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Control of Sexual Reproduction in Aspergillus Species

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Control of Sexual Reproduction in Aspergillus Species School of Biology (Life Sciences) Control of Sexual Reproduction in Aspergillus Species Author: Adel Omar Ashour BSc, MSc Thesis submitted to the University of Nottingham (UK) for the degree of Doctor of Philosophy Feburary 2014 I Abstract The principal aim of the present study was to investigate biochemical, evolutionary and genetic factors that influence and control sexual reproduction in Aspergillus species. The aspergilli include species of major economic and medical importance, with some species reproducing by sexual means but many being only known to reproduce by asexual means. It was anticipated that an improved understanding of the factors controlling sexual reproduction would provide fundamental insights into biological processes controlling sex in ascomycete fungi as a whole, as well as providing insights to enable methods to be designed to promote sexual reproduction in the laboratory. The sexual cycle could then be used in classical genetic studies and strain improvement programmes. Studies were focussed mainly on three representative Aspergillus species, namely the homothallic (self fertile) Aspergillus nidulans, Eurotium repens and Neosartorya fischeri. Several isolates were obtained from different worldwide locations and their identity verified by phylogenetic means prior to main experimental work. Firstly, conditions were optimised for both sexual and asexual reproduction for each species to facilitate later experimental work. This involved growth under a variety of different environmental parameters including media type, temperature, light, dark, sealing or non-sealing of plates, and incubation in variable stack number, Interestingly it was found that highest levels of cleistothecia of the model species A. nidulans were produced at 32ºC, rather than the 37ºC routinely used in laboratories worldwide, and by incubating plates in a single layer. Secondly, investigations were made to assess whether asexual conidia and sexual ascospores of A. nidulans exhibited differential resistance to environmental stress, which might be of importance for the evolutionary maintenance of different forms of reproduction in this species. Conidia and ascospores from a variety of isolates and strains were subjected to thermal stress, involving exposure to a range of temperatures between 50ºC and 75ºC for 30 min, and in addition to UV radiation stress, involving exposure to 254 nm for different time points between 10 and II 60 min. Spore viability data for both heat and UV shock was converted to D-values, revealing that ascospores were slightly more resistant than conidia to thermal shock and had markedly greater resistance to UV shock. These results help to explain why homothallism might be retained in species that are able to produce asexual spores at much lower metabolic cost. Parallel studies with E. repens also showed that ascospores exhibited higher thermal resistance than conidia. Thirdly, the possible evolution of asexuality was studied. Previous classic work by Mather and Jinks (1958) suggested that a gradual loss of sexuality occurs when fungi are subcultured solely by asexual transfer. This claim was tested by serial asexual transfer and subsequent assessment of sexual potential for a variety of A. nidulans, E. repens and N. fischeri isolates and strains. A ‘slow decline’ in sexual fertility was indeed observed in the majority when repeatedly subcultured by asexual conidia. Staining with Hoechst 33258 and Calcofluor was used to correlate the number of mitotic divisions occurred in the apical cells with the decrease in sexual fertility for all three species. Significantly, it was found that the sexual fertility of most long-term asexual strains could be restored either partly of fully back to initial levels by propagation by ascospore transfer. This suggested that a mixture of epigenetic and mutational factors might be partly responsible for the evolution of asexuality in fungi. Finally, investigations were made to identify novel genes involved in the regulation of sexual fertility in the aspergilli. A series of gene disruption cassettes were used to delete putative high-mobility group transcription factors from the genome of A. nidulans. Deletion of one particular gene caused a loss of sexual fertility indicating that this gene acts as a sexual regulator. This gene was termed ‘steD’. Complementation work via the sexual cycle confirmed that sex could be restored by restoration of this gene. This discovery indicated that many so far unidentified genes are likely to have key roles regulating sexual fertility of A. nidulans and ascomycete fungi in general. Thus, the loss of function of a wide range of genes might lead to the evolution of asexuality in ascomycete fungi. III Acknowledgements All praise and glory be to Allah, who is the most merciful and grateful. I thank him for giving me the patience and health to finish the PhD. Sincere thanks to my family particularly my mother, brothers and sisters for continuously support during my studying and staying here in the UK. Also, I cannot forget to thank my kind father who looked after me in each second of my life before he sadly passed away in 2001. Special thanks go to my faithful-kind wife ‘Kamilia’, my lovely little daughter ‘Fatima’ and the new gorgeous son ‘Yazan’ who strongly helped and encouraged me throughout my PhD study and staying in Nottingham with their patience and love. I kindly appreciate everything in which they have done for me. I fully appreciate my supervisors Dr. Paul Dyer and Prof. David Archer for helping and supporting me to get started and to undertake this project and also for their constant advice throughout my PhD studies. I am thankful to Dr. Sameira Swilaiman who gave me a hand at the start of my lab work. Also, thanks go to Lee Shunburne, Matthew Kokolski, Marylin Wagner and Elaine for assistance and providing the lab materials and equipment. Big thanks to my colleagues in lab B58 and office 77 for their constant support. I would like to thank Dr. Asam Latif for proofreading and the Ministry of Higher Education of Libya for funding me to do my PhD. I am grateful to Dr. Tom Hartman for taking the photomicrographs of cleistothecia, and Dr. Tom Reader for advice on statistical analysis. Many thanks to Prof. Rolf Hoekstra, Dr. George Szakacs, Dr. Ozgur Bayram, Prof. Robert A. Samson and Jos Houbraken for providing some fungal isolates used in this study. Also thanks go to Prof. Michelle Momany and Prof. Susan Kaminskyj for recommending protocols to stain hyphae and nuclei of the fungal species used in this project. IV Glossary Anamorph: the asexual (‘imperfect’) form or morph characterised by the presence of conidia. Ascoma: plural is ascomata, an ascus-containing structure. Ascospore: A spore produced in an ascus by ‘free cell formation’. Ascus: a typical sac-like cell characteristic of the Ascomycota in which eight ascospores are produced after karyogamy and meiosis. Conidiophore: a simple or branched hypha bearing or consisting of conidiogenous cells from which conidia are produced. Holomorph: the whole fungus in all its morphs and phases Hülle cells: terminal or intercalary thick-walled cells, which occur in large numbers in association with the ascomata of some aspergilli, for example Aspergillus nidulans Karyogamy: the fusion of two nuclei after cell fusion, i.e. after plasmogamy. Plasmogamy: the fusion of two cells without immediate karyogamy or a precursor to karyogamy Teleomorph: the sexual (‘perfect’) form or morph, characterised by ascomata The definitions are taken from Kirk and Ainsworth (2008). V Abbreviations ACM Aspergillus complete medium AMM Aspergillus minimal medium ANOVA Analysis of variance APN2 Well conserved anaphase promoting gene bordering the MAT locus in ascomycete AspGD Aspergillus Genome Database ATP Adenosine triphosphate aw Water activity BLAST Basic local alignment search tool Bt2a Beta-tubulin 2a primer Bt2b Beta-tubulin 2b primer CDA Czapek dox agar d day(s) dH2O Distilled water DNA Deoxyribonucleic acid D-value Decimal reduction time dNTP Deoxyribonucleotide triphosphate EDTA Ethylene diamine tetraaceticacid F F factor FGSC Fungal Genetics Stock Centre VI GMEA Glucose malt extract agar HCl Hydrochloric acid HMG High-mobility group KH2PO4 Monopotassium phosphate K2HPO4 Dipotassium phosphate MAT Mating-type MEA Malt extract agar MgSO4 Magnesium sulphate M40Y Malt extract medium mRNA Messenger ribonucleic acid mtDNA Mitochondrial DNA NaCl Sodium chloride Na2HPO4 Sodium phosphate NaOH Sodium hydroxide OA Oatmeal agar ORF Open reading frame PABA Para-Amino benzoic Acid PCR Polymerase chain reaction PDOX Pyridoxine HCL PEG Polyethylene glycol psi Precocious sexual inducer VII QMC Queen Medical Centre, University of Nottingham RAPD Random amplified polymorphic DNA RNA Ribonucleic acid rpm Revolutions per minute RT-PCR Reverse transcriptase polymerase chain reaction RT Room temperature SDS Sodium dodecyl sulphate SLA2 Well conserved DNA lyase gene bordering the MAT locus in most filamentous ascomycetes TBE Tris borate EDTA buffer TEM Transmission electron microscopy Tris Tris-hydroxymethyl-methylamine or TRIZMA Tris-HCl Tris hydroxymethyl amino methane TWA Tap water agar UV Ultra violet v/v Volume fraction or volume concentration VeA Velvet gene Wk Week (s) w/v Weight per volume YEG Yeast extract glucose media Deletion mutant VIII Table of Contents Abstract ....................................................................................... II Acknowledgements ...................................................................
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