Skip to main content
Log in

Three symbionts involved in interspecific plant-soil feedback: epichloid endophytes and mycorrhizal fungi affect the performance of rhizobia-legume symbiosis

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

Abstract

Aims

Plants interact by modifying soil conditions in plant-soil feedback processes. Foliar endophytes of grasses exert multiple effects on host rhizosphere with potential consequences on plant-soil feedback. Here, we hypothesize that the grass-endophyte symbiosis impairs soil symbiotic potential, and in turn influences legume performance and nitrogen acquisition.

Methods

Soil was conditioned in pots, growing Lolium multiflorum with or without the fungal endophyte Epichloë and with or without arbuscular mycorrhizal fungi (AMF). Then, Trifolium repens grew in all types of conditioned soils with high or low rhizobia availability.

Results

Endophyte soil conditioning reduced AMF spores number and rhizobial nodules (−27 % and −38 %, respectively). Seedling survival was lower in endophyte-conditioned soil and higher in mycorrhizal soils (−27 % and +24 %, respectively). High rhizobia-availability allowed greater growth and nitrogen acquisition, independent of soil conditioning. Low rhizobia-availability allowed both effects only in endophyte-conditioned soil.

Conclusion

Endophyte-induced changes in soil (i) hindered symbiotic potential by reducing AMF spore availability or rhizobia nodulation, (ii) impaired legume survival irrespective of belowground symbionts presence, but (iii) mimicked rhizobia effects, enhancing growth and nitrogen fixation in poorly nodulated plants. Our results show that shoot and root symbionts can be interactively involved in interspecific plant-soil feedback.

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

Similar content being viewed by others

References

  • Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman JA (2008) Even after death the endophytic fungus of Schenodorus phoenix reduces the arbuscular mycorrhiza of other plants. Funct Ecol 22:912–918

    Article  Google Scholar 

  • Appleby CA (1984) Leghemoglobin and rhizobium respiration. Annu Rev Plant Physiol 35:443–478

    Article  CAS  Google Scholar 

  • Bååth E, Hayman DS (1984) Effect of soil volume and plant density on mycorrhizal infection and growth response. Plant Soil 77(2–3):373–376

  • Bacon CW, White JFJ (1994) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. doi:10.18637/jss.v067.i01

    Article  Google Scholar 

  • Baxendale C, Orwin KH, Poly F, Pommier T, Bardgett RD (2014) Are plant-soil feedback responses explained by plant traits? New Phytol 204:408–423

    Article  PubMed  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 

  • Bever JD, Broadhurst LM, Thrall PH (2013) Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks. Ecol Lett 16:167–174

    Article  PubMed  Google Scholar 

  • Bowatte S, Barrett B, Luscombe C, Hume DE, Luo D, Theobald P, Newton PC (2011) Effect of grass species and fungal endophyte on soil nitrification potential. N Z J Agric Res 54:275–284

    Article  CAS  Google Scholar 

  • Breen JP (1994) Acremonium endophyte interactions with enhanced plant resistance to insects. Annu Rev Entomol 39:401–423

    Article  Google Scholar 

  • Buyer JS, Zuberer DA, Nichols KA, Franzluebbers AJ (2011) Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant Soil 339(1–2):401–412

  • Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340:347–355

    Article  CAS  Google Scholar 

  • Casas C, Torreta JP, Exeler N, Omacini M (2016) What happens next? Legacy effects induced by grazing and grass-endophyte symbiosis on thistle plants and their floral visitors. Plant Soil 405:211–229

    Article  CAS  Google Scholar 

  • Chu-Chou M, Guo B, An Z-Q, Hendrix JW, Ferriss RS, Siegel MR, Dougherty CT, Burrus PB (1992) Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol Biochem 24:633–637

    Article  Google Scholar 

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744

    Article  CAS  PubMed  Google Scholar 

  • Cripps MG, Edwards GR, McKenzie SL (2013) Grass species and their fungal symbionts affect subsequent forage growth. Basic Appl Ecol 14:225–234

    Article  Google Scholar 

  • Eerens JPJ, Lucas RJ, Easton HS, White JGH (1998) Influence of the ryegrass endophyte Neotyphodium lolii. in a cool-moist environment III Interaction with white clover. N Z J Agric Res 41:201–207

    Article  Google Scholar 

  • Franzluebbers AJ (2006) Short-term responses of soil C and N fractions to tall fescue endophyte infection. Plant Soil 282:153–164

    Article  CAS  Google Scholar 

  • García Parisi PA, Grimoldi AA, Omacini M (2014) Endophytic fungi of grasses protect other plants from aphid herbivory. Fungal Ecol 9:61–64

    Article  Google Scholar 

  • García Parisi PA, Lattanzi FA, Grimoldi AA, Omacini M (2015) Multi-symbiotic systems: functional implications of the coexistence of grass–endophyte and legume–rhizobia symbioses. Oikos 124:553–560

    Article  Google Scholar 

  • Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244

    Article  Google Scholar 

  • Grace JB, Tilman D (1990) Perspectives on plant competition. Academic Press, San Diego

    Google Scholar 

  • Grigulis K, Lavorel S, Krainer U, Legay N, Baxendale C, Dumont M, Kastl E, Arnoldi C, Bardgett RD, Poly F, Pommier T, Schloter M, Tappeiner U, Bahn M, Clément J-C (2013) Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J Ecol 101:47–57

    Article  Google Scholar 

  • Grimoldi AA, Kavanová M, Lattanzi FA, Schnyder H (2005) Phosphorus nutrition-mediated effects of arbuscular mycorrhiza on leaf morphology and carbon allocation in perennial ryegrass. New Phytol 168:435–444

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Fitter AH (2013) Microbial mediation of plant competition and community structure. Funct Ecol 27:865–875

    Article  Google Scholar 

  • Högberg P (1997) Tansley review no. 95. 15 N natural abundance in soil-plant systems. New Phytol 137:179–203

    Article  Google Scholar 

  • Jenkins MB, Franzluebbers AJ, Humayoun SB (2006) Assessing short-term responses of prokaryotic communities in bulk and rhizosphere soils to tall fescue endophyte infection. Plant Soil 289:309–320

    Article  CAS  Google Scholar 

  • Ke PJ, Miki T, Ding TS (2015) The soil microbial community predicts the importance of plant traits in plant-soil feedback. New Phytol 206:329–341

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kong CH, Xu X, Zhou B, Hu F, Zhang C, Zhang M (2004) Two compounds from allelopathic rice accession and their inhibitory activity on weeds and fungal pathogens. Phytochemistry 65:1123–1128

    Article  CAS  PubMed  Google Scholar 

  • Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148

    Article  Google Scholar 

  • Larimer AL, Bever JD, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121:2090–2096

    Article  Google Scholar 

  • Larimer AL, Clay K, Bever JD (2014) Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95:1045–1054

    Article  PubMed  Google Scholar 

  • Legay N, Baxendale C, Grigulis K, Krainer U, Kastl E, Schloter M, Bardgett RD, Arnoldi C, Bahn M, Dumont M, Poly F, Pommier T, Clément JC, Lavorel S (2014) Contribution of above- and below-ground plant traits to the structure and function of grassland soil microbial communities. Ann Bot 114:1011–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leuchtmann A, Bacon CW, Schardl CL, White JF, Tadych M (2014) Nomenclatural realignment of Neotyphodium species with genus Epichloe. Mycologia 106:202–215

    CAS  PubMed  Google Scholar 

  • Levizou E, Karageorgou P, Petropoulou Y, Grammatikopoulos G, Manetas Y (2004) Induction of ageotropic response in lettuce radical growth by epicuticular flavonoid aglycones of Dittrichia viscosa. Biol Plant 48:305–307

    Article  CAS  Google Scholar 

  • Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320

    Article  Google Scholar 

  • Matthews JW, Clay K (2001) Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82:500–509

    Google Scholar 

  • Novas MV, Iannone LJ, Godeas AM, Scervino JM (2011) Evidence for leaf endophyte regulation of root symbionts: effect of Neotyphodium endophytes on the pre-infective state of mycorrhizal fungi. Symbiosis 55:19–28

    Article  Google Scholar 

  • Omacini M (2013) Asexual endophytes of grasses: invisible symbionts, visible imprints in the host neigbourhood. In: Verma VC, Gange AC (eds) Advances in endophytic research. Springer, India, pp. 143–157

    Google Scholar 

  • Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232

    Article  Google Scholar 

  • Omacini M, Semmartin M, Perez LI, Gundel PE (2012) Grass-endophyte symbiosis: a neglected aboveground interaction with multiple belowground consequences. Appl Soil Ecol 61:273–279

    Article  Google Scholar 

  • Ott T, van Dongen JT, Gu C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535

    Article  CAS  PubMed  Google Scholar 

  • Pérez LI, Gundel PE, Omacini M (2016) Can defensive mutualism between grasses and fungal endophytes protect non-symbiotic neighbours from soil pathogens? Plant Soil 405:289–298

    Article  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Ponce MA, Bompadre MJ, Scervino JM, Ocampo JA, Chaneton EJ, Godeas AM (2009) Flavonoids, benzoic acids and cinnamic acids isolated from shoots and roots of Italian rye grass (Lolium multiflorum lam.) with and without endophyte association and arbuscular mycorrhizal fungus. Biochem Syst Ecol 37:245–253

    Article  CAS  Google Scholar 

  • Quigley PE (2000) Effects of Neotyphodium lolii infection and sowing rate of perennial ryegrass (Lolium perenne) on the dynamics of ryegrass/subterranean clover (Trifolium subterraneum) swards. Aust J Agric Res 50:47–56.

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Rice EL (1984) Allelopathy. Academy Press, New York

    Google Scholar 

  • Rudgers JA, Clay K (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biology Reviews 21:107–124

    Article  Google Scholar 

  • Rudgers JA, Orr S (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97:247–255

    Article  Google Scholar 

  • Saikkonen K, Ruokolainen K, Huitu O, Gundel PE, Piltti T, Hamilton CE, Helander M (2013) Fungal endophytes help prevent weed invasions. Agric Ecosyst Environ 165:1–5

    Article  Google Scholar 

  • Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137

    Article  CAS  Google Scholar 

  • Slaughter LC, Carlisle AE, Nelson JA, McCulley RL (2016) Fungal endophyte symbiosis alters nitrogen source of tall fescue host, but not nitrogen fixation in co-occurring red clover. Plant Soil 405:243–256

    Article  CAS  Google Scholar 

  • Snell FJJ, Quigley PEE (1993) Allelopathic effects of endophyte in perennial ryegrass residues on young subterranean clover plants. In: Baker AM, Crush JR, Humpries LM (eds) Proceedings of the XVII International Grassland Congress. New Zealand Grassland Association, Palmerston North, pp. 343–344

    Google Scholar 

  • Springer TL (1996) Allelopathic effects on germination and seedling growth of clover by endophyte-free and -infected tall fescue. Crop Sci 36:1639–1642

    Article  Google Scholar 

  • Sutherland BL, Hoglund JH (1989) Effect of ryegrass containing the endophyte (Acremonium lolii) on the performance of associated white clover and subsequent crops. Proc New Zeal Grassl Assoc 50:265–269

  • Sutherland BL, Hume DE, Tapper BA (1999) Allelopathic effects of endophyte-infected perennial ryegrass extracts on white clover seedlings. N Z J Agric Res 42:19–26

    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 

  • Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276

    Article  Google Scholar 

  • Vázquez-de-Aldana BR, Romo M, García-Ciudad A, Petisco C, García-Criado B (2011) Infection with the fungal endophyte Epichloë festucae may alter the allelopathic potential of red fescue. Ann Appl Biol 159:281–290

    Article  Google Scholar 

  • Vignale MV, Iannone LJ, Pinget AD, De Battista JP, Novas MV (2016) Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 405:279–287

    Article  CAS  Google Scholar 

  • Walker C, Mize C, McNabb H Jr (1982) Populations of endogonaceous fungi at two locations in Central Iowa. Can J Bot 60:2518–2529

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Watson RN (1990) Effects of plant nematodes and Acremonium endophyte on white clover establishment with ryegrass or tall fesuce. Proceedings of the Forty Third New Zealand Weed and Pest Control Conference. pp 347–351

  • Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297

    Article  CAS  PubMed  Google Scholar 

  • Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Laura Ventura, Rudi Schäufele, Mirta M. Rabadán, for their technical assistance. Rizobacter Argentina S.A. (Pergamino, Argentina) generously donated rhizobial inoculants. We are grateful to Dr. Milena M. Manzur, the editor and three anonymous reviewers whose constructive comments on earlier versions improved the manuscript. P. G. P and M. D. are supported by postdoctoral fellowships from the National Council of Scientific and Technical Research (CONICET - Argentina). The study was supported by University of Buenos Aires, grants from ANPCyT (PICT 1525) and an international project cooperation from MINCyT (AL-1205, Argentina) - BMBF (01DN13006, Germany).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. A. García-Parisi.

Additional information

Responsible Editor: Etienne Laliberté.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Parisi, P.A., Lattanzi, F.A., Grimoldi, A.A. et al. Three symbionts involved in interspecific plant-soil feedback: epichloid endophytes and mycorrhizal fungi affect the performance of rhizobia-legume symbiosis. Plant Soil 412, 151–162 (2017). https://doi.org/10.1007/s11104-016-3054-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3054-3

Keywords

Navigation