I ECOLOGY and EPIDEMIOLOGY of PODOSPHAERA MACULARIS
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ECOLOGY AND EPIDEMIOLOGY OF PODOSPHAERA MACULARIS, THE CAUSAL AGENT OF HOP POWDERY MILDEW A Dissertation Presented to the Faculty of the Graduate School Of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by William Weldon August 2020 i © William Weldon ii ECOLOGY AND EPIDEMIOLOGY OF PODOSPHAERA MACULARIS, THE CAUSAL AGENT OF HOP POWDERY MILDEW William Weldon, Ph. D. Cornell University 2020 Over the past twenty years, hop production has expanded in parallel with the craft brewing industry, resulting in a high-value crop with low tolerance for defect in harvested hop cones. Podosphaera macularis is an ascomycete fungus that causes powdery mildew of hop, which is arguably the most destructive disease with respect to its potential for diminishing yield and cone quality. Historically, research on P. macularis has focused largely on the asexual growth forms of the pathogen, as that is the only phase currently observed in the Pacific Northwest (PNW) US region, where over 96% of US hop production resides. As such, the epidemiology and ecology of the disease with respect to the P. macularis ascigerous stage (chasmothecia) is not well understood, even though this growth form has been reported in most hop growing regions east of the Rocky Mountain range. Furthermore, due to the difficult- to-culture obligately biotrophic nature of the pathogen, there are relatively few molecular tools available to track P. macularis population structure and movement. As such, we developed a library of 54 high-throughput, cost effective amplicon sequencing (AmpSeq) molecular markers by re-purposing an existing transcriptome dataset as the source of genetic variation. While this marker design pipeline serves as a valuable template for generating similar marker libraries for other obligately-biotrophic or otherwise difficult to culture pathogens, the project also provided valuable insight into the current population structure of P. macularis throughout the US. Genotyping results indicate that the strains of P. macularis recently introduced into commercial hop yards throughout the Midwest and Eastern US have likely arrived via infected hop planting material, which harbors a PNW US derived P. macularis strain, as opposed to introductions occurring via wind-dispersal from nearby P. macularis iii populations residing on feral hop. This project also created a novel set of qPCR markers for P. macularis mating type, which were used to provide an updated distribution map of P. macularis mating types within the US. This dissertation also greatly improved understanding of P. macularis overwintering potential via chasmothecia, demonstrating that early season disease incidence can reach levels of up to 70% when conditions are favorable for ascosporic infection. A pair of regressions models were developed to improve the timing at which control measures are taken during the early spring growing season, with the first model predicting the window of chasmothecial maturation based upon degree day accumulation, and the second model assigning an ascosporic infection risk level to rain events based upon the temperature and duration of the precipitation. These studies on the epidemiology of the disease indicate that existing grower practices such as spring pruning, early season fungicide applications, and basal foliage removal are likely even more crucial when the ascigerous P. macularis growth form is present within a hop yard. iv BIOGRAPHICAL SKETCH William (Bill) Andrew Weldon was born and raised in Upper Arlington, Ohio and attended Butler University in Indianapolis, Indiana on both an academic and athletic (M- tennis) scholarship, where he earned a B.S. in Biology, with minors in Chemistry and Spanish. Bill was first introduced to biological research as an undergraduate at Butler in the lab of Dr. Philip Villani. An interest in plant pathology was then fully fostered during the summer of 2014 as an undergraduate summer research scholar in the lab of Dr. David Gadoury at Cornell University. His professional interests are in applied plant pathology, with a special focus on pathogen ecology, epidemiology, and population genetics. The translation of research findings into readily applicable disease management behaviors and strategies is incredibly important aspect of Bill’s research philosophy, and as such, the land grant mission and extension efforts will be inherently intertwined with any research undertakings during his career. Throughout his time at Cornell, he was a familiar face for the hop growers of New York, speaking at field meetings, grower conferences, and making numerous field visits to address individual disease management issues. Bill is highly active in the American Phytopathological Society. He has attended every annual meeting since 2015, delivering two symposium session oral presentations, two technical session oral presentations, and a suite of poster presentations during this time. He also served as vice-chair and chair of the APS Graduate Student Committee during 2018 and 2019. As chair, he led multiple initiatives focused on establishing novel, inclusive graduate student networking opportunities with the national society membership at large, as well as specifically within the agricultural industry sector. While at Cornell, he also mentored four undergraduate research scholars, all of whom have gone on to pursue a higher education degree in the field of plant pathology. Outside of research, he is an active individual that has a passion for athletics, especially tennis and football, as well as the outdoors. Over the past five years, you could frequently find Bill walking along the lakefront or in the numerous creeks of the Finger Lakes region with his loyal companion, a black Labrador retriever named Linus. v Dedicated to my mother and father, for their unwavering support in all that I pursue; and my grandmother, Anne Weldon, who was truly a saint in my life. vi ACKNOWLEDGEMENTS I am and will be eternally grateful to my graduate mentor, Dr. David M Gadoury, for the guidance that he has provided me throughout my time at Cornell University, which started in 2014, when I was a nervous undergraduate summer research intern still trying to pinpoint my passion within the field of Biology. He has opened countless doors for me to pursue almost any research direction of interest and has pushed me to extend my contributions to the field of plant pathology beyond scientific research and into service of the national well-being of the discipline as an active leader within the American Phytopathological Society. I will never again consider Lowe’s to be just a home improvement store, as at least a dozen times, David and I created custom pieces of equipment needed for various projects from loose items at Lowe’s. I also thank my committee member Dr. Lance E. Cadle-Davidson for his mentorship. He is one of the most creative and most compassionate scientists that I have ever met, and I have truly appreciated his presence during my graduate education. Thank you to Dr. David H. Gent, who, as a USDA Research Plant Pathologist located over 2,700 miles from Cornell University, went out of his way to welcome me into the hop pathology research world, making a sincere investment in my professional growth throughout my time as a graduate student. I seriously doubt that there is an adjunct member of a graduate student committee that has put forth more time and effort in a student than Dave has for me. Lastly, a profound thank you to Dr. Gregory M. Loeb and Dr. Stephen Reiners, my minor committee members for the fields of Entomology and Horticulture, respectively. They have both pushed me to grow as a scientist beyond the field of plant pathology and have served as shining examples for how to conduct extension at the highest level for Cornell University and the growers of New York. I also want to sincerely thank the members of the Gadoury, Cadle-Davidson, and Gent labs, past and present, for their support, collaboration, and friendship. A special thank you to Mary Jean Welser, who has been a kind, patient, and understanding pillar of support as the Gadoury laboratory technician upon which all lab members rely. I could not have successfully vii gotten through my graduate research projects without her presence. A second special thank you to Camille Sisto, who started in our lab as a high-school student mentee and has since progressed to take on a wide variety of technician roles within the lab. Again, I could not have successfully completed a lot of my field research without her help and positive spirit. Thank you to the undergraduates who assisted with this research and put up with me as I continued to work on my skills as a mentor – Michael Riga, Matthew Cullen, Teddy Borland, and Owen Washam. Thank you to the faculty and staff within the Plant Pathology and Plant-Microbe Biology section for their inspiration, especially Dr. Christine Smart, Holly Lange, Dr. William Fry, and Dr. Jason Londo. I am also extremely grateful to the Field Research Unit for their support during the design and execution of my various field trials, as well as Dr. Lina Quesada- Ocampo and Dr. Amanda Gevens for their willingness to collaborate on a multi-state pathogen overwintering project. I also want to acknowledge Dr. Philip Villani and Dr. Nathanael Hauck for their mentorship while I was an undergraduate student at Butler University. They are the true reason for my interest in plant pathology research and I owe the entirety of this journey that I have taken since then to those two scientists. Lastly, and more on a personal note, I extend a never-ending appreciation to the friendships that I have developed at Cornell, in particular Chase Crowell, Katrin Ayer, Chris Peritore, Elizabeth Cieniewicz, Angela Kruse, Michael Fulcher, and Greg Vogel. Our adventures have been some of the greatest joys of my life, and these people are huge part of what makes Cornell so special to me.