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1 Etiology, Epidemiology and Management of Fruit Rot Of Etiology, Epidemiology and Management of Fruit Rot of Deciduous Holly in U.S. Nursery Production Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Shan Lin Graduate Program in Plant Pathology The Ohio State University 2018 Dissertation Committee Dr. Francesca Peduto Hand, Advisor Dr. Anne E. Dorrance Dr. Laurence V. Madden Dr. Sally A. Miller 1 Copyrighted by Shan Lin 2018 2 Abstract Cut branches of deciduous holly (Ilex spp.) carrying shiny and colorful fruit are popularly used for holiday decorations in the United States. Since 2012, an emerging disease causing the fruit to rot was observed across Midwestern and Eastern U.S. nurseries. A variety of other symptoms were associated with the disease, including undersized, shriveled, and dull fruit, as well as leaf spots and early plant defoliation. The disease causal agents were identified by laboratory processing of symptomatic fruit collected from nine locations across four states over five years by means of morphological characterization, multi-locus phylogenetic analyses and pathogenicity assays. Alternaria alternata and a newly described species, Diaporthe ilicicola sp. nov., were identified as the primary pathogens associated with the disease, and A. arborescens, Colletotrichum fioriniae, C. nymphaeae, Epicoccum nigrum and species in the D. eres species complex were identified as minor pathogens in this disease complex. To determine the sources of pathogen inoculum in holly fields, and the growth stages of host susceptibility to fungal infections, we monitored the presence of these pathogens in different plant tissues (i.e., dormant twigs, mummified fruit, leaves and fruit), and we studied inoculum dynamics and assessed disease progression throughout the growing season in three Ohio nurseries exposed to natural inoculum over two consecutive years. Additionally, an outdoor container trial was conducted by artificially inoculating plant tissues using individual or combined pathogen inoculum at different stages of plant development (i.e., flower bud, full bloom, petal fall, immature fruit and mature fruit). In ii nursery conditions, fruit rot pathogens were consistently isolated from all types of plant tissues analyzed. Mummified fruit and bark were found to be the main sources of primary inoculum, while leaf spots were identified as a source of secondary inoculum for fruit infections. Alternaria and Colletotrichum had significantly higher isolation frequency after bloom, and peak inoculum capture by spore traps was observed during bloom. In the container trial, Diaporthe ilicicola inoculations during bloom and petal fall stages resulted in latent infections with symptoms developing when fruit reached maturity. In addition, all pathogens successfully infected mature wounded fruit. These results indicate that bloom is a critical stage to manage fruit infections and that implementing practices for fruit injury protection may lower disease levels in the field. This research represent the first step to understand this emerging fruit rot on deciduous holly and to build a foundation for further investigations. Further studies should be conducted to fully understand the effects of environmental parameters on seasonal inoculum dynamics and of host physiological factors contributing to disease development. iii Dedication In memory of my grandmother, Cuifang Liu, whose endless love and support encouraged me to be brave, strong, and to be myself. iv Acknowledgments I would like to express my sincere gratitude to my life-time advisor, Dr. Francesca Peduto Hand for your guidance and support in the past six years since the establishment of your lab. Your wisdom and trust not only encouraged me to become a plant pathologist, but also to become a confident grown-up. How lucky I am to have had you as my advisor! Being your student is one of the best decisions made in my life! I would like to thank my advisory committee members, Dr. Anne Dorrance, Dr. Larry Madden and Dr. Sally Miller, for their guidance and constructive feedback throughout my research. I thank all the faculty, students, and staff in the Department of Plant Pathology, especially Dr. Jason Slot and Emile Gluck-Thaler for their tremendous help on the description of the new Diaporthe species. Special thanks to Dr. Tom Mitchell, Dr. Monica Lewandowski, Jim Chatfield, Dr. Peg McMahon from the Department of Horticulture & Crop Science, as well as Mary Maloney from Chadwick Arboretum, whose enthusiasm and help made me spend a wonderful undergraduate time at Ohio State and become passionate about my dreams. Many thanks to Dr. F. P. Trouillas for assistance with the new species description, and Drs. J. R. Úrbez-Torres and G. Marchi for constructive feedback on my research manuscripts prior to submission. Additionally I would like to thank all the growers in Ohio, Pennsylvania, and Massachusetts who provided fruit samples and field plots to conduct my research trials. v Many, many, thanks to all the members of the Hand Lab: Coralie Farinas and Isabel Emanuel; former members Caterina Villari, Dana Martin, Maria Bellizzi, Veena Devi-Ganeshan; and the undergraduate students Paige Thrush, Nathan Gifford, Jenna Moore, Eric Warne, and Sumner Lonseth, for their help in so many ways. Without you, I would have not been able to finish my PhD. Last but not the least, I want thank my family and friends for their unconditional support and love. Thank you for always being by my side! vi Vita 2013…………………………………. B.S. Agriculture, The Ohio State University, Magna cum laude 2017.………………………………….M.S. Plant Pathology, The Ohio State University 2014-present………………………….Graduate Research Associate, Department of Plant Pathology, The Ohio State University Publications Lin, S., and Peduto Hand, F. 2018. Determining the effects of inoculum concentration and wounding on the development of fruit rot of winterberry holly. Phytopathology 108:S1.183. Lin S., and Peduto Hand, F. 2018. Investigations on the timing of fruit infection by fungal pathogens causing fruit rot of deciduous holly. Plant Disease First Look, retrieved from https://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS-06-18-0973-RE. Lin S., Taylor, N. J., and Peduto Hand, F. 2018. Identification and characterization of fungal pathogens causing fruit rot of deciduous holly. Plant Disease 102:2430-2445. Lin, S., Martin, D. E., Taylor, N. J., Gabriel, C. K., Devi Ganeshan, V., and Peduto Hand F. 2018. First report of Phytophthora aerial blight caused by Phytophthora nicotianae on Vinca, Lobelia and Calibrachoa in Ohio. Plant Disease 102:456. vii Lin, S., Taylor, N. J., and Peduto Hand, F. 2017. Determining the timing of host susceptibility to infection by fungal pathogens associated with fruit rot disease of winterberry holly. Phytopathology 107:S5.34. Lin, S., Martin, D. E., Taylor, N. J., Gabriel, C. K., and Peduto Hand F. 2017. Occurrence of Phytophthora chrysanthemi causing root and stem rot on garden mums in the United States. Plant Disease 101:1060. Lin, S., Taylor, N. J., and Peduto Hand, F. 2016. Identifying sources of inoculum and timing of tissue infection by fungal pathogens associated with winterberry fruit rot. Phytopathology 106:S4.3. Lin, S., Peduto Hand, Taylor, N.J., and Zondag, R. H. 2015. Understanding the emergent fruit rot disease of Winterberry holly. Phytopathology 105:S4.109. Fields of Study Major Field: Plant Pathology viii Table of Contents Abstract ............................................................................................................................... ii Dedication .......................................................................................................................... iv Acknowledgments............................................................................................................... v Vita .................................................................................................................................... vii List of Tables ..................................................................................................................... xi List of Figures .................................................................................................................. xiii Chapter 1: Introduction ................................................................................................... 1 1.1 THE FLORICULTURE INDUSTRY IN THE UNITED STATES ......................... 1 1.2 USE OF ILEX SPP. IN ORNAMENTAL PLANT PRODUCTION ........................ 3 1.3 FRUIT ROT: AN EMERGING DISEASE OF DECIDUOUS HOLLY .................. 8 1.4 OBJECTIVES ......................................................................................................... 15 Chapter 2: Identification and Characterization of Fungal Pathogens Causing Fruit Rot of Deciduous Holly .............................................................................................................. 17 ABSTRACT .................................................................................................................. 17 INTRODUCTION ........................................................................................................ 18 ix MATERIALS AND METHODS .................................................................................. 20 RESULTS ..................................................................................................................... 26 DISCUSSION ..............................................................................................................
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