Oecologia

, Volume 184, Issue 1, pp 237–245 | Cite as

Symbiosis with systemic fungal endophytes promotes host escape from vector-borne disease

  • L. I. Perez
  • P. E. Gundel
  • H. J. Marrero
  • A. González Arzac
  • M. Omacini
Community ecology – original research

Abstract

Plants interact with a myriad of microorganisms that modulate their interactions within the community. A well-described example is the symbiosis between grasses and Epichloë fungal endophytes that protects host plants from herbivores. It is suggested that these symbionts could play a protective role for plants against pathogens through the regulation of their growth and development and/or the induction of host defences. However, other endophyte-mediated ecological mechanisms involved in disease avoidance have been scarcely explored. Here we studied the endophyte impact on plant disease caused by the biotrophic fungus, Claviceps purpurea, under field conditions through (1) changes in the survival of the pathogen´s resistance structure (sclerotia) during overwintering on the soil surface, and (2) effects on insects responsible for the transportation of pathogen spores. This latter mechanism is tested through a visitor exclusion treatment and the measurement of plant volatile cues. We found no significant effects of the endophyte on the survival of sclerotia and thus on disease inocula. However, both pathogen incidence and severity were twofold lower in endophyte-symbiotic plants than in non-symbiotic ones, though when insect visits were prevented this difference disappeared. Endophyte-symbiotic and non-symbiotic plots presented different emission patterns of volatiles suggesting that they can play a role in this protection. We show a novel indirect ecological mechanism by which endophytes can defend host grasses against diseases through negatively interacting with intermediary vectors of the epidemic process.

Keywords

Mutualism Pathogen transmission Disease avoidance VOCs Epichloë occultans 

Notes

Acknowledgements

In loving memory of Professor Rolando J.C. León. Diego Vazquez and Amy Austin provided useful comments on earlier versions of the manuscript. This work was funded by the University of Buenos Aires (UBA), the National Research Council (CONICET) and the National Scientific and Technological Promotion (FONCYT). L.I.P. holds a Research Scholarship from the National Research Council of Argentina.

Author contribution statement

LIP, MO and PEG conceived and designed the experiments. LIP, AGA and HJM performed the experiments. LIP and AGA analyzed the data. LIP wrote the manuscript and all authors provided editorial advice.

Supplementary material

442_2017_3850_MOESM1_ESM.eps (3.1 mb)
Fig. S1 (a) Schematic drawing showing the arrangement of sixteen 0.7 × 0.7 m plots in eight blocks of two plots each, sown with symbiotic or non-symbiotic seeds (E+ and E−, respectively). (b) Six white tulle bags containing pathogen sclerotia (10 units) were placed on the soil surface in the plots established for evaluation Pre-infection mechanisms of endophytes on disease. From the six sclerotia bags placed in each plot, one-third was covered with 10 × 10 cm mesh bags (2 mm mesh size) containing 4 g of litter biomass produced by E+ plants (L+); another third, with bags containing 4 g of litter produced by E− plants (L−); and the remaining third with empty bags (L0). (c) Vector exclusion treatment was established in order to evaluate Infection-related mechanisms of endophytes on disease. Prior to anthesis, each plot was randomly divided in halves. All the spikes from one of the subplots were covered with white tulle bags to keep insects out; spikes from the other subplot were grouped simulating the effect of bagging but allowing arthropod vectors to visit the plants (V− and V+, respectively). Supplementary material 1 (EPS 3193 kb)
442_2017_3850_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 13 kb)

References

  1. Afkhami ME, Rudgers JA, Stachowicz JJ (2014) Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology 95:833–844. doi: 10.1890/13-1010.1 CrossRefPubMedGoogle Scholar
  2. Alderman SC (1993) Aerobiology of Claviceps purpurea in Kentucky bluegrass. Plant Dis 77:1045–1049CrossRefGoogle Scholar
  3. 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 22:912–918CrossRefGoogle Scholar
  4. Bacon CW, White JFJ (1994) Stains, media, and procedures for analyzing endophytes. CRC Press, Boca RatonGoogle Scholar
  5. Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030CrossRefGoogle Scholar
  6. Birgander J, Rousk J, Olsson PA (2014) Comparison of fertility and seasonal effects on grassland microbial communities. Soil Biol Biochem 76:80–89CrossRefGoogle Scholar
  7. Borer ET, Hosseini PR, Seabloom EW, Dobson AP (2007) Pathogen-induced reversal of native dominance in a grassland community. Proc Natl Acad Sci USA 104:5473–5478CrossRefPubMedPubMedCentralGoogle Scholar
  8. Branca A, Simonian P, Ferrante M, Novas E, Negri RM (2003) Electronic nose based discrimination of a perfumery compound in a fragrance. Sens Actuators B 92:6CrossRefGoogle Scholar
  9. 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 339:401–412CrossRefGoogle Scholar
  10. Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340:347–355CrossRefGoogle Scholar
  11. Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890. doi: 10.1111/ele.12279 CrossRefPubMedGoogle Scholar
  12. Clarke BB, White JF Jr, Hurley RH, Torres MS, Sun S, Huff DR (2006) Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Dis 90:994–998CrossRefGoogle Scholar
  13. Clay K (1993) The ecology and evolution of endophytes. Agr Ecosyst Environ 44:39–64CrossRefGoogle Scholar
  14. Clay K (1996) Interactions among fungal endophytes, grasses and herbivores. Res Popul Ecol 38:191–201CrossRefGoogle Scholar
  15. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127CrossRefPubMedGoogle Scholar
  16. Crossley DA Jr, Blair JM (1991) A high-efficiency, “low-technology” Tullgren-type extractor for soil microarthropods. Agr Ecosyst Environ 34:187–192. doi: 10.1016/0167-8809(91)90104-6 CrossRefGoogle Scholar
  17. Dabkevičius Z, Mikaliunaite R (2006) The effect of fungicidal seed treaters on germination of rye ergot (Claviceps purpurea (Fr.) Tul.) sclerotia and on ascocarp formation. Crop Prot 25:677–683CrossRefGoogle Scholar
  18. D’Alessandro M, Turlings TC (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24–32CrossRefPubMedGoogle Scholar
  19. Elmi AA, West CP, Robbins RT, Kirkpatrick TL (2000) Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Sci 55:166–172CrossRefGoogle Scholar
  20. Feldman TS, O’Brien HE, Arnold AE (2008) Moths that vector a plant pathogen also transport endophytic fungi and mycoparasitic antagonists. Microb Ecol 56:742–750CrossRefPubMedGoogle Scholar
  21. García Parisi PA, Grimoldi AA, Omacini M (2014) Endophytic fungi of grasses protect other plants from aphid herbivory. Fungal Ecol 9:61–64. doi: 10.1016/j.funeco.2014.01.004 CrossRefGoogle Scholar
  22. Gill HK, McSorley R (2010) Effect of integrating soil solarization and organic mulching on the soil surface insect community. Florida Entomol 93:308–309. doi: 10.1653/024.093.0224 CrossRefGoogle Scholar
  23. Gorischek AM, Afkhami ME, Seifert EK, Rudgers JA (2013) Fungal symbionts as manipulators of plant reproductive biology. Am Nat 181:562–570CrossRefPubMedGoogle Scholar
  24. Gundel PE, Garibaldi LA, Martínez-Ghersa MA, Ghersa CM (2012) Trade-off between seed number and weight: influence of a grass–endophyte symbiosis. Basic Applied Ecol 13(1):32–39. doi: 10.1016/j.baae.2011.10.008 CrossRefGoogle Scholar
  25. Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10CrossRefGoogle Scholar
  26. Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–385CrossRefPubMedGoogle Scholar
  27. Johnston WJ, Golob CT, Sitton JW, Schultz TR (1996) Effect of temperature and postharvest field burning of Kentucky bluegrass on germination of sclerotia of Claviceps purpurea. Plant Dis 80:766–768CrossRefGoogle Scholar
  28. Kunkel BA, Grewal PS, Quigley MF (2004) A mechanism of acquired resistance against an entomopathogenic nematode by Agrotis ipsilon feeding on perennial ryegrass harboring a fungal endophyte. Biol Control 29:100–108CrossRefGoogle Scholar
  29. Lemons A, Clay K, Rudgers JA (2005) Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia 145:595–604CrossRefPubMedGoogle Scholar
  30. Li T, Blande JD, Gundel PE, Helander M, Saikkonen K (2014) Epichloë endophytes alter inducible indirect defences in host grasses. PLoS One 9:e101331. doi: 10.1371/journal.pone.0101331 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  32. Marrero HJ, Torretta JP, Medan D (2014) Effect of land use intensification on specialization in plant–floral visitor interaction networks in the Pampas of Argentina. Agr Ecosyst Environ 188:63–71. doi: 10.1016/j.agee.2014.02.017 CrossRefGoogle Scholar
  33. Matthews JW, Clay K (2001) Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82:500–509. doi:10.1890/0012-9658(2001)082[0500:IOFEIO]2.0.CO;2Google Scholar
  34. McLaren NW, Flett BC (1998) Use of weather variables to quantify sorghum ergot potential in South Africa. Plant Dis 82:26–29CrossRefGoogle Scholar
  35. Mitchell CE et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740CrossRefPubMedGoogle Scholar
  36. Neal PR, Anderson GJ (2004) Does the ‘old bag’ make a good ‘wind bag’?: comparison of four fabrics commonly used as exclusion bags in studies of pollination and reproductive biology. Ann Bot 93:603–607CrossRefPubMedPubMedCentralGoogle Scholar
  37. Newton AC, Fitt BDL, Atkins SD, Walters DR, Daniell TJ (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol 18:365–373. doi: 10.1016/j.tim.2010.06.002 CrossRefPubMedGoogle Scholar
  38. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81CrossRefPubMedGoogle Scholar
  39. 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 20:226–232CrossRefGoogle Scholar
  40. Omacini M, Chaneton E, Ghersa C (2007) Neotyphodium impacts on soil nematode communities: Rhizosphere-and litter-mediated interactions Proc. 6th Int Symp Fungal Endophytes Grasses. Grassl Res Practice Series, vol. 13, pp 107–110Google Scholar
  41. Omacini M, Chaneton EJ, Bush L, Ghersa CM (2009) A fungal endosymbiont affects host plant recruitment through seed- and litter-mediated mechanisms. Funct Ecol 23:1148–1156CrossRefGoogle Scholar
  42. Omacini M, Semmartin M, Pérez LI, Gundel PE (2012) Grass-endophyte symbiosis: a neglected aboveground interaction with multiple belowground consequences. Appl Soil Ecol 61:273–279CrossRefGoogle Scholar
  43. Pańka D, West CP, Guerber CA, Richardson MD (2013) Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte symbiosis. Ann Appl Biol 163:257–268CrossRefGoogle Scholar
  44. Pérez LI, Gundel PE, Ghersa CM, Omacini M (2013) Family issues: fungal endophyte protects host grass from the closely related pathogen Claviceps purpurea. Fungal Ecol 6:379–386. doi: 10.1016/j.funeco.2013.06.006 CrossRefGoogle Scholar
  45. Prom LK, Isakeit T (2003) Laboratory, greenhouse, and field assessment of fourteen fungicides for activity against Claviceps africana, causal agent of sorghum ergot. Plant Dis 87:252–258CrossRefGoogle Scholar
  46. Prom LK, Lopez JD Jr (2004) Viability of Claviceps africana spores ingested by adult corn earworm moths, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae). J Econ Entomol 97:764–767CrossRefPubMedGoogle Scholar
  47. Prom LK, Lopez JD Jr, Mayalagu GP (2005) Passive transmission of sorghum ergot (Claviceps africana) by four species of adult stink bugs. Southwest Entomol 30:29–34Google Scholar
  48. Rius M, Potter EE, Aguirre JD, Stachowicz JJ (2014) Mechanisms of biotic resistance across complex life cycles. J Anim Ecol 83:296–305CrossRefPubMedGoogle Scholar
  49. Rojas X, Guo J, Leff JW, McNear DH, Fierer N, McCulley RL (2016) Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities. Microb Ecol 72:197–206. doi: 10.1007/s00248-016-0750-8 CrossRefPubMedGoogle Scholar
  50. Rúa MA, McCulley RL, Mitchell CE (2013) Fungal endophyte infection and host genetic background jointly modulate host response to an aphid-transmitted viral pathogen. J Ecol 101:1007–1018CrossRefGoogle Scholar
  51. Rudgers JA, Clay K (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecol Lett 11:831–840CrossRefPubMedGoogle Scholar
  52. Rudgers JA, Orr S (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97:247–255CrossRefGoogle Scholar
  53. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  54. Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968. doi: 10.1007/s10886-013-0310-3 CrossRefPubMedGoogle Scholar
  55. Schardl CL, Leuchtmann A (2004) Spiering MJ. Symbioses of grasses with seedborne fungal endophytes 55:315–340Google Scholar
  56. Schardl CL et al (2013) Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 9:e1003323. doi: 10.1371/journal.pgen.1003323 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Schiestl FP et al (2006) Evolution of ‘pollinator’-attracting signals in fungi. Biol Let 2:401–404CrossRefGoogle Scholar
  58. Soriano A (1992) Río de la Plata Grasslands. Elsevier, AmsterdamGoogle Scholar
  59. Szpeiner A, Martínez-Ghersa MA, Ghersa CM (2009) Wheat volatile emissions modified by top-soil chemical characteristics and herbivory alter the performance of neighbouring wheat plants. Agr Ecosyst Environ 134:99–107CrossRefGoogle Scholar
  60. Telleria MC (1996) Plant resources foraged by Polybia scutellaris (Hym. Vespidae) in the Argentine pampas. Grana 35:302–307CrossRefGoogle Scholar
  61. Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2007) Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 22:120–126CrossRefPubMedGoogle Scholar
  62. Tian P, Nan Z, Li C, Spangenberg G (2008) Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. Eur J Plant Pathol 122:593–602CrossRefGoogle Scholar
  63. Tognetti P, Chaneton E (2012) Invasive exotic grasses and seed arrival limit native species establishment in an old-field grassland succession. Biol Invasions 14:2531–2544. doi: 10.1007/s10530-012-0249-2 CrossRefGoogle Scholar
  64. Vignale MV, Astiz-Gassó MM, Novas MV, Iannone LJ (2013) Epichloid endophytes confer resistance to the smut Ustilago bullata in the wild grass Bromus auleticus (Trin.). Biol Control 67:1–7. doi: 10.1016/j.biocontrol.2013.06.002 CrossRefGoogle Scholar
  65. Waldrop MP, Firestone MK (2006) Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb Ecol 52:470–479CrossRefPubMedGoogle Scholar
  66. Wäli PR, Helander M, Nissinen O, Saikkonen K (2006) Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Can J Bot 84:1043–1051CrossRefGoogle Scholar
  67. Wäli PP, Wäli PR, Saikkonen K, Tuomi J (2013) Is the pathogenic ergot fungus a conditional defensive mutualist for its host grass? PLoS One 8(7):e69249. doi: 10.1371/journal.pone.0069249 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Welty RE, Barker RE, Azevedo MD (1991) Reaction of tall fescue infected and noninfected by Acremonium coenophialum to Puccinia graminis subsp. graminicola. Plant Dis 75:883–886CrossRefGoogle Scholar
  69. West CP, Gwinn KD (1993) Role of Acremonium in drought, pest, and disease tolerances of grasses 2nd International symposium Acremonium/grass interactions. AG Research, Hamilton, pp 131–140Google Scholar
  70. West CP, Izekor E, Oosterhuis DM, Robbins RT (1988) The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 112:3–6CrossRefGoogle Scholar
  71. Yue Q, Miller CJ, White JF Jr, Richardson MD (2000) Isolation and characterization of fungal inhibitors from Epichloe festucae. J Agric Food Chem 48:4687–4692CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • L. I. Perez
    • 1
  • P. E. Gundel
    • 1
  • H. J. Marrero
    • 2
  • A. González Arzac
    • 1
  • M. Omacini
    • 1
  1. 1.IFEVA-Facultad de Agronomía (UBA)/CONICET, Cátedra de Ecología, Av. San Martín 4453Buenos AiresArgentina
  2. 2.Instituto Argentino de Investigaciones de las Zonas Áridas, CONICETMendozaArgentina

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