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Open Zitomer.Pdf The Pennsylvania State University The Graduate School College of Agricultural Sciences MYCOTOXICOLOGY TO ACCOMPANY PHYLOGENETIC REVISIONS TO THE GENUS FUSARIUM A Thesis in Plant Pathology by Nicholas C. Zitomer © 2006 Nicholas C. Zitomer Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2006 The thesis of Nicholas C. Zitomer was reviewed and approved* by the following: Gretchen A. Kuldau Assistant Professor of Plant Pathology Thesis Co-Adviser Co-Chair of Committee David M. Geiser Associate Professor of Plant Pathology Thesis Co-Adviser Co-Chair of Committee Erick D. DeWolf Assistant Professor of Plant Pathology Douglas D. Archibald Research Associate, College of Agricultural Sciences A. Daniel Jones Senior Scientist, Department of Chemistry Barbara J. Christ Professor of Plant Pathology Head of the Department of Plant Pathology *Signatures are on file in The Graduate School. iii ABSTRACT Fusarium species traditionally have been and still are problematic to identify using morphology. This is an issue of concern since many fusaria are toxigenic, producing such toxins as trichothecenes, fumonisins and zearalenone. Fumonisins are sphingolipid analogues associated primarily with the Gibberella fujikuroi species complex (GFC). Fusarium trichothecenes are sesquiterpenoid mycotoxins, and are generally divided into two categories: type A, which lack oxygen at the C-8 position and include T-2 toxin and diacetoxyscirpenol, and type B, which include nivalenol and deoxynivalenol. Zearalenone is an estrogenic mycotoxin. Phylogenetically characterized isolates were subjected to mycotoxin analysis via high performance liquid chromatography and atmospheric pressure chemical ionization mass spectrometry (HPLC/APCI-MS), HPLC and electrospray ionization mass spectrometry (HPLC/ESI-MS), or HPLC using fluorescence detection. Isolates with previous reports of toxin production outside of the groups analyzed were also included in the mycotoxin analyses. Our results reveal scattered toxin production within the GFC (fumonisin) and the trichothecene-producing fusaria (trichothecenes and zearalenone), as well as by a few isolates outside of these groups. Phylogenetic placement in either group is predictive of toxin production potential, but not toxin production, level or toxin class (type A or type B trichothecenes). iv TABLE OF CONTENTS List of Tables……………………………………………………..…………….………..vii List of Figures………..……………….……………….………………………………...viii Acknowledgements……...…………………………………………………………….….ix CHAPTER 1: Introduction and Literature Review...………………………………..…….1 I. Literature Review…………………………………….……….…………….…………..1 A. History of Fusarium Taxonomy..……………………..……………..………...1 B. New Phylogenetic Concepts in Fusarium..…………………………...……….3 C. Fusarium Mycotoxins…………..………………………...……………………5 i. Fumonisins……………………………………………………...……….5 ii. Zearalenone……………………………………………………………..7 iii. Trichothecenes………………………………………………...……….8 D. Mycotoxicology of Fusarium ……………………………………...……...…11 i. Regulation of Toxin Production…..…………………………………...15 ii. Biosynthesis………………………………………………...…………17 E. Mycotoxin Detection and Quantification..……………………..……………..19 i. Trichothecenes……………………….………………..……………….19 ii. Fumonisins………………...…………………………………...……..20 iii. Zearalenone…………………………………………………..………20 II. Research Objectives………………………………………...…………………..…….21 A. Project Rationale………………………………………...……………………21 B. Research Objectives…………………………………….…………………….22 i. Survey of Fumonisin Production in the Gibberella fujikuroi Species Complex…………………………………………………..…….………..22 ii. Evaluation of Trichothecene Production Using New Phylogenetic Data..……………………………………………..…………….……….22 iii. Evaluation of Zearalenone Production Using New Phylogenetic Data...…………………..………………………………………………23 v CHAPTER 2: The Phylogenetics of Trichothecene Production in Fusarium..……...…..24 I. Acknowledgements …………………………………………………………………...24 II. Abstract ……..………………………………………………………………………..24 III. Introduction…...……………………………………………………………………...25 IV. Methods………...……………………………………………………………………31 A. Chemicals and Reagents…………………………………...………....31 B. Culturing……………………………………………………………...31 C. DNA Analyses…..……………………………………………,………32 D. Extraction and Sample Preparation…………………………………...33 E. HPLC-MS……………………………………………………………..33 F. Data Analysis………………………………………………….……....35 V. Results and Discussion…………..…..………………………………………………..38 A. Phylogenetics of the Trichothecene-Producing Fusaria..……………..38 B. Detection Levels of Trichothecenes and Toxin Responses…………...39 C. Trichothecene Production in Clade 1………………………………....47 D. Trichothecene Production in Clade 2…………...…….……………....51 E. Trichothecene Production in Clade 3…………………….…………...60 F. Trichothecene Production in Clade 4…………………………….…...63 G. Conclusions.......................................…………………………….…...66 CHAPTER 3: The Phylogenetics of Zearalenone Production in Fusarium…….…..…...68 I. Acknowledgements…………………………………………………………………....68 II. Abstract ……………………………………………………………………………....68 III. Introduction………………….…………………………………………………….…69 IV. Methods…………………………………………………………………………...…76 A. Chemicals and Reagents………………………………………….…..76 B. Culturing……………………………………………………………...76 C. Extraction and Sample Preparation…………………………………...77 D. HPLC…………………………………………………………………78 V. Results...……………………………………………………………………………...78 VI. Discussion……………………………………………………………………….…..86 CHAPTER 4: Fumonisin Production Investigated Within a Phylogenetic Analysis of the Gibberella fujikuroi Species Complex…………………………………………………...93 I. Acknowledgements……………………………………………………………………93 II. Abstract ………………………………………………………………………………93 III. Introduction……………………………………………………………………….....94 IV. Materials and Methods……………………………………………………………....98 A. Fungal Strains……..…………………………………...……………..98 vi B. Culture Prepartion…...………………………………………………..98 C. Extraction and Cleanup .……………………………………………...99 D. LC-MS………………………………………………………………100 V. Results and Discussion……………..………………………………………………..101 A. Impetus and Methodological Results……………………………..…101 B. Fumonisin Production in the African Clade of the GFC………….…104 C. Fumonisin Production in the Asian Clade of the GFC……………....110 D. Fumonisin Production in the American Clade of the GFC………….113 E. Other isolates Analyzed……………………………………………...116 Chapter 5: Conclusion…………………………………………………………………..138 References………………………………………………………………………………141 Appendices……………………………………………………………………………...166 Appendix A: Example Mass Spectra of Trichothecenes and Hydrocortisone………………………………………………………….166 Appendix B: Type A and B Trichothecene Production by Strain in Phylogenetic Order…………………………………………………..…176 Appendix C: Strain List for the Fumonisin Assays………….………....185 Appendix D: Strain List for the Trichothecene Analysis……………….191 vii LIST OF TABLES Table 1.1: Fusarium Species with Reported Fumonisin Production .…….…..………....12 Table 1.2: Fusarium Species Within the Trichothecene-Producing Clade and Their Reported Trichothecene and Zearalenone Production..……………….…………………14 Table 2.1: Masses of Trichothecene Ions and Fragment Ions Used for Mass Spectrometry Quantification and Verification……..…………………………………………………...37 Table 3.1: Reported Zearalenone Producers………...……..………….…………………73 Table 3.2: Summary of Pooled Zearalenone Analysis by HPLC……………………..…81 Table 3.3: Zearalenone and Zearalenol Amounts (in μg/g rice) Produced Under Three Temperature Regimes by Fusarium Species……………………..…………………...…84 Table 4.1: Fusarium Species with Reported Fumonisin Production…………...………..96 Table 4.2: Strains Within the GFC Analyzed for Toxin Production …………………..119 viii LIST OF FIGURES Fig. 1.1: The Chemical Structure of Fumonisins ……...…..………...……….………...…7 Fig. 1.2: The Chemical Structures of Zearalenone and Zearalenol.……….…….…......…8 Fig. 1.3: The Chemical Structures of Five Type A Trichothecenes ……………….....…10 Fig. 1.4: The Chemical Structures of Five Type B Trichothecenes….……...………...…11 Fig. 2.1: Structure of Type A Trichothecenes with R-Groups for Each Toxin ……..…..30 Fig. 2.2: Structure of Type B Trichothecenes with R-Groups for Each Toxin …..……...30 Fig. 2.3: An Example LC/MS Chromatogram Showing Separation of Trichothecene Mycotoxins in Run of Standards………………………………………………….……...35 Fig. 2.4: Phylogenetic Tree Resulting from Maximum Parsimony Analysis……..……..43 Fig 2.5: Profiles of Individual Toxin Production Within Each Clade of the Trichothecene- Producing Fusaria………………………………………………………………….…….44 Fig. 2.6: The Observed Toxin Response of all Isolates Within Each Clade Displayed by Percent Total of Toxin Amounts Produced…………………………………………...…45 Fig. 2.7: Phylogenetic Tree Resulting from Maximum Parsimony Analysis Showing Trichothecene Concentrations……………………………………………………….…..46 Fig. 3.1: The Chemical Structures of Zearalenone and Zearalenol…………………..….72 Fig. 3.2: Phylogenetic Tree Resulting from Maximum Parsimony Analysis of Multiple Gene Regions from Species Representing the Diversity of the Trichothecene-Producing Fusaria……………………………………………………………………………………75 Fig. 3.3: Phylogenetic Tree Representing the Diversity of the Trichothecene-Producing Fusaria with Zearalenone-Producing Species Identified Upon It………………………..83 Fig. 4.1: The Chemical Structure of Select Fumonisins……...………………………….95 Fig. 4.2: Phylogenetic Tree Created by Neighbor Joining Analysis of EF-1α .………..137 ix ACKNOWLEDGEMENTS I would like to thank my thesis advisers, Gretchen Kuldau and David Geiser, for all their support and guidance during this process. In addition, I'd like to thank the rest of my thesis committee members for their invaluable assistance and expertise in guiding
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