Skip to main content
SpringerLink
Log in

Arbuscular mycorrhizal fungi can shift plant-soil feedback of grass-endophyte symbiosis from negative to positive

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

Abstract

Aims

Plants affect each other by modifying soils conditions in plant-soil feedbacks, where associated microbes have an integral role. Since epichloid endophytes and arbuscular mycorrhizal fungi (AMF) are highly widespread grass symbionts, here we explore the role of AMF and endophyte in plant-soil feedback within the same grass population.

Methods

Through a manipulative experiment, we evaluated the performance of endophyte-free and endophyte-associated Lolium multiflorum plants grown in soils previously conditioned by endophyte-free and endophyte-associated plants and inoculated or not with three AMF species.

Results

The biomass of endophyte-free and endophyte-associated plants was increased by AMF inoculation, when growing in soils conditioned by equal endophytic status plants (i.e. home soils). When growing in soils conditioned by plants with different endophytic status, plant biomass was higher than in home soil only in absence of AMF. The content of P and the arbuscular colonization also increased in plants growing in home soils.

Conclusion

We demonstrated that AMF shift the intraspecific feedback effects between E+ and E- conspecific plants from negative to positive. Furthermore, we found that the outcome of simultaneous occurrence of foliar and root symbionts on grass performance depends on the matching with the endophytic status of the previous plant.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Antunes PM, Miller J, Carvalho LM et al (2008) Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct Ecol 22:912–918. doi:10.1111/j.1365-2435.2008.01432.x

    Article  Google Scholar 

  • Arrieta AM, Iannone LJ, Scervino JM et al (2015) A foliar endophyte increases the diversity of phosphorus-solubilizing rhizospheric fungi and mycorrhizal colonization in the wild grass Bromus auleticus. Fungal Ecol 17:146–154. doi:10.1016/j.funeco.2015.07.001

    Article  Google Scholar 

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

    Google Scholar 

  • Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc B 269:2595–2601. doi:10.1098/rspb.2002.2162

    Article  PubMed  PubMed Central  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473. doi:10.1046/j.1469-8137.2003.00714.x

    Article  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. doi:10.2307/2960528

    Article  Google Scholar 

  • Bowatte S, Barrett B, Luscombe C et al (2011) Effect of grass species and fungal endophyte on soil nitrification potential. New Zeal J Agric Res 54:275–284. doi:10.1080/00288233.2011.606325

    Article  CAS  Google Scholar 

  • Breen JP (1994) Acremonium endophyte interactions with enhanced plant resistance to insects. Annu Rev Entomol 39:401–423. doi:10.1146/annurev.en.39.010194.002153

    Article  Google Scholar 

  • Brinkman EP, Van der Putten WH, Bakker E-J, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073

    Article  Google Scholar 

  • Buyer JS, Zuberer D, Nichols K, Franzluebbers AJ (2011) Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant Soil 339:401–412. doi:10.1007/s11104-010-0592-y

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/s11104-010-0607-8

    Article  CAS  Google Scholar 

  • Casas C, Gundel PE, Semmartin M et al (2016a) The enhancement of invasion ability of an annual grass by its fungal endophyte depends on recipient community structure. Biol Invasions 18:1853–1865. doi:10.1007/s10530-016-1129-y

    Article  Google Scholar 

  • Casas C, Torretta JP, Exeler N, Omacini M (2016b) What happens next? Legacy effects induced by grazing and grass-endophyte symbiosis on thistle plants and their floral visitors. Plant Soil 405:211–229. doi:10.1007/s11104-015-2644-9

    Article  CAS  Google Scholar 

  • Chu-Chou M, Guo B, An Z-Q et al (1992) Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol Biochem 24:633–637. doi:10.1016/0038-0717(92)90041-U

    Article  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. doi:10.1016/j.baae.2013.01.008

    Article  Google Scholar 

  • De Battista JP (2005) Neotyphodium research and application in South America. In: Roberts C, West C, Spiers D (eds) Neotyphodium in cool season grasses. Blackwell Publishing, Ames, pp 63–69

    Google Scholar 

  • Druille M, Cabello MN, García Parisi PA et al (2015) Glyphosate vulnerability explains changes in root-symbionts propagules viability in pampean grasslands. Agric Ecosyst Environ 202:48–55. doi:10.1016/j.agee.2014.12.017

    Article  CAS  Google Scholar 

  • Druille M, García-Parisi PA, Golluscio RA et al (2016) Repeated annual glyphosate applications may impair beneficial soil microorganisms in temperate grassland. Agric Ecosyst Environ 230:184–190. doi:10.1016/j.agee.2016.06.011

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks

  • Franzluebbers AJ (2006) Short-term responses of soil C and N fractions to tall fescue endophyte infection. Plant Soil 282:153–164. doi:10.1007/s11104-005-5447-6

    Article  CAS  Google Scholar 

  • García Parisi PA, Casas C, Gundel PE, Omacini M (2012) Consequences of grazing on the vertical transmission of a fungal Neotyphodium symbiont in an annual grass population. Austral Ecol 37:620–628. doi:10.1111/j.1442-9993.2011.02325.x

    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. doi:10.1111/oik.01540

    Article  Google Scholar 

  • García-Parisi PA, Lattanzi FA, Grimoldi AA et al (2017) 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. doi:10.1007/s11104-016-3054-3

  • 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. doi:10.1111/j.1469-8137.2005.01500.x

    Article  CAS  PubMed  Google Scholar 

  • Gundel PE, Batista WB, Texeira M et al (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. Proc R Soc B 275:897–905. doi:10.1098/rspb.2007.1494

    Article  PubMed  PubMed Central  Google Scholar 

  • Gundel PE, Garibaldi LA, Tognetti PM et al (2009) Imperfect vertical transmission of the endophyte Neotyphodium in exotic grasses in grasslands of the flooding pampa. Microb Ecol 57:740–748. doi:10.1007/s00248-008-9447-y

    Article  PubMed  Google Scholar 

  • Gundel PE, Garibaldi LA, Martinez-Ghersa MA, Ghersa CM (2011) Neotyphodium endophyte transmission to Lolium multiflorum seeds depends on the host plant fitness. Environ Exp Bot 71:359–366. doi:10.1016/j.envexpbot.2011.02.002

    Google Scholar 

  • Guo BZ, Hendrix JW, An Z-Q, Ferriss RS (1992) Role of Acremonium endophyte of fescue on inhibition of colonization and reproduction of mycorrhizal fungi. Mycologia 84:882–885. doi:10.2307/3760286

    Article  Google Scholar 

  • Hanson WC (1950) The photometric determination of phosphorus in fertilizers using the phosphovanado-molybdate complex. J Sci Food Agric 1:172–173. doi:10.1002/jsfa.2740010604

    Article  CAS  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. doi:10.1007/s11104-006-9141-0

    Article  CAS  Google Scholar 

  • Kardol P, Cornips NJ, van Kempen MM et al (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162. doi:10.1890/06-0502

    Article  Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. doi:10.1038/417067a

    Article  CAS  PubMed  Google Scholar 

  • Kong CH, Xu X, Zhou B et al (2004) Two compounds from allelopathic rice accession and their inhibitory activity on weeds and fungal pathogens. Phytochemistry 65:1123–1128. doi:10.1016/j.phytochem.2004.02.017

    Article  CAS  PubMed  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. doi:10.1111/j.1600-0706.2012.20153.x

    Article  Google Scholar 

  • Liu Q, Parsons AJ, Xue H et al (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus Spp. Fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol 25:910–920. doi:10.1111/j.1365-2435.2011.01853.x

    Article  Google Scholar 

  • Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320. doi:10.1111/j.2007.0030-1299.15973.x

    Article  Google Scholar 

  • Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil 227:115–126

    Article  CAS  Google Scholar 

  • Malinowski DP, Belesky DP, Hill NS et al (2008) Influence of phosphorus on the growth and ergot alkaloid content of Neotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb.) Plant Soil 198:53–61

    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, Cabral D, Godeas AM (2005) Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30

    Google Scholar 

  • Novas MV, Iannone LJ, Godeas AM, Cabral D (2009) Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol Prog 8:75–81. doi:10.1007/s11557-008-0579-8

    Article  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. doi:10.1007/s13199-011-0140-4

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM (2005) A hierarchical framework for understanding the ecosystem consequences of endofhyte-grass symbioses. In: Roberts C, West CP, Spiers DE (eds) Neotyphodium in cool-season grasses current research applications. Blackwell Publishing, Boston, pp 141–161

  • Omacini M, Eggers T, Bonkowski M et al (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232. doi:10.1111/j.1365-2435.2006.01099.x

    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. doi:10.1016/j.apsoil.2011.10.012

    Article  Google Scholar 

  • Pérez LI, Gundel PE, Omacini M (2016) Can the defensive mutualism between grasses and fungal endophytes protect non-symbiotic neighbours from soil pathogens? Plant Soil 405:289–298. doi:10.1007/s11104-015-2568-4

    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 55:158–163

    Article  Google Scholar 

  • Pinheiro JC, Bates D, DebRoy S et al (2015) {nlme}: Linear and Nonlinear Mixed Effects Models. R package version 3.1-121

  • Ponce M, Bompadre MJ, Scervino JM et al (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. doi:10.1016/j.bse.2009.03.010

    Article  CAS  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rasmussen S, Parsons AJ, Newman JA (2009) Metabolomics analysis of the Lolium perenne--Neotyphodium lolii symbiosis: more than just alkaloids? Phytochem Rev 8:535–550. doi:10.1007/s11101-009-9136-6

    Article  CAS  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. doi:10.1111/j.1365-2745.2008.01478.x

    Article  Google Scholar 

  • Rudgers JA, Koslow JM, Clay K (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol Lett 7:42–51. doi:10.1046/j.1461-0248.2003.00543.x

    Article  Google Scholar 

  • Van Der Putten WH, Van Dijk C, Peters B (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56. doi:10.1038/362053a0

    Article  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. doi:10.1111/1365-2745.12054

    Article  Google Scholar 

  • van der Putten WH, Bradford MA, Pernilla Brinkman E et al (2016) Where, when and how plant–soil feedback matters in a changing world. Funct Ecol 30:1109–1121. doi:10.1111/1365-2435.12657

    Article  Google Scholar 

  • Van Hecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:101–109. doi:10.1007/s11104-005-0380-2

    Article  Google Scholar 

  • Vignale MV, Iannone LJ, Pinget AD et al (2016) Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 405:279–287. doi:10.1007/s11104-015-2522-5

    Article  CAS  Google Scholar 

  • Wagg C, Boller B, Schneider S et al (2015) Intraspecific and intergenerational differences in plant–soil feedbacks. Oikos 124:994–1004. doi:10.1111/oik.01743

    Article  Google Scholar 

  • Zhou Y, Li X, Qin J et al (2016) Effects of simultaneous infections of endophytic fungi and arbuscular mycorrhizal fungi on the growth of their shared host grass Achnatherum Sibiricum under varying N and P supply. Fungal Ecol 20:56–65. doi:10.1016/j.funeco.2015.11.004

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Laura Ventura for her technical assistance with the conductance of the experiment and to Fabián Garello for his assistance with P determinations. We are grateful to Dr. Milena E. Manzur and three anonymous reviewers for their comments on the manuscript. P. G. P is supported by postdoctoral fellowships from the National Council of Scientific and Technical Research (CONICET - Argentina). The study was supported by University of Buenos Aires, and grants from ANPCyT (PICT 1525) and CONICET (PIP- 112 201301 00227).

Author information

Authors and Affiliations

  1. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos-CITNOBA, CONICET – UNNOBA, Monteagudo, 2772, Pergamino, Provincia de Buenos Aires, Argentina

    P. A. García-Parisi

  2. Universidad de Buenos Aires, Facultad de Agronomía, Deartamento de Producción Animal, Cátedra de Forrajicultura, Buenos Aires, Argentina

    P. A. García-Parisi

  3. CONCIET -Universidad de Buenos Aires, Facultad de Agronomía, Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA) - Departamento de Recursos Naturales y Ambiente, Cátedra de Ecología, Buenos Aires, Argentina

    M. Omacini

Authors
  1. P. A. García-Parisi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Omacini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. A. García-Parisi.

Additional information

Responsible Editor: Tatsuhiro Ezawa.

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., Omacini, M. Arbuscular mycorrhizal fungi can shift plant-soil feedback of grass-endophyte symbiosis from negative to positive. Plant Soil 419, 13–23 (2017). https://doi.org/10.1007/s11104-017-3216-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3216-y

Keywords

Search

Navigation