Arbuscular mycorrhiza (AM) and ectomycorrhiza (EcM) are the most abundant and widespread types of mycorrhizal symbiosis, but there is little and sometimes conflicting information regarding the interaction between AM fungi (AMF) and EcM fungi (EcMF) in soils. Their competition for resources can be particularly relevant in successional ecosystems, which usually present a transition from AM-forming herbaceous vegetation to EcM-forming woody species. The aims of this study were to describe the interaction between mycorrhizal fungal communities associated with AM and EcM hosts naturally coexisting during primary succession on spoil banks and to evaluate how this interaction affects growth and mycorrhizal colonization of seedlings of both species. We conducted a greenhouse microcosm experiment with Betula pendula and Hieracium caespitosum as EcM and AM hosts, respectively. They were cultivated in three-compartment rhizoboxes. Two lateral compartments contained different combinations of both host plants as sources of fungal mycelia colonizing the middle compartment, where fungal biomass, diversity, and community composition as well as the growth of each host plant species' seedlings were analyzed. The study's main finding was an asymmetric outcome of the interaction between the two plant species: while H. caespitosum and associated AMF reduced the abundance of EcMF in soil, modified the composition of EcMF communities, and also tended to decrease growth and mycorrhizal colonization of B. pendula seedlings, the EcM host did not have such effects on AM plants and associated AMF. In the context of primary succession, these findings suggest that ruderal AM hosts could hinder the development of EcM tree seedlings, thus slowing the transition from AM-dominated to EcM-dominated vegetation in early successional stages.

Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires Argentina

Department of Experimental Plant Biology Faculty of Science Charles University Prague Czechia

Department of Mycorrhizal Symbioses Institute of Botany Czech Academy of Sciences Průhonice Czechia

Faculty of Science Institute for Environmental Studies Charles University Prague Czechia

Institute of Microbiology Czech Academy of Sciences Prague Czechia

Laboratorio de Microbiología Aplicada y Biotecnología Centro Regional Universitario Bariloche Universidad Nacional del Comahue IPATEC Bariloche Argentina

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Allen M. F., Crisafulli C. M., Morris S. J., Egerton-Warburton L. M., MacMahon J. A., Trappe J. M. (2005). “Mycorrhizae and Mount St. Helens: story of a symbiosis,” in Ecological Responses to the 1980 Eruption of Mt. St. Helens. eds. Dale V. H., Swanson C. M., Crisafulli C. M. (New York, NY: Springer-Verlag; ), 221–232.

Bååth E. (2003). The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microb. Ecol. 45, 373–383. doi: 10.1007/s00248-003-2002-y, PMID: PubMed DOI

Becklin K. M., Galen C. (2009). Intra- and interspecific variation in mycorrhizal associations across a heterogeneous habitat gradient in alpine plant communities. Arct. Antarct. Alp. Res. 41, 183–190. doi: 10.1657/1938-4246-41.2.183 DOI

Becklin K. M., Pallo M. L., Galen C. (2012). Willows indirectly reduce arbuscular mycorrhizal fungal colonization in understorey communities. J. Ecol. 100, 343–351. doi: 10.1111/j.1365-2745.2011.01903.x DOI

Bengtsson-Palme J., Veldre V., Ryberg M., Hartmann M., Branco S., Wang Z., et al. . (2013). ITSx: improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for use in environmental sequencing. Methods Ecol. Evol. 4, 914–919. doi: 10.1111/2041-210X.12073 DOI

Bödeker I. T., Lindahl B. D., Olson Å., Clemmensen K. E., Treseder K. (2016). Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct. Ecol. 30, 1967–1978. doi: 10.1111/1365-2435.12677 DOI

Brundrett M. C., Tedersoo L. (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220, 1108–1115. doi: 10.1111/nph.14976, PMID: PubMed DOI

Casanova-Katny M. A., Torres-Mellado G. A., Palfner G., Cavieres L. A. (2011). The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21, 613–622. doi: 10.1007/s00572-011-0367-1, PMID: PubMed DOI

Cheng W. J., Xu Y. J., Huang G. M., Rahman M. M., Xiao Z. Y., Wu Q. S. (2020). Effects of five mycorrhizal fungi on biomass and leaf physiological activities of walnut. Not. Bot. Horti. Agrobot. Cluj-Napoca 48, 2021–2031. doi: 10.15835/nbha48412144 DOI

Cosme M., Fernández I., Van der Heijden M. G. A., Pieterse C. M. J. (2018). Non-mycorrhizal plants: the exceptions that prove the rule. Trends Plant Sci. 23, 577–587. doi: 10.1016/j.tplants.2018.04.004, PMID: PubMed DOI

Fernandez C. W., Kennedy P. G. (2015). Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol. 209, 1382–1394. doi: 10.1111/nph.13648, PMID: PubMed DOI

Flores-Rentería L., Lau M. K., Lamit L. J., Gehring C. A. (2014). An elusive ectomycorrhizal fungus reveals itself: a new species of Geopora (Pyronemataceae) associated with Pinus edulis. Mycologia 106, 553–563. doi: 10.3852/13-263, PMID: PubMed DOI

Frouz J., Elhottová D., Baldrián P., Chroňáková A., Lukešová A., Nováková A., et al. . (2014). “Soil microflora development in post-mining sites,” in Soil Biota and Ecosystem Development in Post Mining Sites. ed. Frouz J. (Boca Raton, FL, USA: CRC Press; ), 153–171.

Frouz J., Toyota A., Mudrák O., Jílková V., Filipová A., Cajthaml T. (2016). Effects of soil substrate quality, microbial diversity and community composition on the plant community during primary succession. Soil Biol. Biochem. 99, 75–84. doi: 10.1016/j.soilbio.2016.04.024 DOI

García de León D., Moora M., Öpik M., Neuenkamp L., Gerz M., Jairus T., et al. . (2016). Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS. Microb. Ecol. 92:fiw097. doi: 10.1093/femsec/fiw097, PMID: PubMed DOI

Gorzelak M. A., Asay A. K., Pickles B. J., Simard S. W. (2015). Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7:plv050. doi: 10.1093/aobpla/plv050, PMID: PubMed DOI PMC

Hachani C., Lamhamedi M. S., Cameselle C., Gouveia S., Zine El Abidine A., Khasa D. P., et al. . (2020). Effects of ectomycorrhizal fungi and heavy metals (Pb, Zn, and cd) on growth and mineral nutrition of Pinus halepensis seedlings in North Africa. Microorganisms 8:2033. doi: 10.3390/microorganisms8122033, PMID: PubMed DOI PMC

Haskins K. E., Gehring C. A. (2004). Interactions with juniper alter pinyon pine ectomycorrhizal fungal communities. Ecology 85, 2687–2692. doi: 10.1890/04-0306 DOI

Hoeksema J. D., Chaudhary V. B., Gehring C. A., Johnson N. C., Karst J., Koide R. T., et al. . (2010). A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394–407. doi: 10.1111/j.1461-0248.2009.01430.x, PMID: PubMed DOI

Huang L. J., Liu Z., Zhu B. C., Bing Y. H., Zhang X. X., Lü C. (2016). The allelopathic effects of humus soil from Betula platyphylla and Quercus liaotungensis on undergrowth medicinal species in the Qiaoshan area. Adv. J. Food Sci. Technol. 10, 610–615. doi: 10.19026/ajfst.10.2192 DOI

Hubert N. A., Gehring C. A. (2008). Neighboring trees affect ectomycorrhizal fungal community composition in a woodland-forest ecotone. Mycorrhiza 18, 363–374. doi: 10.1007/s00572-008-0185-2, PMID: PubMed DOI

Ihrmark K., Bödeker I. T. M., Cruz-Martinez K., Friberg H., Kubartova A., Schenck J., et al. . (2012). New primers to amplify the fungal ITS2 region – evaluation by 454-sequencing of artificial and natural communities. FEMS Microb. Ecol. 82, 666–677. doi: 10.1111/j.1574-6941.2012.01437.x, PMID: PubMed DOI

Janos D. P. (1980). Mycorrhizae influence tropical succession. Biotropica 12, 56–64. doi: 10.2307/2389230 DOI

Janos D. P., Scott J., Aristizábal C., Bowman D. M. J. S. (2013). Arbuscular-mycorrhizal networks inhibit Eucalyptus tetrodonta seedlings in rain forest soil microcosms. PLoS One 8:e57716. doi: 10.1371/journal.pone.0057716, PMID: PubMed DOI PMC

Janoušková M., Rydlová J., Püschel D., Száková J., Vosátka M. (2011). Extraradical mycelium of arbuscular mycorrhizal fungi radiating from large plants depresses the growth of nearby seedlings in a nutrient deficient substrate. Mycorrhiza 21, 641–650. doi: 10.1007/s00572-011-0372-4, PMID: PubMed DOI

Johnson N. C., Graham J. H., Smith F. A. (1997). Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135, 575–585. doi: 10.1046/j.1469-8137.1997.00729.x DOI

Jones M. D., Durall D. M., Tinker P. B. (1998). A comparison of arbuscular and ectomycorrhizal Eucalyptus coccifera: growth response, phosphorus uptake efficiency and external hyphal production. New Phytol. 140, 125–134. doi: 10.1046/j.1469-8137.1998.00253.x DOI

Klinsukon C., Lumyong S., Kuyper T. W., Boonlue S. (2021). Colonization by arbuscular mycorrhizal fungi improves salinity tolerance of eucalyptus (Eucalyptus camaldulensis) seedlings. Sci. Rep. 11:4362. doi: 10.1038/s41598-021-84002-5, PMID: PubMed DOI PMC

Knoblochova T., Kohout P., Püschel D., Doubková P., Frouz J., Cajthaml T., et al. . (2017). Asymmetric response of root-associated fungal communities of an arbuscular mycorrhizal grass and an ectomycorrhizal tree to their coexistence in primary succession. Mycorrhiza 27, 775–789. doi: 10.1007/s00572-017-0792-x, PMID: PubMed DOI

Kolaříková Z., Kohout P., Krüger C., Janoušková M., Mrnka L., Rydlová J. (2017). Root-associated fungal communities along a primary succession on a mine spoil: distinct ecological guilds assemble differently. Soil Biol. Biochem. 113, 143–152. doi: 10.1016/j.soilbio.2017.06.004 DOI

Koske R. E., Gemma J. N. (1989). A modified procedure for staining roots to detect VA mycorrhizas. Mycol. Res. 92, 486–488. doi: 10.1016/S0953-7562(89)80195-9 DOI

Lambers H., Raven J. A., Shaver G. R., Smith S. E. (2008). Plant nutrient-acquisition strategies change with soil age. Trends Ecol. Evol. 23, 95–103. doi: 10.1016/j.tree.2007.10.008, PMID: PubMed DOI

Lau J. A., Lennon J. T. (2012). Rapid responses of soil microorganisms improve plant fitness in novel environments. PNAS 109, 14058–14062. doi: 10.1073/pnas.1202319109, PMID: PubMed DOI PMC

Lin G., McCormack M. L., Guo D. (2015). Arbuscular mycorrhizal fungal effects on plant competition and community structure. J. Ecol. 103, 1224–1232. doi: 10.1111/1365-2745.12429 DOI

Lindahl B. D., Tunlid A. (2015). Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytol. 205, 1443–1447. doi: 10.1111/nph.13201 PubMed DOI

Lodge D. J., Wentworth T. R. (1990). Negative associations among va-mycorrhizal fungi and some ectomycorrhizal fungi inhabiting the same root system. Oikos 57, 347–356. doi: 10.2307/3565964 DOI

Long D., Liu J., Han Q., Wang X., Huang J. (2016). Ectomycorrhizal fungal communities associated with Populus simonii and Pinus tabuliformis in the hilly-gully region of the loess plateau, China. Sci. Rep. 6:24336. doi: 10.1038/srep24336, PMID: PubMed DOI PMC

McHugh T. A., Gehring C. A. (2006). Below-ground interactions with arbuscular mycorrhizal shrubs decrease the performance of pinyon pine and the abundance of its ectomycorrhizas. New Phytol. 171, 171–178. doi: 10.1111/j.1469-8137.2006.01735.x, PMID: PubMed DOI

Michelsen A., Schmidt I. K., Jonasson S., Dighton J., Jones H. E., Callaghan T. V. (1995). Inhibition of growth, and effects on nutrient uptake of arctic graminoids by leaf extracts – allelopathy or resource competition between plants and microbes? Oecologia 103, 407–418. doi: 10.1007/BF00328678, PMID: PubMed DOI

Moguilevsky D., Fernández N. V., Cornejo P. E., Puntieri J., Fontenla S. B. (2018). Nothofagus pumilio forests affected by tephra deposition in northern Patagonia: I - environmental traits influencing seedling growth. J. Soil Sci. Plant Nutr. 18, 487–498. doi: 10.4067/S0718-95162018005001502 DOI

Montesinos-Navarro A., Valiente-Banuet A., Verdú M. (2018). Processes underlying the effect of mycorrhizal symbiosis on plant-plant interactions. Fungal Ecol. 40, 98–106. doi: 10.1016/j.funeco.2018.05.003 DOI

Moora M., Zobel M. (1996). Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia 108, 79–84. doi: 10.1007/BF00333217, PMID: PubMed DOI

Mudrák O., Frouz J. (2012). Allelopathic effect of Salix caprea litter on late successional plants at different substrates of post-mining sites: pot experiment studies. Botany 90, 311–318. doi: 10.1139/b2012-005 DOI

Mudrák O., Hermová M., Tesnerová C., Rydlová J., Frouz J. (2016). Above-ground and below-ground competition between the willow Salix caprea and its understorey. J. Veg. Sci. 27, 156–164. doi: 10.1111/jvs.12330 DOI

Nara K. (2006a). Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol. 169, 169–178. doi: 10.1111/j.1469-8137.2005.01545.x, PMID: PubMed DOI

Nara K. (2006b). Pioneer dwarf willow may facilitate tree succession by providing late colonizers with compatible ectomycorrhizal fungi in a primary successional volcanic desert. New Phytol. 171, 187–198. doi: 10.2307/3694495, PMID: PubMed DOI

Nguyen N. H., Song Z., Bates S. T., Branco S., Tedersoo L., Menke J., et al. . (2016). FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248. doi: 10.1016/j.funeco.2015.06.006 DOI

Nilsson M. C., Hogberg P., Zackrisson O., Fengyou W. (1993). Allelopathic effects by Empetrum hermaphroditum on development and nitrogen uptake by roots and mycorrhizae of Pinus sylvestris. Canad. J. Bot. 71, 620–628. doi: 10.1139/b93-071 DOI

Olsson P. A. (1999). Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol. Ecol. 29, 303–310. doi: 10.1016/S0168-6496(99)00021-5 DOI

Oravecz O., Elhottová D., Kristůfek V., Sustr V., Frouz J., Tríska J., et al. . (2004). Application of ARDRA and PLFA analysis in characterizing the bacterial communities of the food, gut and excrement of saprophagous larvae of Penthetria holosericea (Diptera: Bibionidae): a pilot study. Folia Microbiol. 49, 83–93. doi: 10.1007/BF02931652, PMID: PubMed DOI

Peay K. G. (2016). The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu. Rev. Ecol. Evol. 47, 143–164. doi: 10.1146/annurev-ecolsys-121415-032100 DOI

Piotrowski J. S., Lekberg Y., Harner M. J., Ramsey P. W., Rillig M. C. (2008). Dynamics of mycorrhizae during development of riparian forests along an unregulated river. Ecography 31, 245–253. doi: 10.1111/j.0906-7590.2008.5262.x DOI

Prach K., Lencová K., Řehounková K., Dvořáková H., Jírová A., Konvalinková P., et al. . (2013). Spontaneous vegetation succession at different central European mining sites: a comparison across seres. Environ. Sci. Pollut. Res. 20, 7680–7685. doi: 10.1007/s11356-013-1563-7, PMID: PubMed DOI

Püschel D., Rydlová J., Vosátka M. (2007a). Mycorrhiza influences plant community structure in succession on spoil banks. Basic Appl. Ecol. 8, 510–520. doi: 10.1016/j.baae.2006.09.002 DOI

Püschel D., Rydlová J., Vosátka M. (2007b). The development of arbuscular mycorrhiza in two simulated stages of spoil-bank succession. Appl. Soil Ecol. 35, 363–369. doi: 10.1016/j.apsoil.2006.07.001 DOI

R Core Team (2018). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

Read D. J. (1991). Mycorrhizae in ecosystems. Experientia 47, 376–391. doi: 10.1007/BF01972080 DOI

Rydlová J., Püschel D., Dostálová M., Janousková M., Frouz J. (2016). Nutrient limitation drives response of Calamagrostis epigejos to arbuscular mycorrhiza in primary succession. Mycorrhiza 26, 757–767. doi: 10.1007/s00572-016-0712-5, PMID: PubMed DOI

Rydlová J., Püschel D., Janousková M., Vosátka M. (2014). “Interactions of plants with arbuscular mycorrhizal fungi during ecosystem development at post mining sites in the most coal basin (Czech Republic)” in Soil Biota and Ecosystem Development in Post Mining Sites. ed. Frouz J. (Boca Raton, FL, USA: CRC Press; ), 153–171.

Sharma M. P., Buyer J. S. (2015). Comparison of biochemical and microscopic methods for quantification of arbuscular mycorrhizal fungi in soil and roots. Appl. Soil Ecol. 95, 86–89. doi: 10.1016/j.apsoil.2015.06.001 DOI

Shemesh H., Boaz B. E., Millar C. I., Bruns T. D. (2019). Symbiotic interactions above treeline of long-lived pines: Mycorrhizal advantage of limber pine (Pinus flexilis) over Great Basin bristlecone pine (Pinus longaeva) at the seedling stage. J. Ecol. 108, 908–916. doi: 10.1111/1365-2745.13312 DOI

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

Šnajdr J., Valášková V., Merhautová V., Cajthaml T., Baldrian P. (2008). Activity and spatial distribution of lignocellulose-degrading enzymes during forest soil colonization by saprotrophic basidiomycetes. Enzyme Microb. Technol. 43, 186–192. doi: 10.1016/j.enzmictec.2007.11.008 DOI

Southworth D., Frank J. L. (2011). Linking mycorrhizas to sporocarps: a new species, Geopora cercocarpi on Cercocarpus ledifolius (Rosaceae). Mycologia 103, 1194–1200. doi: 10.3852/11-053, PMID: PubMed DOI

Stella T., Covino S., Burianová E., Filipová A., Křesinová Z., Voříšková J., et al. . (2015). Chemical and microbiological characterization of an aged PCB-contaminated soil. Sci. Total Environ. 533, 177–186. doi: 10.1016/j.scitotenv.2015.06.019, PMID: PubMed DOI

Tedersoo L., Bahram M. (2019). Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biol. Rev. 94, 1857–1880. doi: 10.1111/brv.12538, PMID: PubMed DOI

Teste F. P., Jones M. D., Dickie I. A. (2020). Dual-mycorrhizal plants: their ecology and relevance. New Phytol. 225, 1835–1851. doi: 10.1111/nph.16190, PMID: PubMed DOI

Thomson B. D., Grove T. S., Malajczuk N., Hardy G. E. S. J. (1994). The effectiveness of ectomycorrhizal fungi in increasing the growth of Eucalyptus globulus Labill. in relation to root colonization and hyphal development in soil. New Phytol. 126, 517–524. doi: 10.1111/j.1469-8137.1994.tb04250.x, PMID: PubMed DOI

Treseder K. K. (2013). The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371, 1–13. doi: 10.1007/s11104-013-1681-5 DOI

Trouvelot A., Kough J. L., Gianinazzi-Pearson V. (1986). “Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methodes d’estimation ayant une signification fonctionnelle,” in Physiological and Genetical Aspects of Mycorrhizae. eds. Gianinazzi-Pearson V., Gianinazzi S. (Paris: INRA; ), 217–221.

van der Heijden M. G. A., Bardgett R. D., van Straalen N. M. (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310. doi: 10.1111/j.1461-0248.2007.01139.x, PMID: PubMed DOI

Varga S., Kytöviita M. M. (2016). Faster acquisition of symbiotic partner by common mycorrhizal networks in early plant life stage. Ecosphere 7:e01222. doi: 10.1002/ecs2.1222 DOI

Vetrovský T., Baldrian P., Morais D. (2018). SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics 34, 2292–2294. doi: 10.1093/bioinformatics/bty071, PMID: PubMed DOI PMC

Walder F., Niemann H., Natarajan M., Lehmann M. F., Boller T., Wiemken A. (2012). Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 159, 789–797. doi: 10.1104/pp.112.195727, PMID: PubMed DOI PMC

White T. J., Bruns T., Lee S., Taylor J. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in PCR Protocols: a guide to Methods and Applications. eds. Innis M. A., Gelfand D. H., Sninsky J. J., White T. J. (New York: Academic Press; ), 315–322.

Zhenxing Y., Jing X., Shijun L., Liangliang H., Minglei R., Yu L., et al. . (2019). Adult plants facilitate their conspecific seedlings by enhancing arbuscular mycorrhizae in a saline soil. Plant Soil 447, 333–345. doi: 10.1007/s11104-019-04382-6 DOI

Zhou Y., Li X., Gao Y., Liu H., Gao Y. B., van der Heijden M. G. A., et al. . (2018). Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct. Ecol. 32, 1168–1179. doi: 10.1111/1365-2435.13084 DOI