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IDENTIFICATION, PREVALENCE and IMPACTS of VIRAL DISEASES of UK WINTER WHEAT LAURA JANE FLINT, Bsc. Thesis Submitted to the Unive

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IDENTIFICATION, PREVALENCE and IMPACTS of VIRAL DISEASES of UK WINTER WHEAT LAURA JANE FLINT, Bsc. Thesis Submitted to the Unive IDENTIFICATION, PREVALENCE AND IMPACTS OF VIRAL DISEASES OF UK WINTER WHEAT LAURA JANE FLINT, BSc. Thesis submitted to the University of Nottingham for the degree of Doctor of Philosophy December 2013 Abstract The potential for viruses to be causing the plateau in the yield of UK wheat (Triticum aestivum) was investigated. Mechanical inoculation of Cynosurus mottle virus to wheat cv. Scout and cv. Gladiator caused 83% and 58% reduction in the number of grains produced, highlighting the potential of viruses to cause disease and yield loss. Viruses historically detected in cereals in the UK were not found to be prevalent following real time reverse transcriptase polymerase chain reaction testing of 1,356 UK wheat samples from 2009-2012 using eleven assasys developed in the project. This included an assay for Cynosurus mottle virus, which was based on its complete genome sequence which was obtained for the first time in this project. Viruses detected were Barley yellow dwarf virus-MAV (6 samples) (BYDV-MAV), Barley yellow dwarf virus-PAV (6 samples) (BYDV-PAV) and Soil-borne cereal mosaic virus (12 samples) (SBCMV). There was a higher prevalence of viruses in the south, thought to be due to warmer temperatures which benefitted insect vectors and the molecular processes of infection. Viruses were most commonly detected in the variety JB Diego, perhaps because this variety has no known resistance to viruses. The low prevalence of known viruses could also have been because they were outcompeted or replaced by previously unknown ones. Next generation sequencing was used to test 120 samples from an organic site, including wheat, weeds and insects, to search for novel viruses. Testing of twelve storage regimes for insect traps using BYDV-PAV infected Sitobion avenae for recovery of PCR amplifiable RNA using 18S rRNA and BYDV-PAV assays found that 0.5 M EDTA was the most successful regime which was therefore used in the collection of samples for sequencing. Known viruses such as BYDV-PAV were detected along with some additional potentially novel viruses (eight possibly novel viruses or strains of viruses with four in wheat). One such virus was apparently present in 25% of all wheat I samples tested, making it potentially very significant. This could be important for unlocking the yield potential of wheat because it could be a cryptic virus which is highly prevalent. In order to control the spread of viruses their methods of transmission must be understood, therefore testing of seeds and resulting plants from Cynosurus mottle virus infected material was done. Tests did not detect the virus, therefore it was concluded that seed transmission does not occur. However, further tests are required. In conclusion this study indicates that known viruses are not currently a major problem for UK winter wheat. However, novel viruses that are a problem may be detected in the future perhaps by next generation sequencing. Additonal viruses from abroad would add to the threat. The impact of all viruses in wheat may be greater in the future due to climate change. II Acknowledgments I would like to thank my supervisors Prof Matthew Dickinson, Prof Neil Boonham, Adrian Fox and Dr Judith Turner for their advice and support throughout this project. I appreciate it a lot, thank you. In addition thank you to all staff and students at The Food and Environment Research Agency (Fera) who have always offered guidance and have become friends. In particular I would like to thank Dr Ian Adams, Ben Barratt, Samantha Bennett, Ian Brittain, Mark Daly, Tracey Chantry, Rachel Glover, Val Harju, Dr Toby Hodges, Dr Jennifer Hodgetts, Dr Philip Jennings, Louisa Kitchingman, Lynn Laurenson, Dr Jeff Peters, Dr Stephane Pietravalle, Anna Skelton, Danny Skelton, Dr Moray Taylor, Gilli Thorp and Dr Jennifer Tomlinson. Thank you also to staff of the Imaging department at The University of York, especially Meg Stark, for use of their transmission electron microscope. Thank you to the funders of this project who were the cereals and oilseed division of the Agriculture and Horticulture Development Board (AHDB-HGCA) and Defra Seedcorn. It’s been great getting to know some of those from the HGCA at annual seminars and Cereals and I’ve also appreciated the help when publishing requests for samples. In a similar vein thank you to Farmers Guardian, Farmers Weekly and other publishers of the sample request. Further to that thank you to the farmers and commercial partners who sent samples to me. Last, but my no means least thank you to mum, dad, Thomas and Tim for your support during this project, I am very grateful. III Contents Page Abstract I Acknowledgments III Contents IV List of Figures XVII List of Tables XXII List of viruses XXIV List of abbreviations XXVII Chapter 1 - Introduction 1 1.1 The importance of wheat 1 1.2 Wheat production in the UK and globally 1 1.3 The changing yield of wheat in the UK 2 1.4 Could viruses help explain the current plateau in the yield of wheat? 4 1.5 Introduction to viruses and their impacts on wheat 7 1.6 Transmission methods of viruses 11 1.7 Control measures for viral diseases of wheat 14 1.8 Climate change – to date and for the future 17 1.9 Trade-offs when attempting to improve wheat yields 27 1.10 Diagnosis of viruses of wheat 28 1.11 A review of viruses of wheat and other members of the Gramineae 34 1.11.1 Viruses of wheat reported in the UK, and their incidence in Europe and 35 globally 1.11.1.1 Agropyron mosaic virus 35 1.11.1.2 Aubian wheat mosaic/Bedford virus 36 IV 1.11.1.3 Barley yellow dwarf virus 37 1.11.1.4 Cocksfoot mild mosaic virus 42 1.11.1.5 Cocksfoot mottle virus 43 1.11.1.6 Cocksfoot streak virus 44 1.11.1.7 Cynosurus mottle virus 44 1.11.1.8 European wheat striate mosaic virus 45 1.11.1.9 Oat chlorotic stunt virus 46 1.11.1.10 Oat mosaic virus 46 1.11.1.11 Ryegrass mosaic virus 47 1.11.1.12 Soil-borne wheat mosaic virus/Soil borne cereal mosaic virus 48 1.11.1.13 Wheat spindle streak mosaic virus 49 1.11.2 Viruses of Gramineae (not reported in wheat to date) reported in the UK, 50 and their incidence in Europe and globally 1.11.3 Other viruses of wheat reported in Europe, but not currently known in the 52 UK 1.11.3.1 Barley stripe mosaic virus 52 1.11.3.2 Barley yellow striate mosaic virus 53 1.11.3.3 Brome mosaic virus 54 1.11.3.4 Brome streak mosaic virus 54 1.11.3.5 Festuca leaf streak virus 54 1.11.3.6 Flame chlorosis virus 55 1.11.3.7 Soil-borne wheat mosaic virus 55 1.11.3.8 Sugarcane mosaic virus 56 1.11.3.9 Wheat dwarf virus 56 1.11.3.10 Wheat streak mosaic virus 57 V 1.11.4 Viruses of Gramineae (not reported in wheat or in the UK to date) and their 59 incidence in Europe and globally (excluding viruses mentioned in 1.11.2) 1.11.5 Other viruses of wheat reported globally (excluding those in 1.11.1 and 60 1.11.3) 1.11.6 Viruses of Gramineae (not reported in wheat or the UK to date) reported 65 globally (excluding those in 1.11.2 and 1.11.4) 1.12 Significant viruses 66 1.13 Mission statement 67 1.14 Aims 68 Chapter 2 - Methods 69 2.1 CTAB extraction 69 2.2 Total nucleic acid extraction by Kingfisher96 69 2.3 Standard qRT-PCR cycling conditions 70 2.4 ELISA 70 2.5 Mechanical inoculation 70 Chapter 3 - Annual survey of wheat for viruses 71 3.1 Introduction 71 3.2 Materials and methods 71 3.2.1 Selection of viruses to test for 71 3.2.2 qRT-PCR assay design 72 3.2.2.1 Positive control material 72 3.2.2.2 Specificity testing of the qRT-PCR assays 73 3.2.2.3 Troubleshooting selected qRT-PCR assays 73 3.2.2.3.1 Re-extraction of positive controls 73 3.2.2.3.2 Sequencing products of qRT-PCR 73 VI 3.2.2.3.3 Oat mosaic virus assay 73 3.2.3 The survey 74 3.2.3.1 Winter wheat samples 74 3.2.3.1.1 Defra winter wheat disease survey samples 74 3.2.3.1.2 Other samples 79 3.2.3.2 Extraction of total nucleic acid from survey samples 79 3.2.3.3 Preparation of plates for qRT-PCR testing of survey samples 80 3.2.3.4 Repeats of possible positive results 80 3.3 Results 80 3.3.1 Assay development 80 3.3.1.1 Assay specificity tests 80 3.3.1.2 Troubleshooting the assays 81 3.3.1.2.1 Extraction of fresh samples of RgMV, BYDV-MAV, BYDV-PAV and OMV 81 3.3.1.2.2 Sequencing qRT-PCR products 81 3.3.1.2.3 Oat mosaic virus 82 3.3.2 The main survey 83 3.3.2.1 Wheat phenylalanine ammonia-lyase assays 83 3.3.2.2 Survey results 85 3.3.2.2.1 2009 85 3.3.2.2.2 2010 85 3.3.2.2.3 2011 85 3.3.2.2.4 2012 86 3.3.2.3 Viruses found in wheat by the virology department at Fera 89 3.4 Discussion 90 3.4.1 Assay development 90 VII 3.4.2 The main survey 91 3.4.2.1Wheat phenylalanine ammonia-lyase assay 91 3.4.2.2 Cut off values for positive results 92 3.4.2.3 Results of the assays for viruses 93 3.4.2.4 Climate data 95 3.4.2.5 Location of viruses 97 3.4.2.6 The viruses which were not found in this survey 100 3.4.3 Discussion of methods 101 3.4.3.1 Specificity testing of assays 101 3.4.3.2 Extraction method 101 3.4.3.3 Check for inhibitors in wheat samples 102 3.4.3.4 Choice of diagnostic method 102 3.4.3.5 Samples 103 3.5 Conclusion 105 Chapter 4 - Using next-generation sequencing technology to search for novel 107 wheat viruses 4.1 Introduction 107 4.2 Materials and methods 108 4.2.1 Sample collection 108 4.2.2 Investigating storage regimes for insect traps for the preservation of insect 109 and viral RNA 4.2.2.1 Introduction 109 4.2.2.2 Establishing a set of BYDV-PAV infected insects and natural variation 110 (baseline) testing 4.2.2.3 Testing storage regimes 111 VIII 4.2.2.4 Rationale for regime choices 111 4.2.2.5 Statistical analysis 113 4.2.2.6 Establishing a set
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