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Abstract Adaptation of the Ballistospore Discharge ABSTRACT ADAPTATION OF THE BALLISTOSPORE DISCHARGE MECHANISM AMONG POROID AGARICOMYCETES by Yunluan Cui Most poroid basidiomycetes produce spores in vertically aligned fertilized hymenia in the form of tubes. The violently discharged spores must be propelled over limited distances to avoid impaction on the opposing surfaces of the tubes. Based on the widely accepted spore discharge model, we aim to find the keys that control the spore discharge distance, in order to reveal how ballistospores are adapted to the wide range of tube sizes. The study involved the use of a high- speed video camera to record the spore discharge process, and morphological studies of the basidiospores using scanning electron microscopy. Our models suggest that the size of Buller’s drop, irrespective of spore size and mass, is the primary determinant of discharge distance. Meanwhile, the diverse morphology of ballistospores plays an important role in determining the final size of Buller’s drop. ADAPTATION OF THE BALLISTOSPORE DISCHARGE MECHANISM AMONG POROID AGARICOMYCETES A Thesis Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Master of Science Department of Botany By Yunluan Cui Miami University Oxford, Ohio 2009 Advisor ____________________ Nicholas P. Money Reader ____________________ Richard C. Moore Reader ____________________ M. Henry H. Stevens TABLE OF CONTENTS CHAPETER Page 1. INTRODUCTION 1 1.1 Background on Agaricomycetes 1 1.1.1 Poroid Agaricomycetes Diversity 2 1.1.2 Basidium Development 3 1.1.3 Morphology and Diversity of Basidiospores in Poroid Fungi 4 1.1.4 Introduction to Polypores Used in the Research 5 1.2 Hypotheses of Spore Discharge Mechanisms 6 1.2.1 Jet Propulsion Mechanism 8 1.2.2 Turgid Cell Rounding-off Mechanism 8 1.2.3 Gas Bubble Explosion Mechanism 9 1.2.4 Electrostatic Propulsion Mechanism 9 1.2.5 Surface Tension Catapult Mechanism 10 1.3 Dispersal of Basidiospores in Tubes 11 1.4 Significance of the Research 12 2. MATERIALS AND METHODS 14 2.1 Organisms 14 2.2 Microscopy 14 2.2.1 Ultra-high-speed Video and Conventional Video Microscopy on Spore Discharge 14 2.2.2 Spore Morphology Studies with Scanning Electron Microscopy 15 3. HYPOTHESES AND MATHEMEDICAL MODELING 17 3.1 Slight Effect of the Spore Size on the Discharge Distance 17 3.2 Involvement of Buller’s Drop in Determining Spore Discharge Distance 18 3.3 Hypothesized Factors Affecting the Size of the Buller’s Drop 19 ii 4. DATA ANALYSES AND RESULTS 21 4.1 Data Obtained from Conventional Video and Ultra-high-speed Video 21 4.2 Development Rate of the Buller's Drop 22 4.3 Ballistospore Morphology 23 5. DISCUSSION 24 5.1 Spore Morphology and the Size of the Buller’s Drop 24 5.2 Evolutionary Trend between the Spore Size and the Pore or Tube Sizes 25 REFERENCES 27 iii LIST OF TABLES Page 1. Ballistospore discharge in three polypores 33 2. Sizes of spores and hilar appendix in three polypores 33 iv LIST OF FIGURES Page 1. Diverse hymenophore structures in Ganoderma applanatum, Pycnoporus cinnabarinus, Trametes hirsuta, Laetiporus sulphae, Trametes versicolor, and Ganoderma lucidum 34 2. Basidia bearing ballistospores in Polyporus squamosus and b, Polyporus badius 35 3. Morphology of six polypore species 36 4. Spore discharge process in Polyporus squamosus 37 5. The process of ballistospore shedding from sterigma 38 6. Pathway of spores after discharge from the inner surface of tubes in a poroid fruiting body 39 7. Relationship between the pore diameter and the wall thickness 40 8. Relationship between the spore volume and the tube size 41 9. 3-D image showing the relationship between the spore sizes, the Buller’s drop sizes, and the spore discharge distance 42 10. Effects of spore morphology on the development of Buller’s drop 43 11. Development rate of the Buller's drop in Polyporus squamosus 44 12. Scanning electron micrographs of spores and basidia 45 13. Successive images showing spore discharge in Trametes versicolor 47 14. Deposit of spores along the inner side of the tubes in Trametes versicolor 48 v APPENDICES Page Appendix A. Development of a typical basidium 49 Appendix B. Different types of mature basidia 50 Appendix C. Scanning electron micrograph showing the structure of a ballistospore in Coprinus cinereus: Agaricomycotina 51 Appendix D. Subdivision in Basidiomycotina 52 vi ACKNOWLEDGEMENT I would like to give my deepest thanks to my advisor Dr. Nicholas P. Money for his patience and warm heart during my master’s research. He has had a great impact on me during my graduate program so far, as well being a scientific mentor and motivator. His professional guidance and encouragement allowed me to feel confident to voice my ideas and opinions about the project. My sincere thanks are also provided to my committee members, Dr. M. Henry H. Stevens and Dr. Richard C. Moore. Their constant support has allowed me to achieve my research goals. Dr. M. Henry H. Stevens selflessly donated his time towards helping me with the statistical analyses. Dr. Mark W. F. Fischer, from College of Mount St. Joseph in Cincinnati, also contributed substantial guidance and brought his perspective and mathematical models to my work. More importantly, the scientific insights and discussions of all the faculty members in my research area greatly improved the completion of this document. Without the support from the faculties, staffs, and students in Department of Botany, I would not have been able to complete my work. I would especially like to thank Jessica L. Stolze- Rybczynski for her amazing help and teaching me how to use the high-speed-video camera and analysis software. Meanwhile, during this project, I learned a lot about electron microscopy from Dr. Richard E. Edelmann and Mr. Matt Duley, who are very experienced in this field, and thank them a lot for all their technical assistance to teach me how to use the scanning and transmission electron microscope. Finally, but most importantly, I would like to thank my parents for their unlimited love to support me to study abroad in America. They encouraged me to go after my dreams, and gave me the confidence to achieve them. My lovely sister gave her endless care about my study and life in American, which also motivated me a lot during my research. I am indebted to the people and organizations that ensured the financial support for this research. Major funding was provided through NSF award 0743074 (to NPM and Diana J. Davis) and the Academic Challenge Program in the Department of Botany, Miami University. vii Chapter 1 Introduction 1.1 Background on Agaricomycetes The fungi kingdom represents a large group in the global ecosystem, and at this time, 70,000 species have been recorded, and new species are still added to update the list (Hawksworth, 1991). As the second largest group of fungi, the Basidiomycota alone consists of 30,000 species, ranked after the Ascomycota, and includes the most diverse fungi in the world (Kirk et al., 2001). The long history of the group is traced back to the Late Devonian, when definitive Basidiomycota fossils were found. The Basidiomycota is further divided into three subphyla: Pucciniomycotina, Ustilaginomycotina, and Agaricomycotina, all of which are characterized by the basidium, a spore-bearing cell. The first two subphyla include the most familiar plant pathogens, causing corn rust and wheat smut. The Agaricomycotina are featured by the hymenia consisting of a layer of basidia under the fruiting bodies, which develop either not enclosed or only with a veil. Three classes in Agaricomycotina include the Agaricomycetes, Dacrymycetes, and Tremellomycetes. The tissue layer of basidia called hymenia under the fruiting bodies of the mushroom-forming fungi develop either not enclosed or only with a veil. Translucent jelly fungi and many yeast-forming species are in the clades of the Dacrymycetes and Tremellomycetes (Hibbett, 2007). The remaining 98% of the 20,000 recorded species in Agaricomycotina belong to Agaricomycetes, which include common mushrooms, bracket fungi, puffballs, and others (Hibbett, 2007). All the members of the clades are characterized by the production of basidiocarps, a multicellular structure on which the hymenium is borne. The size ranges from a few millimeters across to greater than one meter across (Gilbertson and Ryvarden, 1986). Though species share common characteristics, many have their own unique characteristics in terms of shape, color, and size. Further classification into orders includes Polyporales, Boletales, Agaricales and other mushroom-forming fungi. The diverse patterns of fruiting bodies of Agaricomycetes are unmatched by other fungi, including poroid fungi, gilled fungi, tooth fungi, coral fungi, and crust fungi. The caps (i.e., pileus) usually take on a form of umbrella, bell, conical or convex, and others are bracket-shaped - 1 - or crustlike resupinate forms, which may be supported by central or off-center stalks of different length, or are unstalked. Fertilized hymenial tissues underneath the cap are organized in different ways to give diverse patterns of tubes (Polyporales), gills (Agaricales), teeth (Cantharellales), and some directly exposed to the air. For example, Auriscalpium vulgare has a toothed hymenium; Fomitopsis pinicola is a poroid bracket fungus; Philebia chrysocra appears in a resupinate form; and Ramaria botrytis takes on a coral form. The morphological diversity fully reflects that Agaricomycetes have evolved in multiple directions. 1.1.1 Poroid Agaricomycetes Diversity The polyporales (earlier known as Aphyllophorales) are a large group in basidiomycetes, and evolved in polyphyletic direction (Hibbett and Donoghue, 1995; Binder and Hibbett, 2002). The habitats of poroid Agaricomycetes extend widely; many species develop on wood and lack fully developed stems; the fruiting bodies are shelf-like or crust-like, while some have more or less central stems and grow at the base or on the trunk of trees, and a few appear to develop on soil.
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