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Combining Applied and Basic Research Understanding the Powdery Mildew Disease of the Ornamental Plant Phlox: Combining Applied and Basic Research Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Coralie Farinas Graduate Program in Plant Pathology The Ohio State University 2020 Dissertation Committee Dr. Francesca Peduto Hand, Advisor Dr. Pablo S. Jourdan Dr. Thomas K. Mitchell Dr. Pierce A. Paul Dr. Jason C. Slot Copyrighted by Coralie Farinas 2020 1 Abstract The characterization of plant germplasm has tremendous potential to help address the many challenges that the field of plant health is facing, such as climate change continuously modifying the regions of previously known disease occurrence. The worldwide trade of the plant genus Phlox represents an important revenue for the horticultural industry. However, Phlox species are highly susceptible to the fungal disease powdery mildew (PM), and infected materials shipping across borders accelerate the risk of disease spread. Through collaboration with laboratories in the U.S., we investigated the genotypic and phenotypic diversity of a PM population to better understand its capacity to adapt to new environments and new resistant hosts. To do this, we developed tools to grow and study PM pathogens of Phlox in vitro, and then used whole genome comparison and multilocus sequence typing (MLST) analysis to study the genetic structure of the population. Additionally, we explored Phlox germplasm diversity to identify a range of plant responses to PM infection by comparing disease severity progression and length of latency period of spore production across a combination of Phlox species and PM isolates in vitro. Consistent with the literature, our results suggest that compared to most plant pathogenic fungi in the Ascomycota, Golovinomyces magnicellulatus, causal agent of PM, has larger genomes (about 130 Mb) with high repetitive content (about 40%) and a fewer number of protein-coding genes (about 8000). ii We found a lack of population structure and genetic diversity, despite diverse phenotypic responses to Phlox germplasm screening. Interestingly, we identified 7 putative secreted proteins, which are predicted to be involved in the infection process, that are differently distributed between the G. magnicellulatus genomes analyzed. We hypothesize that variation in predicted secreted proteins is at the basis of the differences observed in genetic and phenotypic diversity. Our results also suggest the presence of qualitative and quantitative resistant traits in Phlox germplasm. This research explored the genome variation and evolutionary potential of Phlox PM pathogens to infer durability of host resistance, which are key tools to face plant health’s future challenges. iii Acknowledgments First and foremost, I want to thank my mentor, Dr. Francesca Peduto Hand, whose guidance, trust, and hard work were key to this work and to achieving my goals. Similarly, I am grateful for the generous expertise and guidance offered by my committee members. Dr. Pablo S. Jourdan, Dr. Thomas K. Mitchell, Dr. Pierce A. Paul, and Dr. Jason C. Slot, thank you. I cannot emphasize enough how crucial the help of Justin Morse and Mike Kelly, the greenhouse managers, was to maintain a low thrip populations and low PM disease levels on my Phlox plants collection. I want to recognize all of my former and present lab members: the students, the technicians, and the post-docs who helped me collect the data and provided me with suggestions and guidance. Thank you, Maria Bellizzi, Isabel Emmanuel, Veena Devi Ganeshan, Nathan Grifford, Shan Lin, Dana Martin, Cristian Olmos, Caterina Villari, and Eric Warne. I also want to acknowledge the Ornamental Plant Germplasm Center staff who helped me maintain a micropropagated collection of Phlox species: Eric Renze and Andy Schenkel. I express my sincere gratitude to the Plant Pathology Department as a whole for the supportive and cohesive community that elevates one student to a well-rounded iv professional. The department offers mentoring, opportunities, and true friendship essential to one’s development. Last but certainly not least I thank my friends and family, and specifically Cécile Rémignon Randon, my mother, and Kevin M. Simmt, my partner in life. Their support was essential to the accomplishment of this work. While my mother’s support started more than 29 years ago, it still feels new, infinite, and unconditional. Kevin’s wisdom, kind words, and patience carried me through the happiest, and most tempestuous times. Thank you for building a world of love around my endeavors. v Vita Education Doctor of Philosophy The Ohio State University, 2015-2020 Major: Plant Pathology College of Food, Agriculture, and Environmental Sciences (CFAES) Minor: Public Policy and The John Glenn College of Public Affairs 2018-2019 Management Master of Science The Ohio State University, 2015-2017 Plant Pathology CFAES Bachelor University Montpellier 2, 2012-2013 Functional Plant Biology Faculty of Science, France Associate degree LEGTA Garcia Lorca, France 2009-2011 Horticultural Sciences Professional Experience American Phytopathological Society - Public Policy Board, 2019- 2021 United States Early Career Intern The Ohio State University, Department of Plant Pathology, 2015-2020 Columbus, OH Graduate Research Associate (Ph.D.) AmericanHort, Columbus, OH 2019 HortScholars Coordinator Tree Resistance Advocacy Group (TRAG), United States 2018 - Member The Ohio State University, Ornamental Plant Germplasm Center 2014-2015 (OPGC), Columbus, OH Research assistant Experimental Station SERAIL, Department of Agriculture, France 2013 Research assistant vi National Institute of Agronomy Research (INRA), France 2013 Intern Timbuk Farm, Granville, OH 2012 OSU exchange student Publications Peer-reviewed abstracts Farinas, C, Jourdan, P, Paul, PA, Daughtrey, ML, Peduto Hand, F. 2019. Phlox species have varied susceptibility to powdery mildew isolates from the Eastern United States. Phytopathology. Vol. 109:S2.91 Farinas, C, Peduto Hand, F. 2018. Development of laboratory bioassays to study powdery mildew pathogens of Phlox in vitro. Phytopathology. Vol. 108:S1.27. Farinas, C, Peduto Hand, F. 2017. Genotypic characterization of isolates of Golovinomyces magnicellulatus, the biotrophic powdery mildew pathogen of Phlox. Phytopathology. Vol. 107:S5.122. Peer-reviewed manuscripts Farinas, C., Peduto Hand, F. First report of Golovinomyces spadiceus causing powdery mildew on industrial hemp (Cannabis sativa L.) in Ohio. Submitted to Plant Dis. on 01/29/2020 (Under review). Farinas, C., Jourdan, P., Paul, P., Slot, J., Daughtrey, M., Devi Ganeshan, V., Baysal- Gurel, F., Peduto Hand, F. 2020. Phlox species show quantitative and qualitative resistance to a population of powdery mildew isolates from the eastern United States. Phytopathology. First Look https://doi.org/10.1094/PHYTO-12-19-0473-R vii Baysal-Gurel F., Farinas, C., Peduto Hand, F., Avin, F. 2020. First Report of Powdery Mildew of Phlox Caused by Golovinomyces magnicellulatus in Tennessee. Plant Dis. First Look https://apsjournals.apsnet.org/doi/10.1094/PDIS-11-19-2498-PDN Bonello, P., Campbell, F., Cipollini, D., Conrad, A., Farinas, C., Gandhi, KJ.K., Hain, F., Parry, D., Showalter, D., Villari, C Wallin, K. F. 2020. Invasive tree pests devastate ecosystems–A proposed new response framework. Frontiers in Forests and Global Change. 3, 2. Farinas, C., Gluck-Thaler, E., Slot, J. C., & Hand, F. P. 2019. Whole-Genome Sequence of the Phlox Powdery Mildew Pathogen Golovinomyces magnicellulatus Strain FPH2017-1. Microbiology Resource Announcements, 8(36), e00852-19. Emanuel, IB, Farinas, C, Lin, S, Pyerzynski, J., Crouch, JA, Peduto Hand, F. 2019. “Occurrence of boxwood blight caused by Calonectria pseudonaviculata in Ohio landscapes”. Plant Dis. 103(10): 2670. Farinas, C., Jourdan, P., Paul, P.A., Peduto Hand, F. 2019. Development and evaluation of laboratory bioassays to study powdery mildew pathogens of Phlox in vitro. Plant Dis. 103(7):1536-1543 Farinas, C., Villari, C, Martin, D, Taylor, NJ, Peduto Hand, F. 2016. Magnaporthe oryzae perennial ryegrass pathotype causes leaf spots and blight on Japanese forest grass in Ohio. Plant Dis.101(3): 507 viii Editor-reviewed articles Farinas, C., Henderson, E., Peduto Hand, N. 2020. Evaluation of foliar fungicides in a preventative or curative program to control powdery mildew on garden Phlox, 2019. Plant Dis. Management Reports Vol. 14, OT009. Farinas, C., Gifford, N., Peduto Hand, N. 2017. Evaluation of foliar fungicide applications to control powdery mildew on garden phlox. Plant Dis. Management Reports Vol. 11, OT017. Fields of Study Major Field: Plant Pathology ix Table of Contents Abstract ............................................................................................................................... ii Acknowledgments.............................................................................................................. iv Vita ..................................................................................................................................... vi Table of Contents ................................................................................................................ x List of Tables .................................................................................................................... xii List of Figures .................................................................................................................
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