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The Relationship of Ilyonectria to Replant Disease of American Ginseng (Panax

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The Relationship of Ilyonectria to Replant Disease of American Ginseng (Panax The relationship of Ilyonectria to replant disease of American ginseng (Panax quinquefolius) by Behrang Behdarvandi A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Environmental Sciences Guelph, Ontario, Canada © Behrang Behdarvandi, September, 2020 ABSTRACT THE RELATIONSHIP OF Ilyonectria TO REPLANT DISEASE OF AMERICAN GINSENG (Panax quinquefolius) Behrang Behdarvandi Advisor: University of Guelph, 2020 Professor Paul H. Goodwin Ginseng replant disease involves the high mortality of ginseng plants (Panax quinquefolius) growing in fields previously used for ginseng cultivation, and is linked to root rot caused by Ilyonectria mors-panacis. One hypothesis for replant disease is that there is a selection for highly virulent isolates in the first crop, but no significant differences in root lesion size were observed among 12 isolates of I. mors-panacis and four isolates of Ilyonectria robusta obtained from diseased roots of ginseng in replant or non-replant soil. However, the average growth rate on potato dextrose agar for I. robusta isolates was greater than for I. mors-panacis, and the average virulence was greater for isolates with greater hyphal pigmentation in culture. Based on nucleotide sequences of all exons of the genomes, the I. robusta isolates were distinguishable from the I. mors-panacis isolates, which were divided into types 1 and 2. The division of I. mors-panacis into types was not related to virulence but to secretome sequence differences, particularly small secreted cysteine-rich proteins and secreted lipases. Treatment of ginseng roots with replant soil extract, but not ginseng root extract or non-replant soil extract, increased lesion sizes of roots inoculated with I. mors-panacis compared to water. Increased lesion size was related to a reduced response to I. mors-panacis infection in expression of five genes related to jasmonic acid (JA), ethylene (ET) or necrotrophic infection, whereas expression of a iii salicylic acid (SA) related gene was increased. Formation of JA/ET related immunosuppressing compounds in replant soil may be due to soil bacterial activity as ginseng root extracts could be converted into unknown immunosuppressing compound(s) when incubated in culture medium with an isolate of Pseudomonas plecoglossicida obtained from replant soil. Higher growth of the bacterium with ginseng root extract compared to medium alone indicated that root extract acted as a nutrient. It is hypothesized that ginsenosides and/or other ginseng root compounds enter soil where they are microbially converted into immunosuppressing compounds against the JA/ET defense response of ginseng to I. mors-panacis infection following uptake by roots. Prolonged immunosuppression could increase levels of root rot contributing to ginseng replant disease. iv DEDICATION To honor of my son Rayan--May you never stop learning. v ACKNOWLEDGMENTS I am using this opportunity to express my sincere and special appreciation and thanks to my supervisor Dr. Paul H. Goodwin for his continuous support and guidance during my PhD research project and providing me with the opportunity to pursue my research interest in plant pathology. I express my warm thanks to the members of my supervisory committee, Dr. Kenneth Conn, Dr. Tom Hsiang and Dr. Sean Westerveld for their expert advice and incredible supports in all steps of the project. Thank you to Dr. Ernesto Guzman, Dr. Zamir Punja and Dr. James Longstaffe for serving on my PhD thesis examination. I would also like to thank Dr. Mark Bernards and his research group for their advice and great supports for High Performance Liquid Chromatography analysis of the samples. I would also like to thank Dr. James Longstaffe for his kind helps and support for Nuclear Magnetic Resonance analysis of the samples. Special thanks to my friend and colleague, Moez Valliani, for helping me throughout my research and his great performance in the bioinformatic analysis of data in the project. Thanks to Ontario Ginseng Grower Association and Amy Fung Shi for their supports. The project was funded by Ontario Ministry of Agriculture, Food and Rural Affairs. Finally, I would like to thank to my wife and my parents as well as all my friends for their kind and constant supports. vi TABLE OF CONTENTS Abstract …………………………………………………………………………………..............ii Dedication …………………………………………………………………………………….….iv Acknowledgements……………………………………………………………………………….v Table of Contents…………………………………………………………………………………vi List of Appendices….……………………………………………………………………………..x List of Tables…………………………………………………………………………………….xii List of Figures…………………………………………………………………………………...xiv List of Abbreviations…………………………………………………………………………..xviii 1. Introduction and literature review…………………………………………………………..…..1 1.1. Ginseng history and significance………………………….………………………..........…...1 1.2. Species, geographical distribution, and ecology………………………………………...……2 1.3. Panax quinquefolius…………………………………………………………………...……...2 1.4. Cultivation of Panax quinquefolius in Ontario……………………………………...………..3 1.5. Ginsenosides as secondary metabolites of ginseng…………………………………...………6 1.6. Bioconversion of ginsenosides…………………………………………………...……...….13 1.7. Other secondary metabolites of Panax spp…………………….……………………..……..14 1.8. Panax spp. diseases………………………………………………………………...………..16 1.9. Cylindrocarpon taxonomy and genetics……..……………………………..…….…………18 1.10. Cylindrocarpon destructans (I. radicicola complex) disease cycle…………….........…....20 1.11. Cylindrocarpon virulence……………………………………………………………...…..22 1.12. Morphological and molecular detection of Cylindrocarpon destructans……………….…24 1.13. Ginseng genes involved in fungal resistance……………………………...…….…....……27 1.14. Replant failure in ginseng production…………………………………………..……….…29 vii 1.15. Ginseng replant disease and soil sickness…………….……………………………...…….29 1.16. Influence of ginsenosides and biotic factors on ginseng replant disease……………......…31 1.17. Control of ginseng replant disease……………….………………………………………...33 1.18. Conclusions……………………………………………...…………………………………36 1.19. Hypotheses ………………………………………………….....………………………..…38 1.20. Objectives…………………………………………………………………………...……..38 2. Comparative study of Ilyonectria robusta and I. mors-panacis isolates from American ginseng (Panax quinquefolius) roots in Canada……………………………………………………..39 2.1. Introduction…………………………………………………………….…………………...39 2.2. Materials and methods…………….………………………………………………….……..42 2.2.1. Source of isolates………………………………………………………………….……....42 2.2.2. Isolate Identification……………………………………………………….…………...…43 2.2.3. Isolate growth rate and appearance in culture………………………………………….…44 2.2.4. Root and soil extraction………………….………………………………………….…….44 2.2.5. Detached root assay……………………………………………………………….………45 2.2.6. Genome sequencing, assembly and gene prediction……………..…………………..…...45 2.2.7. Phylogeny……………………………………………………….………………………...46 2.2.8. Secretome protein analysis…………………………………………………………….….47 2.2.9. Selected non-secretome protein analysis………………………………………….………48 2.3. Results……………………………………………………………………………………....49 2.3.1. Identification and cultural characteristics of Ilyonectria isolates…………………………49 2.3.2. Virulence of Ilyonectria isolates………………………………………………………….51 2.3.3. Genomics of the Ilyonectria isolates………………….…………………………………..53 2.3.4. Phylogenetic relationship of the Ilyonectria isolates…………………………….………..54 2.3.5. Relatedness of the secretomes of the Ilyonectria isolates…………………………………56 viii 2.3.6. Relatedness of selected elements of the non-secretomes of the Ilyonectria isolates……...58 2.3.7. Relationship of copy number to growth rate of Ilyonectria isolates………………………61 2.3.8. Relationship of copy number to lesion size caused by Ilyonectria isolates……………….65 2.4. Discussion…………………………………………………………………………………...67 3. Effect of soil and root extracts on root rot of American ginseng (Panax quinquefolius) caused by Ilyonectria mors-panacis…………….…………………………………………………129 3.1. Introduction………………………………………………………..………………...……..129 3.2. Materials and Methods………………………………………………….………………….132 3.2.1. Biological materials………………………………………………………………...……132 3.2.2. Root and soil extraction………………………………..…………………………...……132 3.2.3. Detached root assay…………………………………………...……………………..…..133 3.2.4. RNA extraction……………………………………………...……………………..……133 3.2.5. Primer design used in relative RT-PCR……………………………………………..…..134 3.2.6. Relative RT-PCR…………………………………………...………………………...….136 3.2.7. HPLC-MS analysis……………………………………………………………………....137 3.3. Results………………………………………………………………………………….…..137 3.3.1. Effects of the extracts on root rot disease……………………………………...……...…137 3.3.2 Composition of extracts………………………………………...…………………...……138 3.3.3. Effects of extracts on gene expression……………………………………………...……138 3.4. Discussion……………………………………………………………...…...………….…..142 4. Effects of Pseudomonas plecoglossicida media extracts on root rot development in American ginseng (Panax quinquefolius) caused by Ilyonectria mors-panacis……...……………....160 4.1. Introduction…………………………………………………………….………….……….160 4.2. Materials and Methods…….…………………………………….…………….……...……163 4.2.1. Biological materials…………………………………………………………....…...……163 ix 4.2.2. Root extraction……………………………………………………………………….…..164 4.2.3. Isolation and identification of bacteria from soil………………………………………...164 4.2.4. Bacterial growth and ginsenoside transformation………………………………………..165 4.2.5. Detached root assay…………………………………………………..………...…….….167 4.2.6. Genome sequencing and assembly of Pseudomonas plecoglossicida…………………...167 4.2.7. Phylogeny of
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