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Alternaria Alternata of CITRUS MOLECULAR INTERPLAY AMONG THE REDOX-RESPONSIVE REGULATOR AaAP1, THE TWO-COMPONENT HISTIDINE KINASE AND THE MITOGEN-ACTIVATED PROTEIN (MAP) KINASES IN Alternaria alternata OF CITRUS By CHING-HSUAN LIN A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2010 1 © 2010 Ching-Hsuan Lin 2 To my wife, Ms. Hui-Yu Hsieh, and my sisters, Ms. Mei-Ling Lin and Mei-Jyun Lin for their thorough support and encouragement 3 ACKNOWLEDGMENTS This research project would not have been possible without the support of many people. I would like to express my gratitude to my supervisor, Dr. Kuang-Ren Chung, whose expertise, understanding, and patience, added considerably to my graduate experience. I appreciate his invaluable vast knowledge and skills in many areas and his assistance in my writing. I would like to thank the other members of my committee, Dr. Fredy Altpeter, Dr. Jeffrey A. Rollins, and Dr. Jeffrey B. Jones for their helpful assistance and critical evaluation of this dissertation. Special thanks also to all my graduate friends: Andrew Funk, Franklin Behlau, Qiang Chen, Xiaoen Huang, and Chang-Hua Huang, Sarsha, and Carol. They each helped make my time in the PhD program more fun and interesting. I also want to thank our Lab members, Siwy Ling Yang, Nan-Yi, Wang and Mr. Lenny Venderpool for their assistance to some aspects of my research project. Most importantly, I thank my family for the support they provided me through my entire life and in particular, I must acknowledge my wife without her endless love and encouragement I would not have finished this thesis. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 9 LIST OF FIGURES ........................................................................................................ 10 ABSTRACT ................................................................................................................... 13 CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW ..................................................... 15 Introduction of Alternaria alternata (Fr.) Keissler .................................................... 15 Taxonomy ......................................................................................................... 15 Host-Selective Toxins Produced by A. alternata to Citrus ................................ 15 Disease Symptoms of Alternaria Brown Spot ................................................... 16 Life Cycle .......................................................................................................... 17 Economic Significance and Disease Control .................................................... 17 Oxidative Burst and Strategy of Antioxidant Defense in Fungi ................................ 18 Roles of Reactive Oxygen Species in Plants .................................................... 18 Detoxification of ROS and Fungal Pathogenesis .............................................. 19 Transcriptional Regulation in Response to Oxidative Stress ............................ 20 Signal Transduction Cascades That Regulate Fungal Development and Virulence .............................................................................................................. 21 MAP Kinase Cascade ...................................................................................... 21 Two-Component Histidine Kinases .................................................................. 23 Mitogen-Activated Protein Kinase (MAPK) Network ......................................... 24 Research Overview................................................................................................. 26 2 THE Alternaria alternata AaAP1 TRANSCRIPTION FACTOR INVOLVED IN DETOXIFICATION OF REACTIVE OXYGEN SPECIES IS A KEY PATHOGENICITY FACTOR ON CITRUS .............................................................. 31 Introduction ............................................................................................................. 32 Materials and Methods ............................................................................................ 34 Fungal Strains and Culture Conditions ............................................................. 34 Lipid Peroxidation Assays ................................................................................ 35 Detection of H2O2 in Citrus Leaves ................................................................... 35 Cloning of AaAP1 ............................................................................................. 36 Creation and Identification of the AaAP1 Null Mutants ..................................... 36 Genetic Complementation of an AaAP1-Disrupted Mutant .............................. 37 AaAP1 Localization .......................................................................................... 38 Sensitivity Test of AaAP1 Null Mutants ............................................................ 38 Pathogenicity Assays ....................................................................................... 38 Purification of ACT Host-Selective Toxin .......................................................... 39 5 Microscopy ....................................................................................................... 40 Enzymatic Assays ............................................................................................ 40 Molecular Techniques ...................................................................................... 43 Results .................................................................................................................... 44 Stress Responses of Citrus Leaves Inoculated with A. alternata ..................... 44 Characterization of an AP1 Homolog in A. alternata ........................................ 44 Targeted Disruption of AaAP1 .......................................................................... 45 AaAP1 Is Required for Resistance to Oxidative Stress .................................... 46 AaAP1 Null Mutants Have Defective H2O2 Metabolism .................................... 46 Expression of AaAP1 Is Induced by Oxidative Stress ...................................... 47 Nuclear Localization of AaAP1::sGFP upon Exposure to H2O2 ........................ 47 Regulation of ROS-Related Enzymatic Activities by AaAP1 ............................. 47 Identification of the Genes Whose Expression is Regulated by AaAP1 ........... 48 AaAP1 Is Required for the Virulence in A. alternata ......................................... 48 The AaAP1 Null Mutant Is Impaired in Penetration and Colonization Stages... 49 Disruption of the AaAP1 Gene Did Not Affect Host-Selective Toxin Production ..................................................................................................... 49 NADPH Oxidase Inhibitors Partially Restore Pathogenicity of the AaAP1 Null Mutant .................................................................................................... 50 Discussion .............................................................................................................. 50 3 THE FUS3-TYPE MITOGEN-ACTIVATED PROTEIN KINASE AND THE REDOX-RESPONSIVE AP1 REGULATOR FUNCTION COOPERATIVELY IN Alternaria alternata ................................................................................................. 70 Introduction ............................................................................................................. 70 Materials and Methods ............................................................................................ 72 Fungal Strains and Growth Conditions ............................................................. 72 Cloning of AaFUS3 ........................................................................................... 73 Identification of AaFUS3 Null Mutants .............................................................. 73 Genetic Complementation of AaFUS3-Null Mutant .......................................... 73 Create Double Mutations at AaFUS3 and AaAP1 Genes in A. alternata .......... 74 Miscellaneous Assays for Enzymatic Activities ................................................ 74 Pathogenicity Test ............................................................................................ 77 Detection of Phosphorylated AaFUS3 MAPK ................................................... 77 Results .................................................................................................................... 78 Cloning and Characterization of A Fus3 MAP kinase Gene Homolog in A. alternata of Citrus .......................................................................................... 78 Targeted Disruption of AaFUS3 of A. alternata ................................................ 79 AaFUS3 Is Required for Vegetative Growth, Resistance to Copper Fungicide but Negatively Modulates Salt Tolerance ..................................... 79 AaFUS3 Is Essential for Conidiation ................................................................ 80 The AaFUS3 Is Required for Fungal Virulence ................................................ 80 Expression of the AaFUS3 Gene Is Highly Induced by Leaf Extracts .............. 81 AaFUS3 Regulates the Production of Hydrolytic Enzymes
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