gabon

Institut de Recherche en Ecologie Tropicale Centre National de la Recherche Scientifique et Technologique Libreville Gabon

Institut Facultaire des Sciences Agronomiques de Yangambi Kisangani Democratic Republic of the Congo

Institute of Molecular Biosciences Mahidol University Nakhon Pathom Thailand

Laboratoire Evolution et Diversité Biologique CNRS UPS IRD Université Paul Sabatier Toulouse France

National Biobank of Thailand National Science and Technology Development Agency Khlong Luang Thailand

Sabah Forestry Department Forest Research Centre Sandakan Malaysia

Sarawak Forestry Department Kuching Malaysia

School of Biological Sciences University of Aberdeen Aberdeen UK

School of Biological Sciences University of Nebraska Lincoln NE USA

School of Science Navajo Technical University Crownpoint NM USA

Smithsonian Tropical Research Institute Balboa Panama

Southeast Asia Rainforest Research Partnership Kota Kinabalu Malaysia

Thai Long Term Forest Ecological Research Project Department of Forest Biology Faculty of Forestry Kasetsart University Bangkok Thailand

UK Centre for Ecology and Hydrology Edinburgh UK

Zobrazit více v PubMed

Lambers, H., Mougel, C., Jaillard, B. & Hinsinger, P. Plant–microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321, 83–115 (2009).

Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic Press, 2008).

Tedersoo, L. & Bahram, M. Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biol. Rev. 94, 1857–1880 (2019). PubMed

Branco, S. et al. Mechanisms of stress tolerance and their effects on the ecology and evolution of mycorrhizal fungi. New Phytol. 235, 2158–2175 (2022). PubMed

Jiang, Y. et al. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356, 1172–1175 (2017). PubMed

Howard, N. et al. The potential role of Mucoromycotina ‘fine root endophytes’ in plant nitrogen nutrition. Physiol. Plant. 174, e13715 (2022). PubMed PMC

Hoysted, G. A. et al. Direct nitrogen, phosphorus and carbon exchanges between Mucoromycotina ‘fine root endophyte’ fungi and a flowering plant in novel monoxenic cultures. New Phytol. 238, 70–79 (2023). PubMed

Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220, 1108–1115 (2018). PubMed

Phillips, R. P., Brzostek, E. & Midgley, M. G. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol. 199, 41–51 (2013). PubMed

Wurzburger, N. et al. Mycorrhizal fungi as drivers and modulators of terrestrial ecosystem processes. New Phytol. 213, 996–999 (2017). PubMed

Soudzilovskaia, N. A. et al. Global mycorrhizal plant distribution linked to terrestrial carbon stocks. Nat. Commun. 10, 5077 (2019). PubMed PMC

Gadgil, R. L. & Gadgil, P. D. Mycorrhiza and litter decomposition. Nature 233, 133–133 (1971). PubMed

Rozmoš, M. et al. Organic nitrogen utilisation by an arbuscular mycorrhizal fungus is mediated by specific soil bacteria and a protist. ISME J. 16, 676–685 (2022). PubMed

Wang, L. et al. A core microbiome in the hyphosphere of arbuscular mycorrhizal fungi has functional significance in organic phosphorus mineralization. New Phytol. 238, 859–873 (2023). PubMed

Tedersoo, L., Bahram, M. & Zobel, M. How mycorrhizal associations drive plant population and community biology. Science 367, eaba1223 (2020). PubMed

Becquer, A. et al. in Advances in Botanical Research (ed. Cánovas, F. M.) 77–126 (Academic Press, 2019).

Averill, C. et al. Global imprint of mycorrhizal fungi on whole-plant nutrient economics. Proc. Natl Acad. Sci. USA 116, 23163–23168 (2019). PubMed PMC

Seyfried, G. S., Dalling, J. W. & Yang, W. H. Mycorrhizal type effects on leaf litter decomposition depend on litter quality and environmental context. Biogeochemistry 155, 21–38 (2021).

Steidinger, B. S. et al. Climatic controls of decomposition drive the global biogeography of forest–tree symbioses. Nature 569, 404–408 (2019). PubMed

Read, D. J. Mycorrhizas in ecosystems. Experientia 47, 376–391 (1991).

Braghiere, R. K. et al. Mycorrhizal distributions impact global patterns of carbon and nutrient cycling. Geophys. Res. Lett. 48, e2021GL094514 (2021).

Barceló, M. et al. Climate drives the spatial distribution of mycorrhizal host plants in terrestrial ecosystems. J. Ecol. 107, 2564–2573 (2019).

Lokonda, M. et al. Are soils under monodominant Gilbertiodendron dewevrei and under adjacent mixed forests similar? A case study in the Democratic Republic of Congo. J. Trop. Ecol. 34, 176–185 (2018).

Lee, H. S. et al. Floristic and structural diversity of mixed dipterocarp forest in Lambir Hills National Park, Sarawak, Malaysia. J. Trop. Sci. 14, 379–400 (2002).

Newbery, D. M. et al. Transient dominance in a central African rain forest. Ecol. Monogr. 83, 339–382 (2013).

Beard, J. S. The Mora forests of Trinidad, British West Indies. J. Ecol. 33, 173–192 (1946).

Steidinger, B. S. et al. Variability in potential to exploit different soil organic phosphorus compounds among tropical montane tree species. Funct. Ecol. 29, 121–130 (2015).

Koele, N. et al. No globally consistent effect of ectomycorrhizal status on foliar traits. New Phytol. 196, 845–852 (2012). PubMed

Godoy, R. & Marín, C. in Mycorrhizal Fungi in South America (eds Pagano, M. C. & Lugo, M. A.) 315–341 (Springer International Publishing, 2019).

Marín, C. et al. Geological history and forest mycorrhizal dominance effects on soil fungal diversity in Chilean temperate rainforests. J. Soil Sci. Plant Nutr. 23, 734–745 (2023).

Weemstra, M. et al. Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest. New Phytol. 228, 253–268 (2020). PubMed

Davies, S. J. et al. ForestGEO: understanding forest diversity and dynamics through a global observatory network. Biol. Conserv. 253, 108907 (2021).

Liu, F. & Eugenio, E. C. A review and comparison of Bayesian and likelihood-based inferences in beta regression and zero-or-one-inflated beta regression. Stat. Methods Med. Res. 27, 1024–1044 (2018). PubMed

Zuur, A. F. & Ieno, E. N. Beginner’s Guide to Spatial, Temporal and Spatial-temporal Ecological Data Analysis with R-INLA: GAM and Zero-inflated Models (Highland Statistics Limited, 2018).

Barceló, M. et al. Mycorrhizal tree impacts on topsoil biogeochemical properties in tropical forests. J. Ecol. 110, 1271–1282 (2022).

Newbery, D. M., Alexander, I. J. & Rother, J. A. Phosphorus dynamics in a lowland African rainforest: the influence of ectomycorrhizal trees. Ecol. Monogr. 67, 367–409 (1997).

Henkel, T. W. Monodominance in the ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) from Guyana. J. Trop. Ecol. 19, 417–437 (2003).

Hasselquist, N. J. et al. Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecology 97, 1012–1022 (2016). PubMed

Franklin, O. et al. Forests trapped in nitrogen limitation – an ecological market perspective on ectomycorrhizal symbiosis. New Phytol. 203, 657–666 (2014). PubMed PMC

Näsholm, T. et al. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytol. 198, 214–221 (2013). PubMed

Treseder, K. K. & Allen, M. F. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol. 155, 507–515 (2002). PubMed

Allen, M. F. Mycorrhizal Dynamics in Ecological Systems (Cambridge Univ. Press, 2022).

Martin, F., Kohler, A., Murat, C., Veneault-Fourrey, C. & Hibbett, D. S. Unearthing the roots of ectomycorrhizal symbioses. Nat. Rev. Microbiol. 14, 760–773 (2016). PubMed

Tedersoo, L. & Smith, M. E. in Biogeography of Mycorrhizal Symbiosis (ed. Tedersoo, L.) 125–142 (Springer International Publishing, 2017).

Spatafora, J. W. et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108, 1028–1046 (2016). PubMed PMC

Dickie, I. A. & Moyersoen, B. Towards a global view of ectomycorrhizal ecology. New Phytol. 180, 263–265 (2008). PubMed

Pellitier, P. T. & Zak, D. R. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. New Phytol. 217, 68–73 (2018). PubMed

Peay, K. G. et al. Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient. Ecol. Lett. 18, 807–816 (2015). PubMed

Anthony, M. A. et al. Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. ISME J. 16, 1327–1336 (2022). PubMed PMC

Plett, K. L. et al. Intra-species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus. Environ. Microbiol. 23, 2004–2020 (2021). PubMed

Corrales, A. et al. Variation in ectomycorrhizal fungal communities associated with Oreomunnea mexicana (Juglandaceae) in a Neotropical montane forest. Mycorrhiza 26, 1–17 (2015). PubMed

Tedersoo, L. in Biogeography of Mycorrhizal Symbiosis (ed. Tedersoo, L.) 469–531 (Springer International Publishing, 2017).

Corrales, A. et al. Diversity and distribution of tropical ectomycorrhizal fungi. Mycologia 114, 919–933 (2022). PubMed

Pena, R. & Polle, A. Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress. ISME J. 8, 321–330 (2014). PubMed

Hazard, C. et al. Contrasting effects of intra- and interspecific identity and richness of ectomycorrhizal fungi on host plants, nutrient retention and multifunctionality. New Phytol. 213, 852–863 (2017). PubMed

Hortal, S. et al. Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi. ISME J. 11, 2666–2676 (2017). PubMed PMC

Corrales, A., Henkel, T. W. & Smith, M. E. Ectomycorrhizal associations in the tropics—biogeography, diversity patterns and ecosystem roles. New Phytol. 220, 1076–1091 (2018). PubMed

Nouhra, E. R. et al. in Mycorrhizal Fungi in South America (eds Pagano, M. C. & Lugo, M. A.) 73–95 (Springer International Publishing, 2019).

Cazzolla Gatti, R. et al. The number of tree species on Earth. Proc. Natl Acad. Sci. USA 119, e2115329119 (2022). PubMed PMC

Karst, J., Jones, M. D. & Hoeksema, J. D. Positive citation bias and overinterpreted results lead to misinformation on common mycorrhizal networks in forests. Nat. Ecol. Evol. 7, 501–511 (2023). PubMed

Soudzilovskaia, N. A. et al. FungalRoot: global online database of plant mycorrhizal associations. New Phytol. 227, 955–966 (2020). PubMed

Brundrett, M. & Tedersoo, L. Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. New Phytol. 221, 18–24 (2019). PubMed

Bueno, G. et al. Conceptual differences lead to divergent trait estimates in empirical and taxonomic approaches to plant mycorrhizal trait assignment. Mycorrhiza 29, 1–11 (2019).

Bueno, C. G. et al. Misdiagnosis and uncritical use of plant mycorrhizal data are not the only elephants in the room: a response to Brundrett & Tedersoo (2019) ‘Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions’. New Phytol. 224, 1415–1418 (2019). PubMed

Tedersoo, L. et al. Global database of plants with root-symbiotic nitrogen fixation: NodDB. J. Veg. Sci. 29, 560–568 (2018).

John, R. et al. Soil nutrients influence spatial distributions of tropical tree species. Proc. Natl Acad. Sci. USA 104, 864–869 (2007). PubMed PMC

Hendershot, W. H., Lalande, H. & Duquette, M. in Soil Sampling and Methods of Analysis (eds Carter, M. R. & Gregorich, E. G.) 197–206 (CRC Press, 2008).

Mehlich, A. Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun. Soil Sci. Plant Anal. 15, 1409–1416 (1984).

Bray, R. H. & Kurtz, L. T. Determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 59, 39–46 (1945).

Wolf, J. A. et al. Geospatial observations on tropical forest surface soil chemistry. Ecology 96, 2313–2313 (2015).

Fukuda, M. et al. Evaluation of the Mehlich 3 reagent as an extractant for cations and available phosphorus for soils in Mozambique. Commun. Soil Sci. Plant Anal. 48, 1462–1472 (2017).

Bibiso, M. et al. Evaluation of universal extractants for determination of selected micronutrients from soil. Bull. Chem. Soc. Ethiop. 29, 199–213 (2015).

Tran, T. S. et al. Evaluation of Mehlich‐III extractant to estimate the available P in Quebec soils. Commun. Soil Sci. Plant Anal. 21, 1–28 (1990).

Josse, J. & Husson, F. Handling missing values in exploratory multivariate data analysis methods. J. Soci.été Fr. Stat. 153, 79–99 (2012).

Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).

Ribeiro, P. J. Jr et al. geoR: analysis of geostatistical data. R. package version 1, 8–1 (2020).

Ferrari, S. & Cribari-Neto, F. Beta regression for modelling rates and proportions. J. Appl. Stat. 31, 799–815 (2004).

Blangiardo, M. et al. Spatial and spatio-temporal models with R-INLA. Spat. Spatiotemporal Epidemiol. 4, 33–49 (2013). PubMed

Valencia, R. et al. Tree species distributions and local habitat variation in the Amazon: large forest plot in eastern Ecuador. J. Ecol. 92, 214–229 (2004).

Lepore, M. et al. Fgeo: analyze forest diversity and dynamics. R package version 1.1.4 (2019).

Peña-Claros, M. Changes in forest structure and species composition during secondary forest succession in the Bolivian Amazon. Biotropica 35, 450–461 (2003).

Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).

Riebler, A. et al. An intuitive Bayesian spatial model for disease mapping that accounts for scaling. Stat. Methods Med. Res. 25, 1145–1165 (2016). PubMed

Gómez-Rubio, V. Bayesian Inference with INLA (CRC Press, 2020).

R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2023).

Carpenter, B. et al. Stan: a probabilistic programming language. J. Stat. Softw. 76, jss.v076.i01 (2017).

Gabry, J. & Češnovar, R. Cmdstanr: R interface to ‘CmdStan’. R package version 0.4.0 (2021).

Bürkner, P.-C. Brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, jss.v080.i01 (2017).

Bürkner, P.-C. Advanced Bayesian multilevel modeling with the R package brms. R. J. 10, 395–411 (2018).

Gelman, A. et al. Bayesian Data Analysis (CRC press, 2013).

Rue, H., Martino, S. & Chopin, N. Approximate Bayesian inference for latent gaussian models using integrated nested laplace approximations (with discussion). J. R. Stat. Soc. B 71, 319–392 (2009).

Gabry, J. et al. Visualization in Bayesian workflow. J. R. Stat. Soc. A 182, 389–402 (2019).

Medina-Vega, J. A. et al. Dataset and code accompanying the study by Medina-Vega et al. in Nature Ecology & Evolution: tropical tree ectomycorrhiza are distributed independently of soil nutrients. Zenodo https://doi.org/10.5281/zenodo.10044772 (2023).

Quesada, C. A. et al. Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7, 1515–1541 (2010).

Chave, J. et al. Above-ground biomass and productivity in a rain forest of eastern South. Am. J. Trop. Ecol. 24, 355–366 (2008).

Fanin, N. et al. Does variability in litter quality determine soil microbial respiration in an Amazonian rainforest? Soil Biol. Biochem. 43, 1014–1022 (2011).

Libalah, M. B. et al. Shift in functional traits along soil fertility gradient reflects non-random community assembly in a tropical African rainforest. Plant Ecol. Evol. 150, 265–278 (2017).

Nkongolo, N. V., Mbuyi, J. J. K. & Lokonda, M. W. Quantification of soil carbon in Ituri forest, Democratic Republic of Congo. In Proc. Global Symposium on Soil Organic Carbon 151–153 (Food and Agriculture Organization of the United Nations, 2017).

Baillie, I. C. et al. Stoichiometry of cationic nutrients in Phaeozems derived from skarn and acrisols from other parent materials in lowland forests of Thailand. Geoderma Reg. 12, 1–9 (2018).

Sukri, R. et al. Habitat associations and community structure of dipterocarps in response to environment and soil conditions in Brunei Darussalam, Northwest Borneo. Biotropica 44, 595–605 (2012).

Ross, S. M. & Dykes, A. in Tropical Rainforest Research—Current Issues: Conf. Proc (eds Edwards, D. S. et al.) 259–270 (Springer Netherlands, 1996).

Dent, D. H. et al. Nutrient fluxes via litterfall and leaf litter decomposition vary across a gradient of soil nutrient supply in a lowland tropical rain forest. Plant Soil 288, 197–215 (2006).

Anderson-Teixeira, K. J. et al. CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob. Change Biol. 21, 528–549 (2015).

Moraga, P. Geospatial Health Data: Modeling and Visualization with R-INLA and Shiny (CRC Press, 2019).

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Mycorrhizal symbioses and tree diversity in global forest communities

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