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Structure and Role of Rhizomorphs of Armillaria Luteobubalina

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Structure and Role of Rhizomorphs of Armillaria Luteobubalina Structure and role of rhizomorphs of Armillaria luteobubalina By MAMTA PAREEK A thesis submitted to the University of New South Wales in partial fulfilment of the requirement for the degree of Doctor of Philosophy School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, 2052, Australia 2006 Appendix: Acronyms Carboxy-DFFDA Oregon Green® 488 carboxylic acid diacetate CFD Computational fluid dynamics CFDA Carboxyfluorescein diacetate CMAC 7-amino-4-chloromethyl coumarin CMFDA 5-chloromethyl fluorescein diacetate DIC Differential Interference Contrast FDA Fluorescein diacetate HPTS# 8-hydroxypyrene-1,3,6-trisulfonic acid, trisodium salt MM Malt marmite PIPES Piperazine-N-N’-bis (2-ethanol sulphonic acid) PSP Pseudosclerotial plate PTS 8-hydroxypyrene-1,3,6-trisulphonate RHS Right hand side RO Reverse osmosis ROL Radial oxygen loss #also referred as PTS by many authors. Therefore, PTS has been used interchangeably for HPTS at many places as referred by other authors. i List of publications Written Publications 1. Pareek, M., Cole, L., Ashford, A.E. (2001) Variations in aerial and submerged rhizomorphs of Armillaria luteobubalina suggests that rhizomorphs are organs of absorption rather than long distance translocation. Mycological Research 105, 1377-1387. 2. Pareek, M., Ashford, A.E., Allaway, W.G. and Pareek, V. (2005) Mass transport in small-scale biological entities: An application in plant science. Paper published in 7th World Congress of Chemical Engineers. Paper number: 85553; ISBN number: 0-85295-494-8. 3. Pareek, M., Allaway, W.G., Ashford, A.E. (2006) Armillaria luteobubalina mycelium develops air pores that conduct oxygen to rhizomorph clusters. Mycological Research 110, 38-50. 4. Pareek, M., Ashford, A.E. (2006) Uptake of apoplastic and symplastic tracers by Armillaria luteobubalina rhizomorphs. (Manuscript prepared to be submitted in Mycological Research.) National/International Conferences Presenter is underlined 5. Pareek, M., Cole, L., Ashford, A.E. Are rhizomorphs of Armillaria luteobubalina are organs of absorption. Australasian Mycological Society Conference (AMSC): Cairns, Australia. (Presented as a talk in September, 2001.) ii 6. Pareek, M., Cole, L., Ashford, A.E. Structure and role of rhizomorphs of Armillaria luteobubalina. (Presented as a talk at Sydney Fungal Studies Group workshop in October, 2001.) 7. Pareek, M., Ashford, A.E., Allaway, W.G. Rhizomorphs of Armillaria luteobubalina really do have role in aeration. 7th International Mycological Conference; Oslo, Norway. (Presented as a talk in August, 2002.) 8. Pareek, M., Cole, L., Ashford, A.E. Structure, growth and permeability of rhizomorphs of Armillaria luteobubalina. 7th International Mycological Conference; Oslo, Norway. (Presented as a poster in August, 2002.) 9. Pareek, M., Ashford, A.E., Allaway, W.G. Are rhizomorphs organs of aeration? (Talk at Sydney Fungal Studies Group workshop in October, 2002.) 10. Pareek, M., Ashford, A.E., Allaway, W.G. and Pareek, V. Mass transport in small-scale biological entities: An application in plant science. (Presented a talk in 7th World Congress of Chemical Engineers, Glasgow; 10- 14 July, 2005). iii Acknowledgements First of all, I will express my deepest gratitude to my supervisor Professor A. E. Ashford for her unequivocal support to carry out this research. Despite her busy schedule, I could see her whenever I wanted and that too without a prior appointment. Without her whole-hearted support, this work would not have been possible. I indicate my thanks and indebtedness to her for all her help. I express my sincere gratitude to Professor W. G. Allaway for his timely support and advice on all aspects of this work, especially that on oxygen electrode experiments. Thanks are also due to Dr. G. Hyde and A/Prof. P. Adam for their valuable advice. The help of Dr. Louise Cole, vis-à-vis microscopy and freezing techniques, is highly appreciated. The support given by Ms. Danielle Davies, Dr. Bettye Rees, and Dr. P. Williams was also invaluable. I also thank Professor Alan Walker FAA and Dr. Vishnu Pareek for their valuable suggestions on the mathematical modelling section. I am greatly indebted to my parents and family for their support during this time. I especially thank my mother for visiting us in Perth for babysitting Mihir (our 1 year old son), who otherwise was making it impossible to finish this thesis writing. Last but not least, my husband Vishnu’s support before and during this thesis writing is highly appreciated. iv Abstract Armillaria luteobubalina is one of the most serious pathogens in Australian ecosystems causing much damage particularly in dry sclerophyll eucalypt forests. It produces rhizomorphs like other Armillaria species but at many sites they do not to extend for long distances in soil, and disease spread is caused by mycelial systems via root contact. The aim of this research was to study the growth rate, structure, possible role(s) in absorption, aeration and transport of rhizomorphs and other spatially related structures. Two different types of rhizomorphs were produced by A. luteobubalina in in vitro conditions - aerial and submerged. They differed in growth rate, amount of mucilage, extent of peripheral hyphae, degree of pigmentation and in the structure of inner cortex. Otherwise they had a similar internal structure comprising 4 radial zones, namely, peripheral hyphae, outer cortex, inner cortex and medulla. The central medullary space appeared to be a gas-filled cavity and a zone of inflated hyphae interspersed with narrow hyphae developed at the interface between inner cortex and medulla. This resembled higher plant aerenchyma. No vessel-hyphae equivalent to xylem vessels were found. To examine the role of rhizomorphs in absorption, symplastic and apoplastic tracers were applied to aerial and submerged rhizomorphs. Two membrane permeant symplastic fluorescent tracers, Oregon Green® 488 carboxylic acid diacetate (carboxy-DFFDA) and 7-amino-4-chloromethylcoumarin (CMAC), which are ultimately sequestered in vacuoles, were applied to samples (whole v rhizomorphs and/or cut sections) sectioned free hand. The apoplastic tracer 8- hydroxypyrene-1,3,6-trisulphonate (HPTS) was applied to fresh material and its localisation determined in semi-thin (dry) sections following anhydrous freeze substitution and dry sectioning. Both symplastic tracers behaved in a similar fashion in aerial and submerged rhizomorphs regardless of whether pigment was present in the outer cortical cell walls or in the extracellular material. Rhizomorphs appeared to be mostly impermeable to these probes with exception of a few fluorescent patches that potentially connected peripheral hyphae to inner cortical cells. In contrast, the apoplastic probe appeared to be impeded by the pigmentation in cell walls and/or the extracellular material in the outer cortical zone. Structures that I identified as air pores originated in cultures on agar; they arose directly from the mycelium and grew upwards into the air. As they elongated they differentiated into a cylindrical structure with a more compact basal region from which the loose parallel intertwined hyphae emerge. A cluster of rhizomorph apices is initiated immediately beneath a group of air pores shortly after they have begun to develop. Mature air pores became pigmented as did also the surface mycelium of the colony to form a crust. The pigmented surface layer, or rind, extended into the base of air pores, where it was elevated into a mound by tissue inside the base of the air pore. Beneath the rind and pseudo parenchyma there was a region of loose hyphae with extensive gas space between them. This gas space extended into the base of the air pore and was continuous with the central gas canal of rhizomorphs. The gas space was also continuous with the internal spaces of the air pore (and atmosphere) through vi gaps in the rind layer in its basal region. Oxygen is conducted through the air pores and their associated rhizomorph gas canals (with cut ends) into the oxygen electrode chamber with a conductivity averaging 679r68x10-12 m3s-1. The time averaged oxygen concentration data from the oxygen electrode chamber were used to compare three different air pore diffusion models. It was found that the widely used pseudo-steady-state model overestimated the oxygen conductivity. Finally, a model developed on the basis of fundamental transport equations (widely used in computational fluid dynamics), was used to calculate oxygen diffusivities. This model gave a better comparison with the experimental data. vii Contents APPENDIX: ACRONYMS I LIST OF PUBLICATIONS II ACKNOWLEDGEMENTS IV ABSTRACT V CONTENTS VIII CHAPTER 1. GENERAL INTRODUCTION 1 CHAPTER 2. LITERATURE REVIEW 7 2.1 Introduction 7 2.2 Nomenclature of Multi-hyphal Linear Aggregates 9 2.3 Armillaria species and their Rhizomorphs 12 2.4 Factors Affecting Growth and Development of Rhizomorphs 17 2.5 Organization of the Differentiated Rhizomorphs 22 2.6 Zone lines, Pseudosclerotial plates, Pseudosclerotia 25 2.7 Possible Roles of Rhizomorphs 27 2.7.1 Spread of the infection and survival of the fungus 27 2.7.2 Aeration 29 2.7.3 Uptake and translocation 32 2.8 Apoplastic and Symplastic Pathway 39 2.8.1 Apoplastic probes 43 2.8.2 Symplastic probes 47 2.9 Freeze Substitution 49 CHAPTER 3. STRUCTURE AND GROWTH OF SUBMERGED AND AERIAL RHIZOMORPHS OF ARMILLARIA LUTEOBUBALINA 59 3.1 Introduction 59 3.2 Materials and methods 62 3.2.1 Collection and culture of material 62 3.2.2 Growth Experiments
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