Skip to main content
Log in

No evidence for allelopathic effects of arbuscular mycorrhizal fungi on the non-host plant Stellaria media

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Increasing evidence suggests that several plants, particularly non-mycorrhizal species, are negatively affected by the presence of arbuscular mycorrhizal fungi (AMF). Mechanisms explaining suppressive effects of AMF are, however, still poorly understood. Here we test whether growth suppression of the non-host weed Stellaria media in the presence of AMF can be explained by mycorrhizal alellopathy.

Methods

We grew S. media in microcosms where an active AM mycelium was supported by neighboring wheat (Triticum aestivum) plants. To test for allelopathy, we added activated carbon (AC) to the soil substrate. In addition, we performed two complementary experiments where extracts from roots extensively colonized by AMF (AM exudates) were directly applied to S. media seeds and seedlings.

Results

Stellaria media plants grown in microcosms with AM mycelium showed an 8-fold biomass reduction compared to microcosms where AMF were absent. The addition of AC, which is thought to reduce allelopathic effects by binding organic compounds, did not greatly mitigate the negative effect of AM mycelium on S. media growth. Moreover, AM exudates did not significantly reduce S. media germination and growth.

Conclusions

Results from this study confirm that non-hosts like S. media can be highly suppressed in the presence of AMF. However, we found no evidence that mycorrhizal allelopathy was a major mechanism responsible for growth suppression of S. media in the presence of AMF. Other mechanisms might therefore be more significant in explaining suppressive effects of AMF on non-host plant species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  PubMed  CAS  Google Scholar 

  • Allen MF, Allen EB (1990) Carbon source of VA mycorrhizal fungi associated with Chenopodiaceae from a semiarid shrub-steppe. Ecology 71:2019–2202

    Article  Google Scholar 

  • Allen MF, Allen EB, Friese CF (1989) Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytol 111:45–49

    Article  Google Scholar 

  • Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: From molecules and genes to species interactions. Science 301:1377–1380

    Article  PubMed  CAS  Google Scholar 

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Article  Google Scholar 

  • Boyetchko SM (1996) Impact of soil microorganisms on weed biology and ecology. Phytoprotection 77:41–56

    Article  Google Scholar 

  • Briggs D, Hodkinson H, Block M (1991) Precociously developing individuals in populations of chickweed [Stellaria media (L.) Vill.] from different habitat types, with special reference to the effects of weed control measures. New Phytol 117:153–164

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: A mechanism for exotic invasion. Science 290:521–523

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. FrontEcol Environ 2:436–443

    Article  Google Scholar 

  • Callaway RM, Ridenour WM, Laboski T, Weir T, Vivanco JM (2005) Natural selection for resistance to the allelopathic effects of invasive plants. J Ecol 93:576–583

    Article  Google Scholar 

  • Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE (2004) Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytol 161:485–494

    Article  Google Scholar 

  • Daisog H, Sbrana C, Cristani C, Moonen A-C, Giovannetti M, Bàrberi P (2012) Arbuscular mycorrhizal fungi shift competitive relationships among crop and weed species. Plant Soil 353:395–408

    Article  CAS  Google Scholar 

  • R Development Core Team (2009) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Facelli E, Smith SE, Facelli JM, Christophersen HM, Smith FA (2010) Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytol 185:1050–1061

    Article  PubMed  Google Scholar 

  • Fernandez-Aparicio M, Garcia-Garrido JM, Ocampo JA, Rubiales D (2010) Colonisation of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche species seed germination. Weed Res 50:262–268

    Article  Google Scholar 

  • Fitter A (2003) Making allelopathy respectable. Science 301:1337–1338

    Article  PubMed  CAS  Google Scholar 

  • Francis R, Read DJ (1994) The contributions of mycorrhizal fungi to the determination of plant community structure. Plant Soil 159:11–25

    Google Scholar 

  • Francis R, Read DJ (1995) Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can J Bot 73:S1301–S1309

    Article  Google Scholar 

  • Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386

    Article  PubMed  CAS  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Glenn MG, Chew FS, Williams PH (1985) Hyphal penetration of Brassica (Cruciferae) roots by a vesicular-arbuscular mycorrhizal fungus. New Phytol 99:463–472

    Article  Google Scholar 

  • Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–442

    Article  Google Scholar 

  • Harper JL (1977) The population biology of plants. Academic, London

    Google Scholar 

  • Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423

    Article  Google Scholar 

  • Hartnett DC, Hetrick BAD, Wilson GWT, Gibson DJ (1993) Mycorrhizal influence on intra- and interspecific neighbour interactions among co-occurring prairie grasses. J Ecol 81:787–795

    Article  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431–431

    Article  PubMed  CAS  Google Scholar 

  • Hetrick BAD, Hartnett DC, Wilson GWT, Gibson DJ (1994) Effects of mycorrhizae, phosphorus availability, and plant density on yield relationships among competing tallgrass prairie grasses. Can J Bot 72:168–176

    Article  Google Scholar 

  • Hirrel MC, Mehravaran H, Gerdemann JW (1978) Vesicular-arbuscular mycorrhizae in the Chenopodiaceae and Cruciferae: do they occur? Can J Bot 56:2813–2817

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agr Exp Sta Cir 347:1–32

    Google Scholar 

  • Houba V, van Vark W, Walinga I, van der Lee JJ (1989) Plant Analysis Procedures (Part 7, chapter 2.2). Department of Soil Science and Plant Analysis, Wageningen, The Netherlands

  • Inderjit, Callaway RM (2003) Experimental designs for the study of allelopathy. Plant Soil 256:1–11

    Article  CAS  Google Scholar 

  • Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234

    Article  PubMed  CAS  Google Scholar 

  • Johnson NC (1993) Can fertilization of soil select for less mutualistic mycorrhizae? Ecol Appl 3:749–757

    Article  Google Scholar 

  • Johnson NC (1998) Responses of Salsola kali and Panicum virgatum to mycorrhizal fungi, phosphorus and soil organic matter: implications for reclamation. J Appl Ecol 35:86–94

    Article  CAS  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586

    Article  Google Scholar 

  • Jordan NR, Zhang J, Huerd S (2000) Arbuscular-mycorrhizal fungi: potential roles in weed management. Weed Res 40:397–410

    Article  Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  PubMed  CAS  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • Kulmatiski A, Beard KH (2006) Activated carbon as a restoration tool: Potential for control of invasive plants in abandoned agricultural fields. Restor Ecol 14:251–257

    Article  Google Scholar 

  • Lau JA, Puliafico KP, Kopshever JA, Steltzer H, Jarvis EP, Schwarzlander M, Strauss SY, Hufbauer RA (2008) Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytol 178:412–423

    Article  PubMed  CAS  Google Scholar 

  • Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045

    Article  Google Scholar 

  • Lendzemo VW, Kuyper TW, Matusova R, Bouwmeester HJ, Van Ast A (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signal Behav 2:1–5

    Article  Google Scholar 

  • Lendzemo V, Kuyper TW, Vierheilig H (2009) Striga seed-germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi. Mycorrhiza 19:287–294

    Article  PubMed  CAS  Google Scholar 

  • Lutman PJW, Bowerman P, Palmer GM, Whytock GP (2000) Prediction of competition between oilseed rape and Stellaria media. Weed Res 40:255–269

    Article  Google Scholar 

  • Macias-Rubalcava ML, Hernandez-Bautista BE, Oropeza F, Duarte G, Gonzalez MC, Glenn AE, Hanlin RT, Anaya AL (2010) Allelochemical effects of volatile compounds and organic extracts from Muscodor yucatanensis, a tropical endophytic fungus from Bursera simarub. J Chem Ecol 36:1122–1131

    Article  PubMed  CAS  Google Scholar 

  • Mahall BE, Callaway RM (1992) Root communication mechanisms and intracommunity distributions of two Mojave Desert shrubs. Ecology 73:2145–2151

    Article  Google Scholar 

  • 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 115:495–501

    Article  Google Scholar 

  • Neumann E, George E (2005) Does the presence of arbuscular mycorrhizal fungi influence growth and nutrient uptake of a wild-type tomato cultivar and a mycorrhiza-defective mutant, cultivated with roots sharing the same soil volume? New Phytol 166:601–609

    Article  PubMed  CAS  Google Scholar 

  • Ocampo JA, Martin J, Hayman DS (1980) Influence of plant interactions on vesicular-arbuscular mycorrhizal infections. I. Host and non-host plants grown together. New Phytol 84:27–35

    Article  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mader P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824

    Article  PubMed  CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat Rev Microbiol 6:763–775

    Article  PubMed  CAS  Google Scholar 

  • Pietikainen J, Kiikkila O, Fritze H (2000) Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos 89:231–242

    Article  CAS  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in s and s-plus. Spinger-Verlag, New York

    Book  Google Scholar 

  • Putnam AR (1988) Allelochemicals from plants as herbicides. Weed Technol 2:510–518

    CAS  Google Scholar 

  • Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, Bothe H (2003) Colonization of pennycresses (Thlaspi spp) of the Brassicaceae by arbuscular mycorrhizal fungi. J Plant Physiol 160:615–62

    Article  PubMed  CAS  Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    Article  Google Scholar 

  • Rinaudo V, Barberi P, Giovannetti M, van der Heijden MGA (2010) Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil 333:7–20

    Article  CAS  Google Scholar 

  • Sanders IR, Koide RT (1994) Nutrient acquisition and community structure in co-occuring mycotrophic and non-mycotrophic old-field annuals. Funct Ecol 8:77–84

    Article  Google Scholar 

  • Scheublin TR, van Logtestijn RSP, van der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638

    Article  CAS  Google Scholar 

  • Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004

    Article  CAS  Google Scholar 

  • Siegel OS (1976) Handbuch der landwirtschaftlichen Versuchs‐ und Untersuchungsmethodik (Methodenbuch), Band III. Verlag J. Neumann, Berlin

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, Cambridge

    Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    Article  PubMed  CAS  Google Scholar 

  • Sobey DG (1981) Biological Flora of the British Isles, No. 150 Stellaria media (L.) Vill. J Ecol 69:311–335

    Article  Google Scholar 

  • Van Delden A, Lotz LAP, Bastiaans L, Franke AC, Smid HG, Groeneveld RMW, Kropff MJ (2002) The influence of nitrogen supply on the ability of wheat and potato to suppress Stellaria media growth and reproduction. Weed Res 42:429–445

    Article  Google Scholar 

  • van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150

    Article  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752

    Article  PubMed  Google Scholar 

  • van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Veiga RSL, Jansa J, Frossard E, van der Heijden MGA (2011) Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS One 6:e27825. doi:10.1371/journal.pone.0027825

    Article  PubMed  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    PubMed  CAS  Google Scholar 

  • Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292

    Article  Google Scholar 

  • Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–1313

    Article  PubMed  Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  PubMed  CAS  Google Scholar 

  • Wardle DA, Zackrisson O, Nilsson MC (1998) The charcoal effect in Boreal forests: mechanisms and ecological consequences. Oecologia 115:419–426

    Article  Google Scholar 

  • Weisshuhn K, Prati D (2009) Activated carbon may have undesired side effects for testing allelopathy in invasive plants. Basic Appl Ecol 10:500–507

    Article  CAS  Google Scholar 

  • Wurst S, Vender V, Rillig MC (2010) Testing for allelopathic effects in plant competition: does activated carbon disrupt plant symbioses? Plant Ecol 211:19–26

    Article  Google Scholar 

  • Yoneyama K, Xie XN, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Jürg Hiltbrunner for wheat seeds and Caroline Scherrer for AMF inoculum preparation. We also thank Cameron Wagg for comments on this manuscript and Yann Hautier for statistical advice. This work was supported by the Swiss Federal Government (Agroscope Reckenholz-Tänikon Research Station ART) and grants from the Swiss National Science Foundation (grant numbers: 315230_130764/1 and 31003AS_125428).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rita S. L. Veiga.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Relationship between percentage of root length colonized by G. intraradices in wheat and S. media. Plants were grown with or without addition of activated carbon to the soil substrate (AC and NC, respectively). Results are shown as linear regression slopes and 95 % CI (DOCX 218 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Veiga, R.S.L., Howard, K. & van der Heijden, M.G.A. No evidence for allelopathic effects of arbuscular mycorrhizal fungi on the non-host plant Stellaria media . Plant Soil 360, 319–331 (2012). https://doi.org/10.1007/s11104-012-1256-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-012-1256-x

Keywords

Navigation