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Understanding the Fungal Biology and Fungicide Control Of UNDERSTANDING THE FUNGAL BIOLOGY AND FUNGICIDE CONTROL OF NEOFABRAEA SPECIES CAUSING BULL’S-EYE ROT OF APPLES GROWN IN THE US PACIFIC NORTHWEST By CHRISTIAN GRACE AGUILAR A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY WASHINGTON STATE UNIVERSITY Department of Plant Pathology JULY 2017 © Copyright by CHRISTIAN GRACE AGUILAR, 2017 All Rights Reserved © Copyright by CHRISTIAN GRACE AGUILAR, 2017 All Rights Reserved To the Faculty of Washington State University: The members of the Committee appointed to examine the dissertation of CHRISTIAN GRACE AGUILAR find it satisfactory and recommend that it be accepted. ____________________________________ Mark Mazzola, Ph.D., Chair ____________________________________ Weidong Chen, Ph.D. ____________________________________ Dennis Johnson, Ph.D. ____________________________________ Chang-Lin Xiao, Ph.D. ii ACKNOWLEDGMENTS There are many individuals who provided physical, financial and/or emotional support to me over the course of my Ph.D. studies. I am immensely grateful to these individuals. Specifically, I would like to thank Dr. Mark Mazzola for “adopting” me into his lab and mentoring me throughout the past five years of my degree. He has guided me not only in terms of my research but has also helped me mature professionally by giving me the opportunity to write manuscripts, grants and network at local and national conferences. His patience has been unwavering and I am very thankful to have had the opportunity to work under his direction. Similarly, I would like to thank Dr. Chang-Lin Xiao for providing funding support so that I may conduct my research, and for his active involvement during the planning and execution of my research projects. His insights and criticism have helped to strengthen this work. Additionally, I would like to thank Drs. Weidong Chen and Dennis Johnson for sitting through numerous committee meetings, responding to countless emails, and for reviewing and editing this dissertation. Next I would like to thank Robin Boal, Chris Sater, Sheila Ivanov, Marcia Walter and Xiaowen Zhao for helping me conduct my projects and for providing suggestions when brainstorming and troubleshooting were needed. I am also appreciative of the various conversations shared with these individuals, to which the tedium of everyday lab activities became much more tolerable. I would like to extend my gratitude to Drs. Rosa Caiazzo and Parama Sikdar for helping me navigate through my graduate studies and research work, and also for their kindness and friendship. Furthermore, I would like to recognize the USDA- Agricultural Research Service, the Seattle Chapter of the Achievement Rewards for College Scientists (ARCS) foundation, the iii Washington State University Research Assistantships for Diverse Scholars (RADS) program, the Mike and Kathy Hambelton Fellowship endowment, and the Washington Tree Fruit Research Commission for providing funding support of this work. Without the provisions granted by these agencies, this research could not exist. Lastly, I wish to thank my family for enduring this crazy roller coaster ride with me. Thank you!!! iv UNDERSTANDING THE FUNGAL BIOLOGY AND FUNGICIDE CONTROL OF NEOFABRAEA SPECIES CAUSING BULL’S-EYE ROT OF APPLES GROWN IN THE US PACIFIC NORTHWEST Abstract by Christian Grace Aguilar, Ph.D. Washington State University July 2017 Chair: Mark Mazzola Neofabraea perennans and Neofabraea kienholzii are two of four fungal organisms causing bull’s-eye rot of apples and other pome fruit grown in the US Pacific Northwest. Artificial wound inoculations conducted on ‘Fuji’ and ‘Red Delicious’ apple twigs using the aforementioned species demonstrated that both fungi are capable of inducing tree cankers that are similar in appearance. Cankers were largest following inoculations held in October compared to all other inoculation events evaluated. Additionally, artificial inoculations conducted on ‘Fuji’ and ‘Red Delicious’ apple fruit throughout the growing season revealed that fruit infections were more likely to be established during the final weeks approaching commercial harvest. Together, these studies demonstrate that these fungi are capable of surviving in the orchard as mycelium in tree cankers throughout the year, and under favorable conditions, can cause fruit infections throughout the fruit-growing season. These results highlight the importance of canker pruning as a means of reducing the pathogen inoculum load in the orchard. v Trials were also conducted to evaluate the efficacy of various pre-harvest and postharvest applied fungicides for the control of bull’s-eye rot in ‘Fuji’ apples. Findings from these studies demonstrated that among the materials tested, thiophanate-methyl, thiabendazole and pyrimethanil were the most effective fungicides in suppressing incidence of bull’s-eye rot and were capable of mitigating early, mid and late season fruit infections following a single application near/at the end of the apple-growing season. Although effective in controlling this important postharvest disease of apple, incorporation of these fungicides into spray programs should proceed with caution so as to minimize the risk of fungicide resistance in populations of Neofabraea spp. as well as other major pathogens in the Pacific Northwest. vi TABLE OF CONTENTS Page ACKNOWLEDGMENTS ........................................................................................................ iii ABSTRACT ................................................................................................................................ v LIST OF TABLES ..................................................................................................................... ix LIST OF FIGURES .................................................................................................................... x CHAPTER ONE – Timing of Perennial Canker Development in Apple Trees Caused by Neofabraea perennans and Neofabraea kienholzii ABSTRACT .................................................................................................................... 1 INTRODUCTION .......................................................................................................... 2 MATERIALS AND METHODS .................................................................................... 4 RESULTS ....................................................................................................................... 9 DISCUSSION ............................................................................................................... 12 LITERATURE CITED ................................................................................................. 17 CHAPTER TWO – Timing of Apple Fruit Infection by Neofabraea perennans and Neofabraea kienholzii in Relation to Bull’s-eye Rot Development in Stored Apple Fruit ABSTRACT .................................................................................................................. 31 INTRODUCTION ........................................................................................................ 32 MATERIALS AND METHODS .................................................................................. 35 vii RESULTS ..................................................................................................................... 39 DISCUSSION ............................................................................................................... 42 LITERATURE CITED ................................................................................................. 47 CHAPTER THREE – Control of Bull’s-eye Rot Caused by Neofabraea perennans and Neofabraea kienholzii in Stored Apple Using Pre- and Postharvest Fungicides ABSTRACT .................................................................................................................. 58 INTRODUCTION ........................................................................................................ 59 MATERIALS AND METHODS .................................................................................. 62 RESULTS ..................................................................................................................... 67 DISCUSSION ............................................................................................................... 70 LITERATURE CITED ................................................................................................. 74 viii LIST OF TABLES CHAPTER ONE 1. Comparisons between inoculation event and its effect on acervuli viability of Neofabraea spp. using Fisher’s exact test .............................................................................................. 22 CHAPTER TWO 1. Dates of fruit inoculation and harvest for bull’s-eye rot field trials conducted at Washington State University Sunrise Research Orchard, and environmental conditions recorded during each fruit inoculation event ................................................................................................. 52 CHAPTER THREE 1. Influence of pre-harvest fungicide treatment, inoculation event, Neofabraea species and the interaction of these variables on bull’s-eye rot incidence of ‘Fuji’ apples cultivated during the 2013 and 2014 growing seasons ......................................................................................... 78 2. Influence of postharvest fungicide treatment, inoculation event, Neofabraea species and the interaction of these variables on bull’s-eye
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