A comprehensive characterization of ecological and epidemiological factors driving perennation of Podosphaera macularis chasmothecia

Authors: WELDON, WILLIAM - Cornell University; MARKS, MICHELLE - University Of Wisconsin; GEVENS, AMANDA - University Of Wisconsin; D'ARCANGELO, KIMBERLY - North Carolina State University; QUESADA-OCAMPO, LINA - North Carolina State University; PARRY, STEPHEN - Cornell University; Gent, David - Dave; Cadle-Davidson, Lance; GADOURY, DAVID - Cornell University

Submitted to: American Phytopathological Society
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/1/2021
Publication Date: 4/8/2021
Citation: Weldon, W.A., Marks, M.E., Gevens, A.J., D'Arcangelo, K., Quesada-Ocampo, L.M., Parry, S., Gent, D.H., Cadle Davidson, L.E., Gadoury, D.M. 2021. A comprehensive characterization of ecological and epidemiological factors driving perennation of Podosphaera macularis chasmothecia. American Phytopathological Society. https://doi.org/10.1094/PHYTO-11-20-0492-R.
DOI: https://doi.org/10.1094/PHYTO-11-20-0492-R

Interpretive Summary: Powdery mildew is an important disease of hop in most production areas in the Northern Hemisphere. A key aspect of disease ecology is how the fungus overwinters because this determines when, where, and to what extent the pathogen can infect crops in the following year. There are two potential means by which the hop powdery mildew fungus can overwinter: on living tissue of the host or in a dormant state in a hardy structure called a chasmothecium. In the Pacific Northwestern U.S. at present, the former means of overwintering is the only form of survival from year to year but this could change with a new introduction of the fungus. However, little work has been done to understand the latter means of overwintering and the implications for disease management. We report on a comprehensive set of studies that demonstrate conclusively that chasmothecia of the fungus are a viable overwintering source that can incite severe powdery mildew in spring. Two statistical models were developed to describe and predict when chasmotheica are likely to mature and discharge infectious spores. Separately, we report on studies that quantified the risk of introducing viable chasmothecia on hop seed and on dried hop cones. We found no evidence that the fungus can be transmitted to seedling plants via infested hop seed. However, we found that drying at temperatures of 51.7C or lower may permit a low levels of the fungus to survive the kilning process on infested host tissue. The totality of this research provides critical information and knowledge that can help producers better manage overwintering powdery mildew and guide sound practices and policies to reduce the likelihood of introducing the pathogen on dried cones.

Technical Abstract: Hop powdery mildew, caused by the ascomycete fungus Podosphaera macularis is a consistent threat to sustainable production. The pathogen utilizes two reproductive strategies for overwintering and perennation: (i) asexual vegetative hyphae on dormant hop buds that emerge the following season as infected shoots; or (ii) sexual ascocarps (chasmothecia) that house infectious ascospores, which presumably mature over winter and release on to newly emerged hop tissue the following spring. Little work has been done to understand the biological and epidemiological factors driving the winter maturation of P. macularis chasmothecia and subsequent spring release of ascospores within the context of North American hop production systems. Herein, this is the first study to confirm that P. macularis chasmothecia, in the absence of any asexual P. macularis growth forms, are a highly viable overwintering source that is capable of causing early season infection at levels between 31 – 78% incidence. Two distinct epidemiological models were defined that describe (i) P. macularis chasmothecial maturation, independent of overwintering geography; and (ii) the propensity for P. macularis ascosporic discharge in response to varying durations of rain and temperature. We found no evidence to support the possibility of introducing of P. macularis into new geographies via chasmothecia-infested hop seed, but ascospores did remain viable and infectious at very low, non-zero levels when exposed to temperatures at or below 51.7C, which resides within the lower-end of the post-harvest hop drying temperatures range. Overall, these tools and insights into pathogen ecology will directly improve early season management of hop powdery mildew in the presence of P. macularis chasmothecia.