In a globalized world, plant invasions are common challenges for native ecosystems. Although a considerable number of invasive plants form arbuscular mycorrhizae, interactions between arbuscular mycorrhizal (AM) fungi and invasive and native plants are not well understood. In this study, we conducted a greenhouse experiment examining how AM fungi affect interactions of co-occurring plant species in the family Asteracea, invasive Echinops sphaerocephalus and native forb of central Europe Inula conyzae. The effects of initial soil disturbance, including the effect of intact or disturbed arbuscular mycorrhizal networks (CMNs), were examined. AM fungi supported the success of invasive E. sphaerocephalus in competition with native I. conyzae, regardless of the initial disturbance of CMNs. The presence of invasive E. sphaerocephalus decreased mycorrhizal colonization in I. conyzae, with a concomitant loss in mycorrhizal benefits. Our results confirm AM fungi represent one important mechanism of plant invasion for E. sphaerocephalus in semi-natural European grasslands.

Crop Research Institute Drnovská 507 Prague 6 Czech Republic

Department of Natural Resource Ecology and Management Oklahoma State University Stillwater OK USA

Institute of Microbiology of the Czech Academy of Sciences Vídeňská 1083 Prague 4 Czech Republic

Zobrazit více v PubMed

Spatafora JW, et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108:1028–1046. doi: 10.3852/16-042. PubMed DOI PMC

Smith SE, Read DJ. Mycorrhizal Symbiosis. Amsterdam: Academic Press; 2008.

van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 2015;205:1406–1423. doi: 10.1111/nph.13288. PubMed DOI

Lekberg Y, Hammer EC, Olsson PA. Plants as resource islands and storage units—adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol. Ecol. 2010;74:336–345. doi: 10.1111/j.1574-6941.2010.00956.x. PubMed DOI

Allen MF. Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J. 2007;6:291–297. doi: 10.2136/vzj2006.0068. DOI

Newsham KK, Fitter AH, Watkinson AR. Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J. Ecol. 1995;83:991–1000. doi: 10.2307/2261180. DOI

Vigo C, Norman JR, Hooker JE. Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol. 2000;49:509–514. doi: 10.1046/j.1365-3059.2000.00473.x. DOI

Aroca R, Porcel R, Ruiz-Lozano JM. How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol. 2007;173(4):808–816. doi: 10.1111/j.1469-8137.2006.01961.x. PubMed DOI

Augé, R. M., Toler, H. D. & Saxton, A. M. Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front Plant Sci.5, ARTN 562. 10.3389/fpls.2014.00562 (2014). PubMed PMC

Augé RM, Toler HD, Saxton AM. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza. 2015;25(1):13–24. doi: 10.1007/s00572-014-0585-4. PubMed DOI

Pfeffer PE, Douds DD, Becard G, Shachar-Hill Y. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 1999;120(2):587–598. doi: 10.1104/pp.120.2.587. PubMed DOI PMC

Bago B, Pfeffer PE, Shachar-Hill Y. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 2000;124(3):949–958. doi: 10.1104/pp.124.3.949. PubMed DOI PMC

Horton TR. Mycorrhizal networks. Dordrecht: Springer; 2015.

Walder F, van der Heijden MGA. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat. Plants. 2015;1(11):7. doi: 10.1038/nplants.2015.159. PubMed DOI

van der Heijden MGA, et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature. 1998;396(6706):69–72. doi: 10.1038/23932. DOI

Wilson GWT, Hartnett DC, Rice CW. Mycorrhizal-mediated phosphorus transfer between the tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Funct. Ecol. 2006;20:427–435. doi: 10.1111/j.1365-2435.2006.01134.x. DOI

Bever JD, et al. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 2010;25(8):468–478. doi: 10.1016/j.tree.2010.05.004. PubMed DOI PMC

Walder F, et al. Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 2012;159:789–797. doi: 10.1104/pp.112.195727. PubMed DOI PMC

Weremijewicz J, Sternberg L, Janos DP. Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol. 2016;212(2):461–471. doi: 10.1111/nph.14041. PubMed DOI

Řezáčová V, et al. Little cross-feeding of the mycorrhizal networks shared between C3-Panicum bisulcatum and C4-Panicum maximum under different temperature regimes. Front. Plant Sci. 2018;9:16. doi: 10.3389/fpls.2018.00449. PubMed DOI PMC

Deslippe JR, Simard SW. Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytol. 2011;192:689–698. doi: 10.1111/j.1469-8137.2011.03835.x. PubMed DOI

Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol. Lett. 2009;12(1):13–21. doi: 10.1111/j.1461-0248.2008.01254.x. PubMed DOI

Lendenmann M, et al. Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza. 2011;21(8):689–702. doi: 10.1007/s00572-011-0371-5. PubMed DOI

Kiers ET, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. 2011;333(6044):880–882. doi: 10.1126/science.1208473. PubMed DOI

Rillig MC. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol. Lett. 2004;7:740–754. doi: 10.1111/j.1461-0248.2004.00620.x. DOI

Verbruggen E, Kiers ET. Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl. 2010;3(5–6):547–560. doi: 10.1111/j.1752-4571.2010.00145.x. PubMed DOI PMC

van Kleunen M, et al. Global exchange and accumulation of non-native plants. Nature. 2015;525(7567):100–103. doi: 10.1038/nature14910. PubMed DOI

Pejchar L, Mooney HA. Invasive species, ecosystem services and human well-being. Trends Ecol. Evol. 2009;24(9):497–504. doi: 10.1016/j.tree.2009.03.016. PubMed DOI

Pyšek P, et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species' traits and environment. Glob. Change Biol. 2012;18(5):1725–1737. doi: 10.1111/j.1365-2486.2011.02636.x. DOI

Blackburn, T. M. et al. A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol.12(5), ARTN e1001850. 10.1371/journal.pbio.1001850 (2014). PubMed PMC

Mitchell CE, et al. Biotic interactions and plant invasions. Ecol. Lett. 2006;9(6):726–740. doi: 10.1111/j.1461-0248.2006.00908.x. PubMed DOI

Catford JA, Jansson R, Nilsson C. Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers. Distrib. 2009;15(1):22–40. doi: 10.1111/j.1472-4642.2008.00521.x. DOI

van der Putten WH. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol. Evol. 2010;25(9):512–519. doi: 10.1016/j.tree.2010.06.006. PubMed DOI

Keane RM, Crawley MJ. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 2002;17(4):164–170. doi: 10.1016/S0169-5347(02)02499-0. DOI

Pyšek P, et al. Naturalization of central European plants in North America: species traits, habitats, propagule pressure, residence time. Ecology. 2015;96(3):762–774. doi: 10.1890/14-1005.1. PubMed DOI

Davis MA, Grime JP, Thompson K. Fluctuating resources in plant communities: a generaltheory of invasibility. J. Ecol. 2000;88:528–534. doi: 10.1046/j.1365-2745.2000.00473.x. DOI

Callaway RM, Thelen GC, Rodriguez A, Holben WE. Soil biota and exotic plant invasion. Nature. 2004;427(6976):731–733. doi: 10.1038/nature02322. PubMed DOI

Rudgers JA, Orr S. Non-native grass alters growth of native tree species via leaf and soil microbes. J. Ecol. 2009;97(2):247–255. doi: 10.1111/j.1365-2745.2008.01478.x. DOI

Sun ZK, He WM. Evidence for enhanced mutualism hypothesis: Solidago canadensis plants from regular soils perform better. PLoS ONE. 2010;5(11):5. doi: 10.1371/journal.pone.0015418. PubMed DOI PMC

Dickie IA, et al. The emerging science of linked plant-fungal invasions. New Phytol. 2017;215(4):1314–1332. doi: 10.1111/nph.14657. PubMed DOI

Cronk QCB, Fuller JR. Plant Invaders: The Threat to Natural Ecosystems. London: Earthscan Publications; 2001.

Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmanek M. Plant invasions—the role of mutualisms. Biol. Rev. 2000;75(1):65–93. doi: 10.1017/S0006323199005435. PubMed DOI

Pringle A, et al. Mycorrhizal symbioses and plant invasions. Ann Rev. Ecol. Evol. Syst. 2009;40:699–715. doi: 10.1146/annurev.ecolsys.39.110707.173454. DOI

Wilson GWT, Hickman KR, Williamson MM. Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses. Mycorrhiza. 2012;22:327–336. doi: 10.1007/s00572-011-0407-x. PubMed DOI

Nunez MA, Dickie IA. Invasive belowground mutualists of woody plants. Biol. Invasions. 2014;16:645–661. doi: 10.1007/s10530-013-0612-y. DOI

Bunn RA, Ramsey PW, Lekberg Y. Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J. Ecol. 2015;103:1547–1556. doi: 10.1111/1365-2745.12456. DOI

Gucwa-Przepiora E, Chmura D, Sokolowska K. AM and DSE colonization of invasive plants in urban habitat: a study of Upper Silesia (southern Poland) J. Plant Res. 2016;129:603–614. doi: 10.1007/s10265-016-0802-7. PubMed DOI PMC

Waller LP, Callaway RM, Klironomos JN, Ortega YK, Maron JL. Reduced mycorrhizal responsiveness leads to increased competitive tolerance in an invasive exotic plant. J. Ecol. 2016;104:1599–1607. doi: 10.1111/1365-2745.12641. DOI

Menzel A, et al. Mycorrhizal status helps explain invasion success of alien plant species. Ecology. 2017;98:92–102. doi: 10.1002/ecy.1621. PubMed DOI

Broadbent AAD, Stevens CJ, Ostle NJ, Orwin KH. Biogeographic differences in soil biota promote invasive grass response to nutrient addition relative to co-occurring species despite lack of belowground enemy release. Oecologia. 2018;186:611–620. doi: 10.1007/s00442-018-4081-y. PubMed DOI

Vogelsang KM, Bever JD. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology. 2009;90:399–407. doi: 10.1890/07-2144.1. PubMed DOI

Reinhart KO, Callaway RM. Soil biota and invasive plants. New Phytol. 2006;170:445–457. doi: 10.1111/j.1469-8137.2006.01715.x. PubMed DOI

Pakpour S, Klironomos J. The invasive plant, Brassica nigra, degrades local mycorrhizas across a wide geographical landscape. R. Soc. Open Sci. 2015;2:4. doi: 10.1098/rsos.150300. PubMed DOI PMC

Shah MA, Reshi ZA, Khasa DP. Arbuscular mycorrhizas: Drivers or passengers of alien plant invasion. Bot. Rev. 2009;75:397–417. doi: 10.1007/s12229-009-9039-7. DOI

De Souza TAF, Rodriguez-Echeverria S, de Andrade LA, Freitas H. Could biological invasion by Cryptostegia madagascariensis alter the composition of the arbuscular mycorrhizal fungal community in semi-arid Brazil? Acta Bot. Bras. 2016;30:93–101. doi: 10.1590/0102-33062015abb0190. DOI

Awaydul A, et al. Common mycorrhizal networks influence the distribution of mineral nutrients between an invasive plant, Solidago canadensis, and a native plant, Kummerowa striata. Mycorrhiza. 2019;29:29–38. doi: 10.1007/s00572-018-0873-5. PubMed DOI

Štajerová K, Šmilauerová M, Šmilauer P. Arbuscular mycorrhizal symbiosis of herbaceous invasive neophytes in the Czech Republic. Preslia. 2009;81:341–355.

Hempel S, et al. Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology. Ecology. 2013;94:1389–1399. doi: 10.1890/12-1700.1. PubMed DOI

Callaway RM, Newingham B, Zabinski CA, Mahall BE. Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecol. Lett. 2001;4:429–433. doi: 10.1046/j.1461-0248.2001.00251.x. DOI

Workman RE, Cruzan MB. Common mycelial networks impact competition in an invasive grass. Am. J. Bot. 2016;103:1041–1049. doi: 10.3732/ajb.1600142. PubMed DOI

Zhang Q, et al. Potential allelopathic effects of an invasive species Solidago canadensis on the mycorrhizae of native plant species. Allelopathy J. 2007;20:71–77.

Callaway RM, et al. Novel weapons: Invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology. 2008;89:1043–1055. doi: 10.1890/07-0370.1. PubMed DOI

Sarma KKV. Allelopathic potential of Echinops echinatus and Solanum surratense on seed germination of Argemone mexicana. Trop. Ecol. 1974;15:156–157.

Smith MD, Hartnett DC, Wilson GWT. Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia. 1999;121:574–582. doi: 10.1007/s004420050964. PubMed DOI

Bennett JA, et al. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science. 2017;355:181–184. doi: 10.1126/science.aai8212. PubMed DOI

Liao HX, et al. Soil microbes regulate forest succession in a subtropical ecosystem in China: evidence from a mesocosm experiment. Plant Soil. 2018;430:277–289. doi: 10.1007/s11104-018-3733-3. DOI

Řezáčová V, et al. Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4Panicum grasses. Plant Soil. 2018;425:441–456. doi: 10.1007/s11104-018-3606-9. DOI

Newman EI. A method of estimating total length of root in a sample. J. Appl. Ecol. 1966;3:139–145. doi: 10.2307/2401670. DOI

Bukovská P, Gryndler M, Gryndlerová H, Püschel D, Jansa J. Organic nitrogen-driven stimulation of arbuscular mycorrhizal fungal hyphae correlates with abundance of ammonia oxidizers. Front. Microbiol. 2016;7:711. doi: 10.3389/fmicb.2016.00711. PubMed DOI PMC

Hewitt EJ. Sand and water culture methods used in the study of plant nutrition. CAB Tech. Commun. 1966;22:431–432.

Řezáčová V, et al. Imbalanced carbon-for-phosphorus exchange between European arbuscular mycorrhizal fungi and non-native Panicum grasses—a case of dysfunctional symbiosis. Pedobiologia. 2017;62:48–55. doi: 10.1016/j.pedobi.2017.05.004. DOI

Ohno T, Zibilske LM. Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 1991;55:892–895. doi: 10.2136/sssaj1991.03615995005500030046x. DOI

McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol. 1990;115:495–501. doi: 10.1111/j.1469-8137.1990.tb00476.x. PubMed DOI

Koske RE, Gemma JN. A modified procedure for staining roots to detect VA-mycorrhizas. Mycol. Res. 1989;92:486–505. doi: 10.1016/S0953-7562(89)80195-9. DOI

Gryndler M, et al. Tuber aestivum Vittad. mycelium quantified: advantages and limitations of a qPCR approach. Mycorrhiza. 2013;23:341–348. doi: 10.1007/s00572-012-0475-6. PubMed DOI

Thonar C, Erb A, Jansa J. Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities-marker design, verification, calibration and field validation. Mol. Ecol. Res. 2012;12:219–232. doi: 10.1111/j.1755-0998.2011.03086.x. PubMed DOI

von Felten A, Défago G, Maurhofer M. Quantification of Pseudomonas fluorescens strains F113, CHA0 and Pf153 in the rhizosphere of maize by strain-specific real-time PCR unaffected by the variability of DNA extraction efficiency. J. Microbiol. Methods. 2010;81:108–115. doi: 10.1016/j.mimet.2010.02.003. PubMed DOI

Janoušková M, Püschel D, Hujslová M, Slavíková R, Jansa J. Quantification of arbuscular mycorrhizal fungal DNA in roots: how important is material preservation? Mycorrhiza. 2015;25:205–214. doi: 10.1007/s00572-014-0602-7. PubMed DOI

Arbuscular mycorrhiza can be disadvantageous for weedy annuals in competition with paired perennial plants