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

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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.

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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.

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Authors and Affiliations

  1. IFEVA-Facultad de Agronomía (UBA)/CONICET, Cátedra de Ecología, Av. San Martín 4453, C1417DSE, Buenos Aires, Argentina

    L. I. Perez, P. E. Gundel, A. González Arzac & M. Omacini

  2. Instituto Argentino de Investigaciones de las Zonas Áridas, CONICET, CC 507, 5500, Mendoza, Argentina

    H. J. Marrero

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  1. L. I. Perez
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  2. P. E. Gundel
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  3. H. J. Marrero
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  4. A. González Arzac
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  5. M. Omacini
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Correspondence to L. I. Perez.

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Communicated by Katherine L. Gross.

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442_2017_3850_MOESM1_ESM.eps

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)

Supplementary material 2 (DOCX 13 kb)

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Perez, L.I., Gundel, P.E., Marrero, H.J. et al. Symbiosis with systemic fungal endophytes promotes host escape from vector-borne disease. Oecologia 184, 237–245 (2017). https://doi.org/10.1007/s00442-017-3850-3

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