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Microbial Associates of the Asian Citrus Psyllid and Its Two Parasitoids: Symbionts and Pathogens

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Microbial Associates of the Asian Citrus Psyllid and Its Two Parasitoids: Symbionts and Pathogens MICROBIAL ASSOCIATES OF THE ASIAN CITRUS PSYLLID AND ITS TWO PARASITOIDS: SYMBIONTS AND PATHOGENS By JASON MICHAEL MEYER 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 2007 1 © 2007 Jason Michael Meyer 2 I dedicate this dissertation to my loving wife, Jennifer Lee Meyer. 3 ACKNOWLEDGMENTS Foremost, I thank my advisor and chair of my graduate committee, Dr. Marjorie A. Hoy, for her professional advice, scientific guidance and financial support. I also thank the other members of my graduate committee, Dr. John L. Capinera, Dr. James J. Becnel, and Dr. Eric W. Triplett for their contributions to my research proposal, preparing my qualifying examination and reviewing this dissertation. Additional recognition goes to Dr. Becnel and his laboratory for providing training in electron microscopy and assisting with a class project. I thank Dr. Drion G. Boucias for his instruction and collaboration on projects involving entomopathogenic fungi. Much appreciation is held for Dr. A. Jeyaprakash for his technical advice and assistance with phylogenetics. I acknowledge Lucy Skelley and Reggie Wilcox for their contributions involving insect rearing. Raguwinder Singh is thanked for his efforts during field collection of psyllids. Verena Bläske is acknowledged for her technical assistance with scanning electron microscopy. I thank Vernon Damsteegt for providing psyllids infected with the citrus greening pathogen and Micki Kuhlmann for extracting DNA from these psyllids. I thank Jennifer Zaspel for providing theoretical guidance pertaining to phylogenetic analyses. Heather McAuslane and Karla Addesso are thanked for statistical advice. I thank Mike Rogers and Tim Gast for arranging my trip to collect psyllids from citrus trees with symptoms of citrus greening disease. Lyle Buss, Jane Medley and Mike Sanford are acknowledged for their contributions to photography and figure construction. I thank Dr. Lance Osborne for providing a fungal culture and Dr. James Kimbrough for assistance with fungal morphology. I thank my family for their constant encouragement during my graduate experience. Finally, I wish to acknowledge my wife, Jennifer L. Meyer, for her dedication, patience and unwavering support. This research was 4 funded, in part, by the Davies, Fischer, and Eckes Endowment to Marjorie A. Hoy in biological control. 5 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................4 LIST OF TABLES...........................................................................................................................9 LIST OF FIGURES .......................................................................................................................10 ABSTRACT...................................................................................................................................11 CHAPTER 1 INTRODUCTION ..................................................................................................................13 Literature Review ...................................................................................................................13 Overview of Psyllids .......................................................................................................13 Biology of the Asian Citrus Psyllid.................................................................................15 Citrus Greening Disease..................................................................................................17 Biology of Tamarixia radiata .........................................................................................19 Biology of Diaphorencyrtus aligarhensis.......................................................................20 Other Natural Enemies of D. citri ...................................................................................21 Management of D. citri ...................................................................................................21 Overview of Microbe-Insect Associations ......................................................................22 Research Objectives................................................................................................................24 2 MICROBIAL ENDOSYMBIONTS OF THE ASIAN CITRUS PSYLLID Diaphorina citri KUWAYAMA [HEMIPTERA: PSYLLIDAE] AND ITS PARASITOIDS Tamarixia radiata (WATERSTON) [HYMENOPTERA: EULOPHIDAE] AND Diaphorencyrtus aligarhensis (SHAFEE, ALAM AND AGARWAL) [HYMENOPTERA: ENCYRTIDAE]....................................................................................29 Introduction.............................................................................................................................29 Materials and Methods ...........................................................................................................31 Insect Colonies ................................................................................................................31 Surface Sterilization ........................................................................................................32 Scanning Electron Microscopy........................................................................................32 DNA Extraction...............................................................................................................32 High Fidelity Polymerase Chain Reaction ......................................................................33 Cloning and Restriction Fragment Length Polymorphism Analysis...............................34 Phylogenetic Analysis .....................................................................................................34 Antibiotic Treatment and Detection of Wolbachia in D. aligarhensis............................35 Results and Discussion ...........................................................................................................37 Surface Sterilization................................................................................................................37 High-Fidelity PCR Amplification of Symbionts in D. citri and its Parasitoids .....................40 Symbionts of D. citri .......................................................................................................40 6 Symbionts of T. radiata...................................................................................................44 Symbionts of D. aligarhensis..........................................................................................46 Antibiotic Treatment of D. aligarhensis .........................................................................47 Phylogenetic Analysis .....................................................................................................50 Conclusions.............................................................................................................................52 3 LOW INCIDENCE OF Candidatus Liberibacter asiaticus IN Diaphorina citri POPULATIONS BETWEEN NOVEMBER 2005 AND JANUARY 2006: RELEVANCE TO MANAGEMENT OF CITRUS GREENING DISEASE IN FLORIDA...............................................................................................................................66 Scientific Note ........................................................................................................................66 Summary.................................................................................................................................70 4 MORPHOLOGICAL AND MOLECULAR CHARACTERIZATION OF A Hirsutella SPECIES INFECTING THE ASIAN CITRUS PSYLLID IN FLORIDA ............................74 Introduction.............................................................................................................................74 Materials and Methods ...........................................................................................................75 Insect Colony...................................................................................................................75 Collection, Maintenance, and Cultivation of the D. citri Pathogen ................................76 Microscopy......................................................................................................................77 Bioassays .........................................................................................................................77 Molecular Analyses.........................................................................................................78 Phylogenetic Analysis .....................................................................................................79 Isolate-Specific PCR .......................................................................................................80 Results.....................................................................................................................................81 Collection, Maintenance and Cultivation of the D. citri Pathogen .................................81 Microscopy......................................................................................................................82 Bioassays .........................................................................................................................83 Molecular Analyses.........................................................................................................84
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