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Ecological and Chemical Aspects of White Oak Decline and Sudden Oak Death, Two Syndromes Associated with Phytophthora Spp

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Ecological and Chemical Aspects of White Oak Decline and Sudden Oak Death, Two Syndromes Associated with Phytophthora Spp ECOLOGICAL AND CHEMICAL ASPECTS OF WHITE OAK DECLINE AND SUDDEN OAK DEATH, TWO SYNDROMES ASSOCIATED WITH PHYTOPHTHORA SPP. A Thesis Presented in Partial Fulfillment of the Requirements for the Degree of Master of Science in the Graduate School of The Ohio State University By Annemarie Margaret Nagle Graduate Program in Plant Pathology The Ohio State University 2009 *** Thesis Committee: Pierluigi (Enrico) Bonello, Advisor Laurence V. Madden Robert P. Long Dennis J. Lewandowski Copyright by: Annemarie Margaret Nagle 2009 ABSTRACT Phytophthora spp., especially invasives, are endangering forests globally. P. ramorum causes lethal canker diseases on coast live oak (CLO) and tanoak, and inoculation studies have demonstrated pathogenicity on other North American oak species, particularly those in the red oak group such as northern red oak (NRO). No practical controls are available for this disease, and characterization of natural resistance is highly desirable. Variation in resistance to P. ramorum has been observed in CLO in both naturally infected trees and controlled inoculations. Previous studies suggested that phloem phenolic chemistry may play a role in induced defense responses to P. ramorum in CLO (Ockels et al. 2007) but did not establish a relationship between these defense responses and actual resistance. Here we describe investigations aiming to elucidate the role of constitutive phenolics in resistance by quantifying relationships between concentrations of individual compounds, total phenolics, and actual resistance in CLO and NRO. Four experiments were conducted. In the first, we used cohorts of CLOs previously characterized as relatively resistant (R) or susceptible (S). Constitutive (pre-inoculation) phenolics were extracted from R and S branches on three different dates. Additional branches from the same trees were inoculated in the greenhouse at the time of phloem sampling to confirm relative resistance. In the second experiment, concentrations and variation in phenolic profiles of CLOs exhibiting apparent field resistance were compared to symptomatic (i.e. ii susceptible) trees. In the third experiment, half-sib families of one-yr-old NRO were inoculated on two occasions and their relative resistance evaluated against concentrations of constitutive phenolics. Certain phenolics were found in higher concentrations in more resistant NROs and CLOs, and their potential use as biomarkers of resistance is discussed. In the fourth experiment, NROs were treated with methyl jasmonate, a phytohormone known to induce phenolic defenses in conifers, but toxicity to phloem prevented conclusive analysis. White oak (WO) plays a vital ecological role and is one of Ohio’s most important hardwoods. The recent decline and death of many WOs in southern Ohio forests is therefore concerning. The concentration of mortality in wet areas and the isolation of P. cinnamomi from rhizospheres of declining oaks suggest this pathogen may be involved in the syndrome. We investigated P. cinnamomi’s potential role with field and greenhouse studies during the summers of 2008 and 2009. In two declining (D) and two healthy (H) WO stands, one pair of soil samples at each of three elevations along 120 m transects were collected monthly to monitor soil moisture and inoculum densities. Relationships between soil moisture and inoculum densities remained unclear, but D stands had significantly higher P. cinnamomi propagule densities than H stands in both years. In the second study, the root systems of potted WOs maintained in the greenhouse were significantly damaged by inoculation of the soil with P. cinnamomi, especially under conditions of periodic experimental flooding. These data provide circumstantial evidence that P. cinnamomi may contribute to WO decline. Finally, recent U.S.-wide surveys for P. ramorum have led to detection and geolocation of known and novel Phytophthora spp. Isolation information, genetic iii analyses, and pathogenicity tests with a suspected novel species closely related to P. gallica are presented. iv DEDICATION To my grandparents, whose passion for the forest inspired my love of trees To my mother, father, and sister, for their boundless support To the kids on two wheels in Columbus v ACKNOWLEDGEMENTS I would like to thank my advisor, Enrico Bonello for allowing me the opportunity to perform the following research, and for providing patient advice and guidance. His commitment to continually challenging me and believing that I would rise to the challenge helped me to grow as both a student and a person. I would also like to thank my committee, Bob Long, Larry Madden, and Dennis Lewandowski, for their helpful input on methods of design and execution of various projects, and for their encouraging words during challenging times. A special thanks to Dr. Long and Tim Fox, who were instrumental in completion of the field work at Scioto Trail and associated greenhouse experiments, for their enthusiasm and willingness to share their resources and time. Dr. Madden’s assistance in analysis of the complicated datasets generated in this fieldwork was also greatly appreciated. I would also like to thank Matteo Garbelotto for providing the lab space, funding, plant material, and personnel for conducting greenhouse experiments on CLO. Katy Hayden worked very hard to coordinate our trans-U.S. collaborations, and Lydia Baker, Alex Lundquist, Ellen Crocker, Doug Schmidt, and Alex Yiu donated their assistance and time to support studies conducted at U.C. Berkeley. I would like to especially thank Brice McPherson for his willingness to share his data and observations about resistance of CLO to SOD in California forests, for his enthusiasm and meticulousness in our vi research, and for caring enough to take the time to take me for a hike. Thanks also to David Wood, whose expertise enriched my knowledge of SOD and forest research. Many members of the Bonello lab have also been instrumental in completion of this work. I would like to thank Duan Wang in particular for her technical expertise and emotional support. She assisted with everything from grinding samples to designing PCR protocols. Thanks also to fellow graduate students Nathan Kleczewski, Justin Whitehill, and Chris Wallis, who educated me on technical laboratory procedures, statistical analysis methods, and assisted with lab and field work. Will Hilinski, Shannon Quinn, Robbie Snyder, Nelda Vazquez, Brian Goldberger, Gerardo Suazo, Zhifeng Cheng, and Amber Hoffstetter also provided essential assistance with lab and fieldwork associated with various projects, and great company. Funding for this research was provided by USDA Forest Service Research Joint Venture Agreement #07-JV-11242300-075, an Ohio Agricultural Research and Development Center grant to AMN, and state funds appropriated to the Department of Plant Pathology, The Ohio State University. vii VITA November 10, 1984....................................................Born, Raleigh NC May 2003 ...................................................................Graduated from Cardinal Gibbons High School, Raleigh NC May 2007 ...................................................................B.S. in Biology, minors in Chemistry and Environmental Science, University of North Carolina Chapel Hill June 2007-present ......................................................Graduate Research Associate, The Ohio State University PUBLICATIONS Kingsolver, J.G. and A. Nagle. 2007. Evolutionary divergence in thermal sensitivity and diapause of field and laboratory populations of Manduca sexta. Physiological and Biochemical Zoology 80(5): 473-479. FIELDS OF STUDY Major Field: Plant Pathology Specializing in: Forest Pathology Chemical Ecology viii TABLE OF CONTENTS Abstract............................................................................................................................... ii Dedication............................................................................................................................v Acknowledgements............................................................................................................ vi Vita................................................................................................................................... viii List of Tables .......................................................................................................................x List of Figures................................................................................................................... xii Chapter 1: Introduction to Phytophthora, a genus of increasing importance in forest pathology .......................................................................................................1 Chapter 2: Relationship between resistance to Phytophthora ramorum and constitutive phenolic chemistry of coast live oaks and northern red oaks...............5 Chapter 3: Relative resistance and constitutive phenolics in cut stems of northern red oak seedlings treated with methyl jasmonate ..................................................43 Chapter 4: Assessing the role of soil moisture and Phytophthora cinnamomi in white oak decline in Southern Ohio.......................................................................55 Chapter 5: Identification and characterization of a previously unknown Phytophthora taxon isolated from an Indiana waterway .......................................93 References........................................................................................................................109
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