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Natural Products and Molecular Genetics Underlying the Antifungal

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Natural Products and Molecular Genetics Underlying the Antifungal Natural products and molecular genetics underlying the antifungal activity of endophytic microbes by Walaa Kamel Moatey Mohamed Mousa A Thesis Presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy In Plant Agriculture Guelph, Ontario, Canada ©Walaa K.M.M. Mousa, 2016 i ABSTRACT Natural products and molecular genetics underlying the antifungal activity of endophytic microbes Walaa K. Mousa Advisory Committee: University of Guelph Dr. Manish N. Raizada (Advisor) Dr. Ting Zhou (Co-advisor) Dr. Adrian Schwan Dr. Katarina Jordan Microbes are robust and promiscuous machines for the biosynthesis of antimicrobial compounds which combat serious crop and human pathogens. A special subset of microbes that inhabit internal plant tissues without causing disease are referred to as endophytes. Endophytes can protect their hosts against pathogens. I hypothesized that plants which grow without synthetic pesticides, including the wild and ancient relatives of modern crops, and the marginalized crops grown by subsistence farmers, host endophytes that have co-evolved to combat host-specific pathogens. To test this hypothesis, I explored endophytes within the ancient Afro-Indian crop finger millet, and diverse maize/teosinte genotypes from the Americas, for anti-fungal activity against Fusarium graminearum. F. graminearum leads to devastating diseases in cereals including maize and wheat and is associated with accumulation of mycotoxins including deoxynivalenol (DON). I have identified fungal and bacterial endophytes, their secreted natural products and/or genes with anti-Fusarium activity from both maize and finger millet. I have shown that some of these endophytes can efficiently suppress F. graminearum in planta and dramatically reduce DON during seed storage when introduced into modern maize and wheat. The most exciting discovery of my research is that an endophytic bacterium (strain M6, Enterobacter sp.), isolated from the roots of finger millet, builds a remarkable physical barrier consisting of bacterial micro-colonies that protect the host against ii pathogen invasion. M6 creates an unusual root hair-endophyte stacking (RHESt) formation that prevents entry and/or traps the pathogen which is then killed. Tn5 mutant analysis demonstrated that the endophyte kills the fungal pathogen by using a c-di-GMP- dependent signaling network and diverse fungicides including phenazine. The endophyte has evolved an epistatic regulatory interaction to suppress an antibiotic released by Fusarium which would otherwise inhibit phenazine release into the RHESt. The end- result of this remarkable physico-chemical barrier is a reduction in levels of the mycotoxin DON, thus potentially protecting millions of subsistence farmers and their livestock. To the best of my knowledge, RHESt represents a novel plant defence mechanism and suggests the value of exploring the microbiomes of the world's ancient, orphan crops as source of endophytes with antimicrobial activity. Keywords: Natural products, Antifungal, Genes, Endophytes, RHESt, Fusarium graminearum, Teosinte, Maize, Finger millet, Phoma sp., Fusarium sp. , Penicillium sp., Enterobacter sp., Citrobacter sp. and Paenibacillus polymyxa. iii ACKNOWLEDGMENTS First and foremost, I would like to express my sincere thanks and gratitude to Dr. Manish Raizada for his unbelievable support, insightful discussions and sincere interest. I appreciate all his contributions of ideas, time and effort to make my Ph.D. experience very successful. I extend my thanks to all my committee members: Dr. Ting Zhou (co- advisor), Dr. Adrian Schwan and Dr. Katerina S. Jordan for their help and support and for letting me work in their laboratories. I am very thankful to Dr. Michaela Strueder-Kypke, Molecular and Cellular Imaging Facility, University of Guelph, for her assistance in confocal microscopy imaging and insightful comments. I am thankful to Charles Shearer for his hard work to perform the greenhouse trials. I would like to thank Marina Attalla for helping in disease scoring. I thank Dr. Hanan Shehata for training on lab protocols and for her insightful comments. I am thankful to Gui-Ying Mei for assistance with the DON detoxification experiment. I would like to extend my sincere gratitude to all my colleagues in the Raizada lab for their advice and support. I am also grateful to Dr. Victor Limay-Rios for carrying out DON quantification assays and to Dr. Art Schaafsma and Dr. Ljiljana Tamburic-Ilincic for kindly providing maize and wheat seeds. I would like to express my thanks, appreciation and love for my professors and colleagues at the Pharmacognosy Department, School of Pharmacy, Mansoura University, for their great advice and support. I am thankful to my family for their love and support and for providing me with the highest possible education. Special thanks to my husband Moustafa Ibrahim and my daughters Hanen and Jana for their continuous motivation and inspiration. I am grateful to the Egyptian government for providing me with the generous funding that made this work possible. iv TABLE OF CONTENTS Abstract Acknowledgments iv List of Tables viii List of Figures x List of Abbreviations xv Chapter 1: Thesis outline and general introduction 1.1 Thesis Outline 1 1.2 General introduction 3 1.3 Hypothesis 16 1.4 Objectives 16 Chapter 2: Natural disease control in cereal grains (literature review) 2.1 Abstract 18 2.2 Introduction 19 2.3 Overview of disease management strategies 20 2.4 Introduction to soil and plant associated microbes 21 2.5 Overview of biocontrol mechanisms 21 2.5.1 Competition 22 2.5.2 Antibiosis 23 2.5.3 Induced host resistance 27 2.5.4 Disease suppressive soil 29 2.5.5 Hyperparasitism 30 2.5.6 Transgenic plants 31 2.6 Microbes that combine multiple mechanisms for biocontrol 32 2.7 Examples of commercial biocontrol products 32 2.8 Discussion 33 Chapter 3: The diversity of anti-microbial secondary metabolites produced by fungal endophytes: An interdisciplinary perspective (review article) 3.1 Abstract 36 3.2 Introduction 37 3.3 Diverse classes of fungal antimicrobial secondary metabolites 38 3.3.1 Terpenoid compounds 38 3.3.2 Alkaloids 50 3.3.3 Phenolic compounds 55 3.3.4 Aliphatic compounds 59 v 3.3.5 Polyketides 61 3.3.6 Peptides 68 3.4 Conclusion and future directions 70 Chapter 4: Biodiversity of genes encoding anti-microbial traits within plant associated microbes (review article) 4.1 Abstract 74 4.2 Introduction 75 4.3 Biosynthetic genes encode diverse classes of anti-microbial 76 compounds 4.3.1 Polyketides 81 4.3.2 Non-ribosomal peptides 87 4.3.3 Terpenoids 95 4.3.4 Alkaloids 101 4.3.5 Heterocyclic nitrogenous compounds 105 4.3.6 Volatile compounds 107 4.3.7 Bacteriocins 108 4.3.8 Enzymes 110 4.4 Discussion 113 4.5 Gaps and Future Perspectives 122 Chapter 5: An endophytic fungus isolated from finger millet (Eleusine coracana) produces anti-fungal natural products 5.1 Abstract 127 5.2 Introduction 128 5.3 Material and Methods 130 5.4 Results 136 5.5 Discussion 159 5.6 Study Limitations and Future Experiments 164 Chapter 6: Characterization of antifungal natural products isolated from endophytic fungi of finger millet (Eleusine coracana) 6.1 Abstract 168 6.2 Introduction 169 6.3 Material and Methods 170 6.4 Results 176 6.5 Discussion 188 vi Chapter 7: Root hair-endophyte stacking (RHESt) in an ancient Afro- Indian crop creates an unusual physico-chemical barrier to trap pathogen(s) 7.1 Abstract 193 7.2 Introduction 194 7.3 Material and Methods 195 7.4 Results 202 7.5 Discussion 228 Chapter 8: Bacterial endophytes from wild maize suppress Fusarium graminearum in modern maize and inhibit mycotoxin accumulation 235 8.1 Abstract 236 8.2 Introduction 237 8.3 Material and Methods 247 8.4 Results 276 8.5 Discussion Chapter 9: An endophytic bacterium isolated from wild maize suppresses Fusarium head blight and DON mycotoxin in modern wheat 9.1 Abstract 283 9.2 Introduction 284 9.3 Material and Methods 286 9.4 Results 291 9.5 Discussion 302 Chapter 10: General Discussion 10.1 Summary of the major finding in the thesis 307 10.2 Significance and impact of the study 309 10.3 Conclusion 311 Chapter 11: References 312 Chapter 12: Appendices 369 vii LIST OF TABLES Table 4.1:Table Summary of anti-microbial compounds belonging to genetic 77 pathways that show evidenceof horizontal gene transfer (HGT). Table 4.2: Summary of anti-microbial compounds belonging to genetic 79 pathways, grouped by different evolutionary levels of diversification. Table 5.1: Effect of endophyte extracts on the growth of a diversity of 140 fungal species. Table 8.1: Effect of the candidate bacterial endophytes on the growth of 251 diverse crop fungal pathogens in vitro. Table 8.2: Suppression of Gibberella Ear Rot by the candidate endophytes 272 in two replicate greenhouse trials. Table 8.3: Reduction of DON mycotoxin accumulation during storage 274 following treatment with the candidate endophytes. Table 9.1: Suppression of Fusarium Head Blight by anti-Fusarium 295 endophytes in two replicate greenhouse trials. Table 9.2: Reduction of DON mycotoxin accumulation during storage 300 following treatment with anti-Fusarium endophytes. Table A5.1 18S rDNA sequences and BLAST analysis of fungal 371 endophytes isolated from finger millet in this study. Table A5.2 Taxonomic identification of the endophytic fungi isolated from 373 finger millet. Table A5.3 List of retention times and expected masses of compounds 374 from extract of WF4 fungus fermented on rice. Table A5.4 List of retention times and expected masses of compounds 375 from extract of WF4 fungus fermented on millet. Table A5.5 NMR data for atomic assignments of compounds isolated from 377 WF4. Table A6.1 NMR data for atomic assignments of compounds isolated from 383 finger millet fungi. viii Table A7.1 Gene-specific primers used in quantitative real-time PCR 390 analysis.
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