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A seed-recruited microbiome protects developing seedlings from disease by altering homing responses of Pythium aphanidermatum zoospores

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Abstract

Aims

We investigated potential mechanisms by which a seed microbiome recruited from vermicomposted dairy manure alters Pythium aphanidermatum zoospore mediated pathogenesis in cucumber.

Methods

Bioassays were conducted to measure arrival of zoospores at the seed surface via qPCR and subsequent seedling disease incidence. Seed exudates were collected at relevant time points for use in zoospore microscopy assays. Metabolomic analysis was used to characterize seed exudates.

Results

Microbes recruited by the germinating seed from a disease suppressive substrate within 8 hours of sowing prevented zoospore arrival at the seed surface, modified seed exudates and reduced disease incidence. In vitro exposure to microbially modified seed exudates altered zoospore homing responses and reduced both encystment and germination compared to control exudates. Combining modified and control exudates failed to restore zoospore attraction to levels observed with control exudates. Observed zoosporolytic activity of the modified exudates was unique to the ethyl acetate fraction and metabolomic analysis revealed several putative zoosporolytic compounds present at higher relative abundance when compared to control exudates.

Conclusions

The observed disease suppression was likely due to the production of a specific zoosporolytic compound or set of compounds in the spermosphere by one or more members of the seed-recruited vermicompost microbiome.

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Acknowledgements

The authors wish to thank Mary Ann Karp, Eric Carr, Monica Minson, Hilary Davis and Lauren Nelson for general technical support. Chemical fractionation of seed exudate samples: Donna Gibson, Bioassay apparatus and seedling photo credits: Kent Loeffler and Claire Smith, statistical consulting: Francoise Vermeylen, qPCR technical support: Eric Markel, manuscript feedback: Emilie Chapelle, Irene de Bruijn, Xu Cheng, Ellen Crocker and the anonymous reviewers for Plant and Soil.

This work was supported by grants from the USDA SBIR [2008-33610-19027 and 2009-33610-20277] as a subcontract to the USDA SBIR principal investigator Thomas Herlihy with matching funds to E. Nelson as principal investigator from NYSTAR CAT (http://www.biotech.cornell.edu/cat); the NY Farm Viability Institute (www.nyfvi.org), the Organic Farming Research Foundation (www.ofrf.org), and USDA NIFA Hatch Funds [NYC-153543]. Additional support was provided to ALH Jack as a scholarship from the Organic Crop Improvement Association (www.ocia.org) and an Andrew W. Mellon fellowship through the Cornell University College of Agriculture and Life Sciences (http://cals.cornell.edu/academics/student-research/graduate-grants-proposal/). Commercial metabolomic analysis was funded by RT Solutions, LLC (www.wormpower.net).

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  1. School of Integrative Plant Sciences, Section of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, New York, 14853, USA

    Allison L. H. Jack & Eric B. Nelson

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  1. Allison L. H. Jack
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  2. Eric B. Nelson
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Correspondence to Allison L. H. Jack.

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A. Jack had a consulting contract with RT Solutions, LLC from January 1, 2013 to January 31, 2013. No other conflicts to report.

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Responsible Editor: Matthieu Barret.

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Jack, A.L.H., Nelson, E.B. A seed-recruited microbiome protects developing seedlings from disease by altering homing responses of Pythium aphanidermatum zoospores. Plant Soil 422, 209–222 (2018). https://doi.org/10.1007/s11104-017-3257-2

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