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University of California Riverside UNIVERSITY OF CALIFORNIA RIVERSIDE An Integrated Study of the Avocado Root Rot Pathogen Phytophthora cinnamomi A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Plant Pathology by Rodger J. Belisle December 2018 Dissertation Committee: Dr. Patricia Manosalva, Chairperson Dr. James E. Adaskaveg Dr. Howard S. Judelson Dr. Hailing Jin Copyright by Rodger J. Belisle 2018 The Dissertation of Rodger J. Belisle is approved: Committee Chairperson University of California, Riverside ACKOWLEDGEMENTS This research was supported by the University of California Riverside Initial Complement Funds, the California Avocado Commission (008599-002), and the USDA- SCBGP (SCB16057). I would like to thank Dr. Frank N. Martin (USDA-ARS, Salinas CA) for providing Cn-2 Phytophthora cinnamomi DNA and the Brokaw Nursery for donating some of the avocado rootstock liners used in this study. I also want to thank Dr. Akif Eskalen for providing 14 P. cinnamomi isolates and the agrochemical industries for supplying fungicides for evaluation. I would also like to acknowledge all of the collaborators for this research including: Drs. Peggy Mauk, Akif Eskalen, and Joey Mayorquin for their advisory role and technical assistance for the experiments conducted in this study. I want to thank Gaju Ntwali, Dario Murillo, and Gio Gemelga for assisting in greenhouse experiments and Dr. Timothy D. Miles for his advice and critical review of the TaqMan quantitative PCR assay. I am also grateful to Dr. Michael D. Coffey for his advice and support throughout my PhD and Dr. Michael Stanghellini for always being available to discuss my work. I would like to thank Dr. William E. Fry for his critical analysis of this research. I am grateful to everyone in the Adaskaveg Lab for all of their hard work during our collaboration. I was particularly fortunate to have Dr. Wei Hao as a co-first author and I would like to thank her for all of her hard work. I am also especially grateful to Dr. Helga Förster for her continued support, advice, and critical review of this research. iv I am deeply indebted to everyone in the Manosalva Lab for their daily support and expertise without which this research would not have been possible. I am especially grateful to Dr. Guangyuan Xu for his assistance with transformation and Western Blot procedures, Natasha Jackson for her help with primer design, and Aidan Shands for his bioinformatics assistance. Finally, I would like to thank Brandon McKee for his help and tremendous experience working with the avocados used in this research. I received several awards which provided additional funding including: The Deans Distinguished Fellowship Award (2012), the Graduate Student Association Travel Award (2015 and 2016), the American Phytopathological Society Travel Award (2016), and the Leo J. Klotz Memorial Endowment Fund (2015 and 2016), and the Oomycete Molecular Genetics Network Annual Meeting Travel Award (2017). I am grateful to my dissertation committee members including: Dr. Howard Judelson for his support, feedback, and expertise that was essential for the completion of this project, Dr. Hailing Jin for her guidance and expertise in plant immunity, and my deepest thanks to Dr. James E. Adaskaveg for his advice and help inside and outside the lab throughout my PhD. Finally, I am especially grateful and indebted to my advisor Dr. Patricia Manosalva who supported my research and expertly guided me through my PhD project in a little more than three years. I know this would not have been possible with most advisors, but Patty has the drive and ambition to make most things possible. I am extremely fortunate to have been a member of her lab. v The text of this dissertation, in part, is a reprint of the materials as it appears in Phytopathology (Belisle, R. J., McKee, B., Hao, W., Crowley, M., Arpaia, M. L., Miles, T. D., Adaskaveg, J. E., and Manosalva, P. 2018. Phenotypic characterization of genetically distinct Phytophthora cinnamomi isolates from avocado. Phytopathology (https://doi.org/10.1094/PHYTO-09-17-0326-R). Dr. Manosalva is the corresponding author and she directed and supervised the research which forms the basis for this dissertation. vi DEDICATION I would like to dedicate this dissertation to all of my friends and family who helped me throughout my PhD. To my parents who have always been there for me. To my son Jack for inspiring me to work harder so I can provide for him and set a good example. Finally, I would like to dedicate this dissertation to my beautiful wife, Wei, who has always believed in me, supported me, and helped me to be a better person. vii ABSTRACT OF THE DISSERTATION An Integrated Study of the Avocado Root Rot Pathogen Phytophthora cinnamomi by Rodger J. Belisle Doctor of Philosophy, Graduate Program in Plant Pathology University of California, Riverside, December 2018 Dr. Patricia Manosalva, Chairperson Phytophthora root rot (PRR), caused by Phytophthora cinnamomi (Pc), is the most destructive disease of avocado worldwide. This study described the phenotype of a subset of Pc isolates representing two, previously identified, genetically distinct clades of A2 mating type isolates in California regarding growth rate, optimal growth temperature, virulence, and fungicide sensitivity. Isolates corresponding to the clade I group exhibited higher mycelial growth rate and were more sensitive to higher temperatures than clade II. Isolates that were more virulent in avocado and less sensitive to potassium phosphite were also identified. A detached leaf Pc inoculation method using Nicotiana benthamiana was developed and validated providing an alternative method for assessing the virulence of a large number of isolates. Seventy-one isolates of Pc collected from avocado growing regions in California were evaluated for their in vitro sensitivities to four new Oomycota fungicides ethaboxam, fluopicolide, mandipropamid, and oxathiapiprolin and two registered fungicides mefenoxam and potassium phosphite. The four new fungicides and viii mefenoxam showed high in vitro toxicities with relatively low mean effective concentrations to inhibit mycelial growth by 50% (EC50) values. Isolates with reduced sensitivity to potassium phosphite were identified. Greenhouse trials were conducted to assess the efficacy of these fungicides for managing PRR on avocado seedlings and rootstocks. Mefenoxam and potassium phosphite were effective treatments, however, oxathiapiprolin, fluopicolide, and mandipropamid were more effective. RNA sequencing (RNAseq) transcriptome analysis of Pc infected N. benthamiana leaves at 6, 12, 24, 36, and 48 hours post-inoculation was performed. Genes involved in hormone signaling, receptor-like kinases, NBS-LRRs, transcription factors, secondary metabolism, and production of antimicrobial compounds were differentially expressed (DE). Major up-regulated biochemical pathways included the biosynthesis of secondary metabolites and plant-pathogen interactions. Major down-regulated biochemical pathways were primary metabolic pathways and carbon metabolism. Among the DE genes identified, a jasmonic acid responsive gene cytochrome P450 was up- regulated 13.3-fold at 36 hpi, and a gene encoding for a salicylic acid binding protein was down-regulated 10.5-fold. WRKY transcription factor 51, up-regulated by 13.5-fold at 24 hpi, was transiently overexpressed in N. benthamiana and significantly decreased the lesion development on Pc inoculated leaves compared to the GFP control. ix TABLE OF CONTENTS CHAPTER I. GENERAL INTRODUCTION.............................................................. 1 References ................................................................................................................ 10 CHAPTER II. PHENOTYPIC CHARACTERIZATION OF GENETICALLY DISTINCT PHYTOPHTHORA CINNAMOMI ISOLATES FROM AVOCADO .... 16 Abstract .................................................................................................................... 16 Introduction .............................................................................................................. 18 Material and Methods ............................................................................................... 23 Results...................................................................................................................... 32 Discussion ................................................................................................................ 38 Acknowledgements .................................................................................................. 48 References ................................................................................................................ 49 Tables and Figures .................................................................................................... 59 CHAPTER III. NEW OOMYCOTA FUNGICIDES WITH ACTIVITY AGAINST PHYTOPHTHORA CINNAMOMI AND THEIR POTENTIAL USE FOR MANAGING AVOCADO ROOT ROT IN CALIFORNIA ...................................... 67 Abstract .................................................................................................................... 67 Introduction .............................................................................................................. 69 Material and Methods ............................................................................................... 72 Results.....................................................................................................................
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