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Plant-Mediated Interactions Between the Potato Cyst Nematode, Globodera Pallida and the Peach Potato Aphid, Myzus Persicae

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Plant-Mediated Interactions Between the Potato Cyst Nematode, Globodera Pallida and the Peach Potato Aphid, Myzus Persicae i Plant-mediated interactions between the potato cyst nematode, Globodera pallida and the peach potato aphid, Myzus persicae Grace Anna Hoysted Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Centre for Plant Sciences School of Biology September 2016 ii The candidate confirms that the work submitted is her own. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgment. © 2016 The University of Leeds, Grace Anna Hoysted iii Acknowledgements I would like to thank my supervisor Prof. Peter Urwin for not only giving me the opportunity to carry out this PhD but also for all of his support, encouragement and wise words over the last four years. Also, to my secondary supervisor Prof. Sue Hartley for her advice and encouragement with all things entomological and paper writing. I would like to thank Dr. Catherine Lilley for all of the time and effort she has invested these last few years while helping me through my project (and also for keeping my haribo drawer stocked). To all members (past and present) of the Plant Nematology Group at the University of Leeds for their constant support and training, in particular Jennie and Fiona for their amazing technical support. I’d also like to thank everyone for their love of Friday cakes and tea, the annual lab day out and not forgetting the endless supply of baby animal YouTube videos ;) To all of the wonderful friends I’ve made whilst in Leeds – thank you for all those crazy lunch time conversations, wild nights out and all of the other fun times from the Lake District to Budapest. A special mention goes to Eimear Quinn, James Cooper, Jess Haigh, Jess Stott and Katie Sageman-Furnas – thank you all for being so amazing and not forgetting Vincent Agboh, Aaron Barrett and Robbie Gillet – thank you for your constant love of “treating” me to the odd Wray and Nephew. To Murri, Luna, JD, Toffee and Sam – thank you for all the animal love! To Subir – thank you for making me smile every single day during my final and most stressful year :) And last but not least a massive thank you to my amazing family – my mother Ann and my brother Karl for their constant support through all of this, for having faith in me and for always looking after me. iv Dedicated to my grandmother Rose Anne Coakley – thank you for always encouraging me to be that great scholar. v Abstract This study elucidated the relationship between the potato cyst nematode, Globodera pallida and the peach-potato aphid, Myzus persicae, two pests that can infect the potato plant and often so simultaneously. The biological, biochemical and molecular responses of potato plants suffering nematode and aphid stress were characterised both singly and in combination. It was established that the reproductive success of aphids was significantly greater on potato plants pre-infected with nematodes compared to non-infected control plants. Endogenous levels of salicylic acid (SA) increased systemically in the leaves of potato plants following nematode and aphid infection singly with a corresponding increase in expression of the SA-mediated marker gene PR-5. Measurements of endogenous levels of jasmonic acid (JA) as well as the expression of JA-mediated defence genes increased in plants infected with aphids but were suppressed when plants were co-infected with both nematodes and aphids. This suppression of JA in co-infected plants shows a different and unique response to that found when the plant was infected with either pest in isolation. These results may indicate antagonistic crosstalk between molecular pathways in the plant following infection of the plant with G. pallida and M. persicae. M. persicae had a negative amensalism effect on G. pallida below-ground whereby pre-infestation of potato plants with M. persicae stimulated a significantly lower cumulative hatch of second-stage juveniles (J2s) when cysts of G. pallida were incubated in root diffusates from aphid-infested plants. A dose-dependent response was responsible for this with the presence of 50 aphids on the foliar parts of the plant causing a significant reduction in the emergence of J2s from cysts. Sequence of arrival experiments showed that pre-infestation of M. persicae significantly reduced the infection rate of G. pallida. This work comprises the first study into dual nematode and aphid attack in the potato crop and the study highlights how multiple stresses elicit a unique molecular response to attack compared to singly stressed plants. vi Contents Acknowledgements ....................................................................................................... iii Abstract ......................................................................................................................... v List of Figures ................................................................................................................. x List of Tables ................................................................................................................ xii List of Abbreviations ................................................................................................... xiii List of Suppliers ........................................................................................................... xvi Chapter 1 Introduction ................................................................................................... 1 1.1. Biotic stress ................................................................................................................... 1 1.1.1. The basal defence response .................................................................................. 1 1.1.2. The specific defence response ............................................................................... 4 1.1.3. Phytohormones involved in pathogen signalling ................................................... 5 1.2. The biology of plant-parasitic nematodes .................................................................... 9 1.2.1. Root knot nematodes .......................................................................................... 10 1.2.2. The biology of cyst nematodes ............................................................................ 11 1.2.3. Effects of cyst nematodes on their hosts ............................................................ 14 1.3.1. Effects on aphid infestation on their hosts .......................................................... 16 1.4. Plant-mediated interactions between above-ground pests and below-ground pathogens .......................................................................................................................... 17 1.4.1. Plant-mediated interactions between aphids and nematodes ........................... 20 1.5. Project Objectives ....................................................................................................... 22 Chapter 2 ..................................................................................................................... 23 General Materials and Methods ................................................................................... 23 2.1. Biological material ...................................................................................................... 23 2.1.1. Species used ......................................................................................................... 23 2.1.2. Growth of Solanum species in soil ....................................................................... 23 2.1.3. Maintenance of cyst nematode populations ....................................................... 23 2.1.4. Extraction of G. pallida cysts from infected soil samples .................................... 24 2.1.5. Preparation of potato and tomato root diffusate ............................................... 24 2.1.6. Hatching of G. pallida cysts for collection of second-stage juveniles .................. 24 2.2. Infection of Solanum tuberosum with Globodera species .......................................... 25 2.2.1. Infection with juvenile G. pallida and G. rostochiensis ........................................ 25 2.2.2. Staining of nematodes with acid fuchsin ............................................................. 25 vii 2.3. Infestation of Solanum tuberosum with Myzus persicae ............................................ 27 2.3.1. Maintenance of aphid culture ............................................................................. 27 2.3.2. Aphid infection of potato plants .......................................................................... 27 2.3.3. Co-infection of potato plants with both nematodes and aphids ........................ 27 2.4. Quantitative RT-PCR analysis of pathogenesis-related (PR) gene expression in the leaves of potato plants ...................................................................................................... 29 2.4.1. Extraction of total RNA ........................................................................................ 29 2.4.2. Reverse transcription of RNA ............................................................................... 29 2.4.3. qPCR primer design .............................................................................................. 30 2.4.4. Quantitative reverse transcriptase (RT)-PCR ....................................................... 30 2.5. Quantification of phytohormones in the leaves of potato
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