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Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass

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Abstract

Background and aims

Plants often establish multiple simultaneous symbiotic associations with different micro-organisms; however, the way in which each symbiont affects the other symbionts and the effects of these multiple interactions on plant performance are not well understood. The aim of this study was to evaluate how two different asexual Epichloë species modulate the establishment of arbuscular mycorrhizal fungi (AMF) in a wild forage grass under different soil fertilization levels.

Methods

We performed a completely randomized 12-month-long field experiment to evaluate the effect of two B. auleticus-endophyte ecotypes and two soil fertilization levels on the colonization of AMF, in seedlings and adult plants. Plant biomass and reproductive tillers production were also measured.

Results

The symbiosis, measured as the total extent of AM fungal colonization and frequency of arbuscules was significantly higher in Epichloë-infected plants and was not affected by fertilization either in seedlings or in adult plants. Plant biomass was increased by fertilization but no differences were observed due to the endophytic status. However, E+ plants produced more panicles than their E− counterparts.

Conclusions

Our findings strongly support the hypothesis of positive association between Epichloë endophytes and AMF in wild grasses, making this model important for agronomic improvement.

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References

  • Abbott L, Robson A (1979) A quantitative study of the spores and anatomy of mycorrhizas formed by a species of Glomus, with reference to its taxonomy. Aust J Bot 27:363–375

    Article  Google Scholar 

  • Afkhami ME, Rudgers JA (2008) Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am Nat 172:405–416

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Balzergue C, Puech-Pagès V, Bécard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 62:1049–1060

    Article  CAS  PubMed  Google Scholar 

  • Bernard E, Gwinn K, Pless C, Williver C (1997) Soil invertebrate species diversity and abundance in endophyte-infected tall fescue pastures. In: Bacon CW, Hill NS (eds) Neotyphodium/grass interactions. Springer, New York, pp 125–135

    Chapter  Google Scholar 

  • Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn AJ, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate‐polluted field site. New Phytol 166:981–992

    Article  CAS  PubMed  Google Scholar 

  • Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068

    Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  Google Scholar 

  • Cheplick GP, Faeth S (2009) Ecology and evolution of the grass-endophyte symbiosis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Chu-Chou M, Guo B, An ZQ, Hendrix J, Ferriss R, Siegel M, Dougherty C, Burrus P (1992) Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol Biochem 24:633–637

    Article  Google Scholar 

  • Clark E, White J, Patterson R (1983) Improved histochemical techniques for the detection of Acremonium coenophialum in tall fescue and methods of in vitro culture of the fungus. J Microbiol Methods 1:149–155

    Article  Google Scholar 

  • Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297

    Article  Google Scholar 

  • Di Rienzo JA, Guzmán AW, Casanoves F (2002) A multiple-comparisons method based on the distribution of the root node distance of a binary tree. J Agric Biol Environ Stat 7:129–142

    Article  Google Scholar 

  • Di Rienzo J, Casanoves F, Balzarini M, González L, Tablada M, Robledo C (2010) Grupo InfoStat. FCA, Universidad Nacional de Córdoba, Argentina

    Google Scholar 

  • Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C (2011) InfoStat versión 2011. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina

    Google Scholar 

  • Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett 7:304–313

    Article  Google Scholar 

  • Guo B, Hendrix J, An ZQ, Ferriss R (1992) Role of Acremonium endophyte of fescue on inhibition of colonization and reproduction of mycorrhizal fungi. Mycologia 84:882–885

    Article  Google Scholar 

  • Hosseini F, Mosaddeghi M, Hajabbasi M, Sabzalian M (2014) Aboveground fungal endophyte infection in tall fescue alters rhizosphere chemical, biological, and hydraulic properties in texture-dependent ways. Plant Soil:1–16

  • Iannone LJ, Cabral D (2006) Effects of the Neotyphodium endophyte status on plant performance of Bromus auleticus, a wild native grass from South America. Symbiosis 41:61–69

    Google Scholar 

  • Iannone LJ, Cabral D, Schardl CL, Rossi MS (2009) Phylogenetic divergence, morphological and physiological differences distinguish a new Neotyphodium endophyte species in the grass Bromus auleticus from South America. Mycologia 101:340–351

    Article  CAS  PubMed  Google Scholar 

  • Iannone LJ, Pinget AD, Nagabhyru P, Schardl CL, De Battista JP (2012) Beneficial effects of Neotyphodium tembladerae and Neotyphodium pampeanum on a wild forage grass. Grass Forage Sci 67:382–390

    Article  Google Scholar 

  • Ji YL, Zhan LH, Kang Y, Sun XH, Yu HS, Wang ZW (2009) A new stromata-producing Neotyphodium species symbiotic with clonal grass Calamagrostis epigeios (L.) Roth. grown in China. Mycologia 101:200–205

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908

    Article  Google Scholar 

  • Koulman A, Lane GA, Christensen MJ, Fraser K, Tapper BA (2007) Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 68:355–360

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (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

    Article  Google Scholar 

  • López-Ráez JA, Pozo MJ, García-Garrido JM (2011) Strigolactones: a cry for help in the rhizosphere. Botany 89:513–522

    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

    Article  Google Scholar 

  • Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940

    Article  CAS  Google Scholar 

  • Marulanda A, Azcon R, Ruiz Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533

    Article  CAS  Google Scholar 

  • Miranda JD, Harris P (2006) Effects of soil phosphorus on spore germination and hyphal growth of arbuscular mycorrhizal fungi. New Phytol 128:103–108

    Article  Google Scholar 

  • Miranda JD, Harris P, Wild A (1989) Effects of soil and plant phosphorus concentrations on vesicular‐arbuscular mycorrhiza in sorghum plants. New Phytol 112:405–410

    Article  Google Scholar 

  • Müller J (2003) Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Funct Plant Biol 30:419–424

    Article  Google Scholar 

  • Nagahashi G, Douds DD Jr (2011) The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biol 115:351–358

    Article  CAS  PubMed  Google Scholar 

  • Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus‐repressible and transcriptionally regulated. New Phytol 181:950–959

    Article  CAS  PubMed  Google Scholar 

  • Novas MV, Gentile A, Cabral D (2003) Comparative study of growth parameters on diaspores and seedlings between populations of Bromus setifolius from Patagonia, differing in Neotyphodium endophyte infection. Flora 198:421–426

    Article  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

    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

    Article  Google Scholar 

  • Oberhofer M, Leuchtmann A (2014) Horizontal transmission, persistence and competition capabilities of Epichloë endophytes in Hordelymus europaeus grass hosts using dual endophyte inocula. Fungal Ecol 11:37–49

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Otero P (2004) Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos 104:581–590

    Article  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 

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

    Article  Google Scholar 

  • Popay AJ (2009) Insect herbivory and defensive mutualisms between plants and fungi. In: White Jr J, Torres M (eds) Defensive mutualism in microbial symbiosis. Boca Raton, pp 347–358

  • Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik J (eds) Arbuscular mycorrhizas: physiology and Function, 2nd edn. Springer, Heidelberg, pp 193–208

    Chapter  Google Scholar 

  • Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte–grass literature. Trends Plant Sci 11:428–433

    Article  CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol Res 109:789–794

    Article  CAS  PubMed  Google Scholar 

  • Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340

    Article  CAS  PubMed  Google Scholar 

  • Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B (2013) Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 9, e1003323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert A, Hayman D (1986) Plant growth responses to vesicular arbuscular mycorrhiza. New Phytol 103:79–90

    Article  Google Scholar 

  • Simpson WR, Schmid J, Singh J, Faville MJ, Johnson RD (2012) A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne. Fungal Biol 116:234–240

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York

    Google Scholar 

  • Sylvia D, Neal L (1990) Nitrogen affects the phosphorus response of VA mycorrhiza. New Phytol 115:303–310

    Article  CAS  Google Scholar 

  • Tadych M, Ambrose KV, Bergen MS, Belanger FC, White JF Jr (2012) Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers 54:117–131

    Article  Google Scholar 

  • Trouvelot A (1986) Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methodes d’estimation ayant une significantion fonctionnelle. In: Gianinazzi‐Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221

    Google Scholar 

  • Vignale M, Astiz-Gassó M, Novas M, Iannone L (2013) Epichloid endophytes confer resistance to the smut Ustilago bullata in the wild grass Bromus auleticus (Trin.). Biol Control 67:1–7

    Article  Google Scholar 

  • White J Jr (1987) Widespread distribution of endophytes in the Poaceae. Plant Dis 71:340–342

    Article  Google Scholar 

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Acknowledgments

This paper is dedicated to the memory of J. P De Battista and we want to thank him for his support and his significant contribution to our research. This research was supported by the University of Buenos Aires UBACyT (2013-2016 20020120200059), CONICET (PIP 2012-2014 11220110100703) and ANPCyT (PICT 2011-1527), PROPLAME-PRHIDEB-CONICET: Publication n° 210.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Lab. de Micología, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires & PROPLAME-PRHIDEB CONICET, Av. Intendente Güiraldes 2160. Pab. II, 4° piso, Cdad.Universitaria, C1428EHA, Buenos Aires, Argentina

    M. Victoria Vignale, Leopoldo J. Iannone & M. Victoria Novas

  2. Departamento de Ingeniería Química, Facultad de Ingeniería, Universidad de Buenos Aires, Buenos Aires, Argentina

    Leopoldo J. Iannone

  3. EEA-INTA, Concepción del Uruguay, Entre Ríos, Argentina

    A. Daniela Pinget & Jose P. De Battista

Authors
  1. M. Victoria Vignale
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  2. Leopoldo J. Iannone
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  3. A. Daniela Pinget
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  4. Jose P. De Battista
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  5. M. Victoria Novas
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Corresponding author

Correspondence to M. Victoria Novas.

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Responsible Editor: Birgit Mitter.

Some months ago, Jose Pedro De Battista passed away

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Vignale, M.V., Iannone, L.J., Pinget, A.D. et al. Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 405, 279–287 (2016). https://doi.org/10.1007/s11104-015-2522-5

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