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Myooviruses in Isolates of Gaeumannomyces And MYOOVIRUSES IN ISOLATES OF GAEUMANNOMYCES AND PHIALOPHORA SPECIES BY Rose Mary McGinty Thesis submitted to the University of London for the degree of Doctor of Philosophy Biochemistry Department, Plant Pathology Department, Imperial College of Rothamsted Experimental Station, Science and Technology, Harpenden, London, Hert fordsh ire, SW7 2AZ. AL5 2JQ. 1981 To my Mother 3 MYCOVIRUSES IN ISOLATES OF GAEUMANNOMYCES AND PHIALOPHORA SPECIES By Rose Mary McGinty ABSTRACT Characterisation of virus particles from the avirulent or weakly pathogenic parasites of cereal roots, Phialophora graminicola (Pg), Phialophora species with lobed hyphopodia (P.sp.(lh)) and Gaeumannomyces graminis var. graminis (Ggg) is described. These fungi can cross protect cereal roots from damage caused by Gaeumannomyces graminis var. tritici (Ggt), the causal agent of "take-all" disease of wheat and barley. Total nucleic acid was extracted frcm the mycelium of each of 12 field isolates of the weakly pathogenic fungi. Extracts were treated with DNAse and RNAse under appropriate conditions to remove DNA and single-stranded RNA respectively, and the remaining dsRNA was then analysed by polyacrylamide gel electrophoresis. Eight isolates were found to contain dsRNA, with components varying from two to five in number for different isolates. Molecular weights of the dsRNA components ranged from 1x10 to greater than 6 x 10 . Isometric virus particles were extracted and purified from three of the isolates found to contain dsKNA, one each from the species Pg, P.sp. (lh) and Ggg. Evidence was obtained for the presence of two sero- logically unrelated viruses in P.sp. (lh), both of which were 35 nm in diameter. Each virus had a capsid composed of one type of polypeptide (molecular weights 65,500 and 60,700 respectively) and each had three c dsRNA components with molecular weights in the range 1.03 x 10 c to 1.32 x 10°. A magnesium dependent RNA polymerase was found associated with the virus particles in P.sp.(lh) and a single stranded RNA product was identified. Nucleic acid hybridisation between the single stranded transcripts of one virus and the double stranded RNA genomes of each virus suggested that the two viruses have a dsRNA component in common. Single viruses were extracted from both Ggg and Pg. The former virus had a diameter of 35 nm and had a major capsid component with a molecular weight of 64,000 and four dsRNA components with molecular weights in the range 1.16 x 10^ to 1.63 x 106. The virus of Pg_ had a diameter of 30 nm and four dsRNA components with molecular weights in the range 1.14 x 106 to 1.32 x 106. 4 Interactions of the three isolates of P.sp.(lh), Pc[ and Ggg with seven isolates of Ggt on three different solid media were examined. No evidence for inhibition of Ggt by the three weakly pathogenic isolates was obtained; on the contrary all seven Ggt isolates were found to inhibit the growth of the weakly pathogenic isolates over the pH range 3.5 to 7.0, with optimal pH for this effect at pH 4.0 to 5.0. Inhibition at a distance was observed, although no killing of hyphae occurred. Culture filtrates were shown to contain a stable, diffusible but non- proteinaceous inhibitor. The significance of these results in relation to the biology of the Gaeumannomyces-Phialophora complex and prospects for the practical control of the "take-all" disease are discussed. 5 ACKNOWLEDGEMENTS I would particularly like to thank Dr. K.W. Buck and Dr. C.J. Rawlinson for their help, advice and support during the course of this work. I thank Professor B.S. Hartley and Mr. E. Lester for the use of the facilities of the Biochemistry Department, Imperial College and the Plant Pathology Department at Rothamsted Experimental Station respectively. I thank Dr. C.J. Rawlinson and Dr. M. Almond for the generous gifts of antisera to Phialophora and Gaeumannomyces viruses and Dr. R.F. Bozarth for the gift of Helminthosporium maydis dsRNA. I thank Dr. K.W. Buck for permission to copy Tables 1 and 2 (Buck, 1980) and Table 9 (Buck et al., 1981) and Dr. T.W. Young for permission to copy Table 3 (Young and Yagui, 1978). I thank Mr. I.P. Blench and Dr. G. Ratti for helpful advice and discussions, Mr. R. Woods for electron microscopy, Mr. G. Millhouse, Mr. G. Higgins and Mr. F. Cowland for photography and Mrs. V. Souilah for her excellent typing. The receipt of a Science Research Council studentship is gratefully acknowledged. CONTENTS PAGE TITLE PAGE 1 ABSTRACT 3 ACKNOWLEDGEMENTS 5 CONTENTS i - viii INTRODUCTION 14 Discovery and occurrence of dsRNA 14 mycoviruses Transmission of mycoviruses 14 Properties of dsRNA mycovirus particles 17 in vitro Effect of dsRNA mycoviruses on their hosts 22 DsRNA and the killer phenomenon 25 Mycoviruses in the take-all fungus 34 The take all disease 34 Control of take-all disease 35 Cross-protection of cereals against take-all disease with weakly pathogenic or avirulent 38 root parasites : possible role of viruses Aims and approach to the investigation 42 ii PAGE ABBREVIATIONS 44 MATERIALS 47 GENERAL METHODS 48 G.M.1. ORGANISMS AND MICROBIOLOGICAL METHODS 48 G.M.2. ISOLATION AND PURIFICATION OF VIRUS 51 a. Small scale preparation of crude virus 51 b. Large scale preparation of crude virus 51 c. Purification of large scale virus 52 preparations by sucrose density gradient centrifugation d. Purification of small scale virus 53 preparations G.M.3. ELECTRON MICROSCOPY 53 G. M. 4. SPECTROPHOTOMETRY 54 G.M.5. PREPARATION OF ANTISERA 54 G.M.6. OUCHTERLONY GEL IMMUNODIFFUSION TEST 55 G.M.7. PREPARATION OF DEAE CELLULOSE 55 G.M.8. PREPARATION OF CF11 CELLULOSE 56 G.M.9. PREPARATION OF SP C-50 SEPHADEX 56 iii PAGE G.M.10. ANALYTICAL ULTRACENTRIFQGATION 56 a. Determination of sedimentation coefficient 56 of virus b. Determination of buoyant density of virus 57 G.M. 11. DETERMINATION OF DENSITY OF CAESIUM 63 CHLORIDE SOLUTIONS G.M.12. NUCLEIC ACID EXTRACTION 64 a. Preparation of total nucleic acid from 64 mycelia b. Preparation of virus RNA 64 G.M.13. ACTION OF NUCLEASES ON TOTAL FUNGAL 65 NUCLEIC ACID AND VIRAL RNA a. Action of DNAse I 65 b. Action of RNAse A 65 G.M. 14. PREPARATION OF EDTA - WASHED PHENOL 65 G.M.15. PREPARATION OF DIALYSIS TUBING 66 G.M. 16. ANALYTICAL GEL ELECTROPHORESIS 66 a. Agarose gel electrophoresis for analysis of 66 intact virus b. Agarose gel electrophoresis for analysis of 67 nucleic acid c. Polyacrylamide gel electrophoresis for analysis 67 and molecular weight determination of nucleic acid i. For dsRNA analysis 67 ii. For dsRNA and ssRNA analysis 68 iv PAGE d. Polyacrylamide gel electrophoresis for 69 analysis and molecular weight deter- mination of polypeptide. e. Combined analysis of intact virus and polypeptide 70 G.M. 17. GLYOXALATION OF DSRNA 71 G.M. 18. SNA-DEPENDENT FNA POLYMERASE ASSAY 71 G.M. 19. PREPARATION OF VIRUS SSRNA TRANSCRIPTS 72 IN VITRO G.M. 20. RNA-RNA HYBRIDISATION ASSAY 72 G. M. 21. FLUOROGRAPHY 73 G.M. 22. SLICING AND SOLUBILISATION OF POLYACRYLAMIDE 74 GELS FOR RADIOACTIVE ANALYSIS G.M.23. INCOMPATIBILITY TESTS OF FUNGAL ISOLATES 74 G.M. 24. PRODUCTION OF INHIBITOR IN LIQUID CULTURE 74 G.M.25 WELL TESTS FOR INHIBITORY ACTIVITY OF CULTURE 75 FILTRATES G.M. 26. TESTS FOR SENSITIVITY OF INHIBITOR TO PROTEASES 75 SECTION 1 - Screening of field isolates of P.sp.(lh)f 77 Ggg and Pg_ for the presence of dsRNA RESULTS 77 DISCUSSION 171 PAGE SECTION 2 - Isolation and properties of virus 89 particles from P.sp.(lh) RESULTS 89 A. Preparation of crude virus 89 B. Purification of virus by sucrose 90 density gradient centrifugation a. Small scale purification of virus 90 b. Large scale zonal purification of virus 90 C. Properties of purified particles 93 a. U.V. spectrum 93 b. Particle morphology 93 c. Sedimentation coefficient 93 d. RNA components 99 e. Polypeptide components 102 D. Preliminary evidence that purified 107 virus preparations contain two distinct viruses in P.sp.(lh)2-2 a. Serology of P.sp.(lh)2-2 virus 107 b. Electrophoretic separation of the 107 viruses on agarose gels c. Fractionation of RNA and polypeptide 110 components across a sucrose gradient. E. Separation of the viruses of P.sp.(lh)2-2 112 F. Properties of each individual virus 117 a. Particle morphology 117 b. U.V. spectra 123 vi PAGE c. Sedimentation coefficients for virus A 123 and virus B d. dsRNA components 123 e. Polypeptide components 128 f. Serology 128 g. Buoyant density 128 G. Virion associated RNA polymerase activity 131 a. Properties of the RNA polymerase reaction 131 b. Analysis of reaction products 136 c. Cross hybridisation experiments 144 H. Alterations of dsRNA migration patterns 145 of viruses A and B repeated fungal subculture DISCUSSION 147 SECTION 3 - Isolation of virus particles from Ggt 159 isolate 45/10 RESULTS 159 A. Comparison of two media for fungal growth 159 prior to virus preparation by the PEG method i. Basal and CSL medium 159 ii. Weste and Throwers medium 160 B. Comparison of four different buffers for 163 virus preparation by the PEG precipitation method and by direct pelleting i. Direct pelleting method 165 ii. PEG precipitation method 165 DISCUSSION 171 VI1 PAGE SECTION 4 - Isolation and properties of virus 174 particles from Ggg isolate G1 RESULTS 174 A. Preparation of crude virus 174 B. Purification of virus by sucrose 174 density gradient centrifugation C. Purification of virus by caesium 176 chloride density gradient centrifugation D. Properties of purified virus particles 176 a.
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