Nonviable biomass of biocontrol agent Papiliotrema flavescens OH 182.9 3C enhances growth of Fusarium graminearum and counteracts viable biomass reduction of Fusarium head blight

Authors: Schisler, David; Yoshioka, Miho; Vaughan, Martha; Dunlap, Christopher; Rooney, Alejandro - Alex

Submitted to: Biological Control
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/11/2018
Publication Date: 10/1/2018
Citation: Schisler, D.A., Yoshioka, M., Vaughan, M.M., Dunlap, C.A., Rooney, A.P. 2018. Nonviable biomass of biocontrol agent Papiliotrema flavescens OH 182.9 3C enhances growth of Fusarium graminearum and counteracts viable biomass reduction of Fusarium head blight. Biological Control. 128:48-55. https://doi.org/10.1016/j.biocontrol.2018.09.006.
DOI: https://doi.org/10.1016/j.biocontrol.2018.09.006

Interpretive Summary: The use of microorganisms to biologically control diseases on agricultural crops continues to gain acceptance from producers and consumers but occasional inconsistent performance of biocontrol agents in reducing plant diseases is not well understood. ARS research scientists in Peoria, IL conducted experiments to determine if cells of the biocontrol yeast Papiliotrema flavescens OH 182.9 that die during product storage and/or during field application can counteract the beneficial effect of live antagonist cells. The scientists determined that live cells of the yeast caused spores of the pathogen that causes Fusarium head blight on wheat to be less effective in germinating and colonizing wheat tissue. However, this positive effect was largely negated when non-viable antagonist cells were mixed with the live cells. Dead antagonist cells supported pathogen growth in a liquid culture medium with no other source of carbon or nitrogen demonstrating that nutrients from dead cells are at least partially responsible for why dead antagonist cells reduce the biocontrol effect of live antagonist cells. Results suggest research to discover protocols for producing and formulating biocontrol cells with improved stress tolerance and shelf-life will minimize the proportion of dead cells present in formulated biocontrol products and therefore, biocontrol product inconsistency in reducing plant disease.

Technical Abstract: Microbially-based plant disease control products have achieved commercial market success, but the efficacy of biocontrol products is sometimes deemed inconsistent. Declines in product viability before or after application results in a mixture of non-viable and viable antagonist cells being present on infection courts. We hypothesized that these non-viable cells could provide a nutritive benefit to plant pathogen propagules and thereby reduce the efficacy and consistency of performance of a biocontrol product. We tested this hypothesis on the pathogen Fusarium graminearum, an important causal agent of Fusarium head blight (FHB) of wheat, and a yeast antagonist Papiliotrema flavescens (formerly Cryptococcus flavescens) strain OH 182.9 3C. When F. graminearum was grown in a liquid basal salts medium without carbon or nitrogen but supplemented with increasing levels of non-viable cells of strain OH 182.9 3C, the amount of pathogen biomass produced increased (P=0.05) with each sequentially higher level of non-viable cell amendment tested. Total conidial germination of F. graminearum on membranes was initially greatest in the control and least when conidia were combined with live cells of antagonist OH 182.9 3C. Though the presence of dead cells initially resulted in reduced conidial germination, the treatment increased bipolar germination of conidia after 6 h compared to the control (89% and 45%, respectively) (P=0.05, FPLSD). Treatment with a combination of dead and live cells supported more bipolar germination than live cells alone (51% and 29%, respectively). After 12 h, dead cells had a similar stimulating effect on the branching of germ tubes and negated the reduction in branching seen when treating with live cells alone. Scanning electron microscopy indicated that the presence of non-viable cells of P. flavescens OH 182.9 3C modified the ectotrophic growth of F. graminearum on wheat lemma tissues. In greenhouse experiments, live cells of P. flavescens tended to reduce FHB incidence, severity and the deoxynivalenol content of spring wheat grain compared to the control but treatment with live cells amended with dead cells increased all of these disease parameters compared to the live cells only treatment (P=0.05, FPLSD). Results indicate that non-viable antagonist cells present in a biocontrol cell treatment can reduce disease control efficacy or even cause the biocontrol treatment to support a net adverse effect on plant health.