Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T08:06:34.212Z Has data issue: false hasContentIssue false

Stable colonization of native plants and early invaders by arbuscular mycorrhizal fungi after exposure to recent invaders from the Asteraceae family

Published online by Cambridge University Press:  09 June 2021

Veronika Řezáčová
Affiliation:
Research Scientist, Crop Research Institute, Prague, Czech Republic
Milan Řezáč
Affiliation:
Research Scientist, Crop Research Institute, Prague, Czech Republic Research Scientist, Czech Academy of Sciences, Institute of Microbiology, Prague, Czech Republic
Zuzana Líblová
Affiliation:
Research Scientist, Czech Academy of Sciences, Institute of Microbiology, Prague, Czech Republic
Tereza Michalová
Affiliation:
Research Scientist, Czech Academy of Sciences, Institute of Microbiology, Prague, Czech Republic
Petr Heneberg*
Affiliation:
Associate Professor, Charles University, Third Faculty of Medicine, Prague, Czech Republic
*
Author for correspondence: Petr Heneberg, Charles University, Third Faculty of Medicine, Ruská 87, CZ-100 00 Prague, Czech Republic. (Email: petr.heneberg@lf3.cuni.cz)

Abstract

Arbuscular mycorrhizal fungi (AMF, Glomeromycota) are globally distributed symbionts of plant roots. Relationships with arbuscular mycorrhizae can provide crucial support for the establishment of any plant in an unfavorable environment. We hypothesized that invasions of neophytes are associated with changes in the colonization of native plants and early invaders (archeophytes) by AMF. We examined changes in AMF colonization in yarrow (Achillea millefolium L.) and wild carrot (Daucus carota L.) (native plants) and tansy (Tanacetum vulgare L.) and false oatgrass [Arrhenatherum elatius (L.) P. Beauv. ex J. Presl & C. Presl] (archeophytes) in response to the invasion of four neophytes from the Asteraceae family, namely great globethistle (Echinops sphaerocephalus L.), New York aster [Symphyotrichum novi-belgii (L.) G. L. Nesom agg.], annual fleabane [Erigeron annuus (L.) Pers.], and Canada goldenrod (Solidago canadensis L.). We found that the AMF colonization of the Asteraceae neophytes was high in the studied monodominant invasions, and the AMF colonization of the neophytes was higher than or equal to that of the studied native plants and archeophytes. Changes in plant dominance did not serve as predictors of the extent of AMF colonization of the native plants and archeophytes despite the invaded plots being associated with strong changes in the availability of primary and secondary mineral nutrients. The absence of a response of AMF colonization of native and archeophyte plant species to the invasion of neophytes suggests that AMF are passengers, rather than drivers, in the course of Asteraceae invasions in central European environments.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Weed Science Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Edith Allen, University of California, Riverside

References

Allen, MF (1991) The Ecology of Mycorrhizae. Cambridge: Cambridge University Press. 184 p Google Scholar
Ampe, F, Omar, NB, Moizan, C, Wacher, C, Guyot, J-P (1999) Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation independent methods to investigate traditional fermentations. Appl Environ Microbiol 65:54645473 10.1128/AEM.65.12.5464-5473.1999CrossRefGoogle ScholarPubMed
Awaydul, A, Zhu, W, Yuan, Y, Xiao, J, Hu, H, Chen, X, Koide, RT, Cheng, L (2019) Common mycorrhizal networks influence the distribution of mineral nutrients between an invasive plant, Solidago canadensis, and a native plant, Kummerowa striata . Mycorrhiza 29:2938 10.1007/s00572-018-0873-5CrossRefGoogle Scholar
Baxter, I, Dilkes, BP (2012) Elemental profiles reflect plant adaptations to the environment. Science 336:16611663 10.1126/science.1219992CrossRefGoogle ScholarPubMed
Betekhtina, AA, Mukhacheva, TA, Kovalev, SY, Gusev, AP, Veselkin, DV (2016) Abundance and diversity of arbuscular mycorrhizal fungi in invasive Solidago canadensis and indigenous S. virgaurea . Russian J Ecol 47:575579 10.1134/S1067413616060035CrossRefGoogle Scholar
Bever, JD, Platt, TG, Morton, ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265283 CrossRefGoogle ScholarPubMed
Bothe, H, Turnau, K, Regvar, M (2010) The potential role of arbuscular mycorrhizal fungi in protecting endangered plants and habitats. Mycorrhiza 20:445457 10.1007/s00572-010-0332-4CrossRefGoogle ScholarPubMed
Bozzolo, FH, Lipson, DA (2013) Differential responses of native and exotic coastal sage scrub plant species to N additions and the soil microbial community. Plant Soil 371:3751 10.1007/s11104-013-1668-2CrossRefGoogle Scholar
Broadbent, AAD, Stevens, CJ, Ostle, NJ, Orwin, KH (2018) Biogeographic differences in soil biota promote invasive grass response to nutrient addition relative to co-occurring species despite lack of belowground enemy release. Oecologia 186:611620 10.1007/s00442-018-4081-yCrossRefGoogle ScholarPubMed
Bücking, H, Kafle, A (2015) Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5:587612 10.3390/agronomy5040587CrossRefGoogle Scholar
Bunn, RA, Ramsey, PW, Lekberg, Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:15471556 CrossRefGoogle Scholar
Busby, RR (2011) Cheatgrass (Bromus tectorum L.) interactions with arbuscular mycorrhizal fungi in the North American steppe: prevalence and diversity of associations, and divergence from native vegetation. Diss Abstr Int 72(11):1136 Google Scholar
Chen, E, Liao, H, Chen, B, Peng, S (2020) Arbuscular mycorrhizal fungi are a double-edged sword in plant invasion controlled by phosphorus concentration. New Phytol 226:295300 CrossRefGoogle ScholarPubMed
Chmura, D, Guczwa-Przepióra, E (2012) Interactions between arbuscular mycorrhiza and the growth of the invasive alien annual Impatiens parviflora DC: a study of forest type and soil properties in nature reserves (S Poland). Appl Soil Ecol 62:7180 CrossRefGoogle Scholar
Cronk, QCB, Fuller, JR (2013) Plant Invaders: The Threat to Natural Ecosystems. London: Earthscan Publications. 241 p Google Scholar
Ehrenfeld, JG, Ravit, B, Elgersma, K (2005) Feedback in the plant-soil system. Annu Rev Environ Res 30:75115 CrossRefGoogle Scholar
Eliason, SA, Allen, EB (1997) Exotic grass competition in suppressing native shrubland re-establishment. Restor Ecol 5:245255 CrossRefGoogle Scholar
El Omari, B, El Ghachtouli, N (2021) Arbuscular mycorrhizal fungi-weeds interaction in cropping and unmanaged ecosystems: a review. Symbiosis 83:279292 CrossRefGoogle Scholar
EN 16170:2016 Sludge, Treated Biowaste and Soil—Determination of Elements Using Inductively Coupled Plasma Optical Emission Spectrometry (ICP-OES).Google Scholar
Grman, E (2012) Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711718 CrossRefGoogle ScholarPubMed
Gucwa-Przepiora, E, Chmura, D, Sokolowska, K (2016) AM and DSE colonization of invasive plants in urban habitat: a study of Upper Silesia (southern Poland). J Plant Res 129:603614 CrossRefGoogle Scholar
Hartwig, UA, Wittmann, P, Braun, R, Hartwig-Räz, B, Jansa, J, Mozafar, A, Lüscher, A, Leuchtmann, A, Frossard, E, Nösberger, J (2002) Arbuscular mycorrhiza infection enhances the growth response of Lolium perenne to elevated atmospheric pCO2 . J Exp Bot 53:12071213 CrossRefGoogle Scholar
Hoeksema, JD, Chaudhary, VB, Gehring, CA, Johnson, NC, Karst, J, Koide, RT, Pringle, A, Zabinski, C, Bever, JD, Moore, JC, Wilson, GWT, Klironomos, JN, Umbanhowar, J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394407 CrossRefGoogle ScholarPubMed
[ISO] International Organization for Standardization (1994) Soil Quality—Pretreatment of Samples for Physico-Chemical Analyses. ISO 11464:1994Google Scholar
[ISO] International Organization for Standardization (1998) Soil Quality—Determination of Organic Carbon by Sulfochromic Oxidation. ISO 14235:1998Google Scholar
Jansa, J, Erb, A, Oberholzer, H-R, Šmilauer, P, Egli, S (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol 23:21182135 CrossRefGoogle ScholarPubMed
Jez, JM, Lee, SG, Sherp, AM (2016) The next green movement: plant biology for the environment and sustainability. Science 353:12411244 CrossRefGoogle ScholarPubMed
Jin, L, Gu, Y, Xiao, M, Chen, J, Li, B (2004) The history of Solidago canadensis invasion and the development of its mycorrhizal associations in newly-reclaimed land. Funct Plant Biol 31:979986 CrossRefGoogle ScholarPubMed
Kempel, A, Nater, P, Fischer, M, Van Kleunen, M (2013) Plant-microbe-herbivore interactions in invasive and noninvasive alien plant species. Funct Ecol 27:498508 CrossRefGoogle Scholar
Klironomos, JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:6770 CrossRefGoogle ScholarPubMed
Lankau, RA, Nodurft, RN (2013) An exotic invader drives the evolution of plant traits that determine mycorrhizal fungal diversity in a native competitor. Mol Ecol 22:54725485 CrossRefGoogle Scholar
Lankau, RA, Strauss, SA (2007) Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317:15611563 CrossRefGoogle Scholar
Lankau, RA, Wheeler, E, Bennett, AE, Strauss, SY (2011) Plant-soil feedbacks contribute to an intransitive competitive network that promotes both genetic and species diversity. J Ecol 99:176185 CrossRefGoogle Scholar
Lee, J, Lee, S, Young, JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339349 CrossRefGoogle ScholarPubMed
Lekberg, Y, Gibbons, SM, Rosendahl, S, Ramsey, PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. Int Soc Microbial Ecol J 7:14241433 Google ScholarPubMed
Lekberg, Y, Hammer, EC, Olsson, PA (2010) Plants as resource islands and storage units—adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336345 CrossRefGoogle ScholarPubMed
Luo, J, Meiners, SJ, Carlsward, BS (2019) Mycorrhizal colonization in a successional plant community. Am Midl Nat 182:1226 CrossRefGoogle Scholar
Majewska, ML, Błaszkowski, J, Nobis, M, Rola, K, Nobis, A, Łakomiec, D, Czachura, P, Zubek, S (2015) Root-inhabiting fungi in alien plant species in relation to invasion status and soil chemical properties. Symbiosis 65:101115 CrossRefGoogle ScholarPubMed
Majewska, ML, Rola, K, Stefanowicz, AM, Nobis, M, Błaszkowski, J, Zubek, S (2018) Do the impacts of alien invasive plants differ from expansive native ones? An experimental study on arbuscular mycorrhizal fungi communities. Biol Fertil Soils 54:631643 CrossRefGoogle Scholar
Mamet, SD, Lamb, EG, Piper, CL, Winsley, T, Siciliano, SD (2017) Archaea and bacteria mediate the effects of native species root loss on fungi during plant invasion. ISME J 11:12611275 CrossRefGoogle ScholarPubMed
McGonigle, TP, Miller, MH, Evans, DG, Fairchild, GL, Swan, JA (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495501 CrossRefGoogle ScholarPubMed
Muyzer, G, De Wall, EC, Uitterlinden, AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695700 CrossRefGoogle ScholarPubMed
Němeček, J, Šimek, J, Ryglevicz, J (1967) Průzkum zemědělských půd ČSSR. Souborná metodika. Prague: MZVž. 125 pGoogle Scholar
Newsham, KK, Fitter, AH, Watkinson, AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:9911000 CrossRefGoogle Scholar
Nunez, MA, Dickie, IA (2014) Invasive belowground mutualists of woody plants. Biol Invas 16:645661 CrossRefGoogle Scholar
Oldroyd, GED, Leyser, O (2020) A plant’s diet, surviving in a variable nutrient environment. Science 368:eaba0196 CrossRefGoogle Scholar
Pyšek, P, Danihelka, J, Sádlo, J, Chrtek, J, Chytrý, M, Jarošík, V, Kaplan, Z, Krahulec, F, Moravcová, L, Pergl, J, Štajerová, K, Tichý, L (2012) Catalogue of alien plants of the Czech Republic (2nd edition) checklist update, taxonomic diversity and invasion patterns. Preslia 84:155255 Google Scholar
Pyšek, P, Sádlo, J, Mandák, B (2002) Catalogue of alien plants of the Czech Republic. Preslia 74:97186 Google Scholar
Reinhart, KO, Callaway, RM (2006) Soil biota and invasive plants. New Phytol 170:445457 CrossRefGoogle ScholarPubMed
Reinhart, KO, Packer, A, Van der Putten, WH, Clay, K (2003) Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:10461050 CrossRefGoogle Scholar
Reinhold-Hurek, B, Bunger, W, Burbano, CS, Sabale, M, Hurek, T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403424 CrossRefGoogle ScholarPubMed
Řezáčová, V, Konvalinková, T, Řezáč, M (2020) Decreased mycorrhizal colonization of Conyza canadensis (L.) Cronquist in invaded range does not affect fungal abundance in native plants. Biologia 75:693699 CrossRefGoogle Scholar
Řezáčová, V, Řezáč, M, Gryndler, M, Hršelová, H, Gryndlerová, H, Michalová, T (2021a) Plant invasion alters community structure and decreases diversity of arbuscular mycorrhizal fungal communities. Appl Soil Ecol 167:104039 CrossRefGoogle Scholar
Řezáčová, V, Řezáč, M, Gryndlerová, H, Wilson, GWT, Michalová, T (2021b) Arbuscular mycorrhizal fungi favor invasive Echinops sphaerocephalus when grown in competition with native Inula conyzae . Sci Rep 10:20287 CrossRefGoogle Scholar
Richardson, DM, Allsopp, N, D’Antonio, CM, Milton, SJ, Rejmanek, M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:6593 CrossRefGoogle ScholarPubMed
Schittko, C, Wurst, S (2014) Above- and belowground effects of plant-soil feedback from exotic Solidago canadensis on native Tanacetum vulgare . Biol Invasions 16:14651479 CrossRefGoogle Scholar
Shah, MA, Reshi, ZA, Khasa, DP (2009) Arbuscular mycorrhizas: drivers or passengers of alien plant invasion. Bot Rev 75:397417 CrossRefGoogle Scholar
Shi, ZY, Feng, G, Christie, P, Li, XL (2006) Arbuscular mycorrhizal status of spring ephemerals in the desert ecosystem of Junggar Basin, China. Mycorrhiza 16:269275 CrossRefGoogle ScholarPubMed
Simon, LM, Lalonde, TD, Bruns, TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291295 CrossRefGoogle ScholarPubMed
Smith, SE, Read, DJ (2008) Mycorrhizal Symbiosis. Amsterdam: Academic Press. 800 p Google Scholar
Štajerová, K, Šmilauerová, M, Šmilauer, P (2009) Arbuscular mycorrhizal symbiosis of herbaceous invasive neophytes in the Czech Republic. Preslia 81:341355 Google Scholar
Stinson, KA, Campbell, SA, Powell, JR, Wolfe, BE, Callaway, RM, Thelen, GC, Hallett, SG, Prati, D, Klironomos, JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727731 CrossRefGoogle ScholarPubMed
Stoeck, T, Bass, D, Nebel, M, Christen, R, Jones, MDM, Breiner, H-W, Richards, TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19:2131 CrossRefGoogle ScholarPubMed
Stromberg, MR, Griffin, JR (1996) Long-term patterns in coastal California grasslands in relation to cultivation, gophers, and grazing. Ecol Appl 6:11891211 CrossRefGoogle Scholar
Stylinski, CD, Allen, EB (1999) Lack of native species recovery following severe exotic disturbance in southern Californian shrublands. J Appl Ecol 36:544554 CrossRefGoogle Scholar
Tawaraya, K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655668 CrossRefGoogle Scholar
Thonar, C, Erb, A, Jansa, J (2012) Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities—marker design, verification, calibration and field validation. Mol Ecol Res 12:219232 CrossRefGoogle ScholarPubMed
van der Heijden, MGA, Martin, FM, Selosse, MA, Sanders, IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:14061423 CrossRefGoogle ScholarPubMed
van der Putten, WH, Klironomos, JN, Wardle, DA (2007) Microbial ecology of biological invasions. ISME J 1:2837 CrossRefGoogle ScholarPubMed
van Grunsven, RHA, van der Putten, WH, Bezemer, TM, Tamis, WLM, Berendse, F, Veenendaal, EM (2007) Reduced plant-soil feedback of plant species expanding their range as compared to natives. J Ecol 95:10501057 CrossRefGoogle Scholar
Vigo, C, Norman, JR, Hooker, JE (2000) Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol 49:509514 CrossRefGoogle Scholar
Vogelsang, KM, Bever, JD (2009) Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399407 CrossRefGoogle ScholarPubMed
Westover, KM, Bever, JD (2001) Mechanisms of plant species coexistence: roles of rhizosphere bacteria and root fungal pathogens. Ecology 82:32853294 CrossRefGoogle Scholar
Wetzel, PR (1996) The Role of Arbuscular Mycorrhizal Fungi in Prairie Wetlands. Ph.D thesis. Ames: Iowa State University. 107 pGoogle Scholar
Wilson, GWT, Hartnett, DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:17321738 CrossRefGoogle ScholarPubMed
Yang, R, Yu, G, Tang, J, Chen, X (2008) Effects of metal lead on growth and mycorrhizae of an invasive plant species (Solidago canadensis L.). J Environ Sci 20:739744 CrossRefGoogle Scholar
Yang, R, Zhou, G, Zan, S, Guo, F, Su, N, Li, J (2014) Arbuscular mycorrhizal fungi facilitate the invasion of Solidago canadensis L. in southeastern China. Acta Oecol 61:7177 CrossRefGoogle Scholar
Yuan, Y, Tang, J, Leng, D, Hu, S, Yong, JWH, Chen, X (2014) An invasive plant promotes its arbuscular mycorrhizal symbioses and competitiveness through its secondary metabolites: indirect evidence from activated carbon. PLoS ONE 9:e97163 CrossRefGoogle ScholarPubMed
Zbíral, J (2010) Analýza půd I. Brno: ÚKZÚZ. 290 p Google Scholar
Zhang, Q, Yang, R, Tang, J, Yang, H, Hu, S, Chen, X (2010) Positive feedback between mycorrhizal fungi and pants influences plant invasion success and resistance to invasion. PLoS ONE 5:e12380 CrossRefGoogle Scholar
Zhang, S, Jin, Y, Tang, J, Chen, X (2009) The invasive plant Solidago canadensis L. suppresses local soil pathogens through allelopathy. Appl Soil Ecol 41:215222 CrossRefGoogle Scholar
Zubek, S, Majewska, LM, Błaszkowski, J, Stefanowicz, AM, Nobis, M, Kapusta, P (2016) Invasive plants affect arbuscular mycorrhizal fungi abundance and species richness as well as the performance of native plants grown in invaded soils. Biol Fertil Soils 52:879893 CrossRefGoogle Scholar
Supplementary material: File

Řezáčová et al. supplementary material

Řezáčová et al. supplementary material

Download Řezáčová et al. supplementary material(File)
File 11.4 KB