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Analysis of Cereal Aphid Feeding Behavior and Transcriptional Responses Underlying Switchgrass-Aphid Interactions

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Analysis of Cereal Aphid Feeding Behavior and Transcriptional Responses Underlying Switchgrass-Aphid Interactions University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Dissertations and Student Research in Entomology Entomology, Department of 8-2017 Analysis of Cereal Aphid Feeding Behavior and Transcriptional Responses Underlying Switchgrass-Aphid Interactions Kyle G. Koch University of Nebraska-Lincoln Follow this and additional works at: https://digitalcommons.unl.edu/entomologydiss Part of the Entomology Commons Koch, Kyle G., "Analysis of Cereal Aphid Feeding Behavior and Transcriptional Responses Underlying Switchgrass-Aphid Interactions" (2017). Dissertations and Student Research in Entomology. 51. https://digitalcommons.unl.edu/entomologydiss/51 This Article is brought to you for free and open access by the Entomology, Department of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Dissertations and Student Research in Entomology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. ANALYSIS OF CEREAL APHID FEEDING BEHAVIOR AND TRANSCRIPTIONAL RESPONSES UNDERLYING SWITCHGRASS-APHID INTERACTIONS by Kyle Koch A DISSERTATION Presented to the Faculty of The Graduate College at the University of Nebraska In Partial Fulfillment of Requirements For the Degree of Doctor of Philosophy Major: Entomology Under the Supervision of Professors Tiffany Heng-Moss and Jeff Bradshaw Lincoln, Nebraska August 2017 ANALYSIS OF CEREAL APHID FEEDING BEHAVIOR AND TRANSCRIPTIONAL RESPONSES UNDERLYING SWITCHGRASS-APHID INTERACTIONS Kyle Koch, Ph.D. University of Nebraska, 2017 Advisors: Tiffany Heng-Moss and Jeff Bradshaw Switchgrass, Panicum virgatum L., is a perennial warm-season grass that is a model species for the development of bioenergy crops. However, the sustainability of switchgrass as a bioenergy feedstock will require efforts directed at improved biomass yield under a variety of stress factors. The objectives of this research were to: (1) elucidate greenbug and yellow sugarcane aphid feeding behavior on resistant and susceptible switchgrasses using electronic penetration graphs (EPG), (2) define transcriptional changes before and during insect feeding through RNA-seq to identify candidate resistance genes in a hybrid switchgrass cultivar, and (3) utilize methods in RNA sequencing of insects to uncover key transcriptional regulatory mechanisms involved in switchgrass-aphid interactions. Electronic penetration graphs on V3 switchgrass corroborated previous work detailing greenbug feeding behavior on V1 grasses. Greenbugs were unable to sustain phloem ingestion on resistant Kanlow plants. However, significant differences were not documented for yellow sugarcane aphid feeding behavior on V1 and V3 switchgrass. Transcriptional changes during insect feeding revealed that both aphids induced remodeling of the transcriptome in the hybrid switchgrass cultivar, KxS. KxS upregulated reactive oxygen species (ROS) metabolizing enzymes and downregulated genes in primary metabolism. Downregulation of genes associated with primary metabolism could effectively starve aphids of nutrients and/or direct resources to the production of defense-related metabolites. However, greenbugs and yellow sugarcane aphids induced divergent defense responses, including phytohormone signaling pathways and metabolite expression. KxS plants responded to yellow sugarcane aphid feeding, but not greenbugs, by inducing genes associated with a flavonoid biosynthesis pathway. Characterizing the molecular response of greenbugs and yellow sugarcane aphids revealed an induction of genes associated with carbohydrate synthesis/metabolism on switchgrass, potentially to compensate for insufficient nutritional resources from the plants. Genes involved in xenobiotic metabolism were increased in aphids that had been starved or fed switchgrass, including Cytochrome P450s. Moreover, proteases were broadly induced in greenbugs that had feed on switchgrass, presumably to overcome plant protease inhibitors. Together, these studies present critical information for improving our knowledge of the plant-aphid interactions within this system and may help in characterizing specific mechanisms of resistance. i Acknowledgments I express my sincerest appreciation for my major advisors, Drs. Tiffany Heng-Moss and Jeff Bradshaw, whom provided support, guidance, and mentorship throughout my degree program. I also express my sincere gratitude to my supervisory committee members, Drs. Gautam Sarath, Joe Louis, and Keenan Amundsen for their valuable input, critiques, advice, and support throughout my PhD program. I would also like to thank Drs. Sarath and Lisa Baird for all the time and effort they invested into helping me work out the callose experiments and for their guidance and mentorship in those research challenges. I sincerely thank Dr. Lia Marchi-Werle, Dr. Travis Prochaska, Dr. Mitch Stamm, Katie Keller, Kait Chapman, Hillary Fischer, Raihanah Hassim and Brittney Reinsch for their assistance and contributions to this research. I would like to thank Drs. Teresa Donze-Reiner and Nathan Palmer, whom contributed significantly to this work and for taking the time to teach me molecular techniques. I also thank the faculty and staff in the Entomology Department at the University of Nebraska-Lincoln for all the support, guidance, and conversations. In addition, thank you to the USDA-NIFA for its funding of this research. I am also extremely grateful for all the great conversations, support and advice I’ve received from my peers throughout my program, and for the friendships I have developed. Specifically, I express my sincere gratitude to Dr. Johan Pretorius, Henda Pretorius, Dr. Justin McMechan, Dr. Ana Velez, Dr. Kenny Roche, Dr. Lia Marchi-Werle, Dr. Matheus Ribeiro, Dr. Louise Lynch, ii Camila Olivera-Hofmann, and Erin Ingram for their friendship and all the support throughout my program. Finally, I lovingly express my deepest gratitude to my parents, Jim and Ronda Koch, my sister and brother-in-law, Jaime and AJ Wiekhorst, my nephews, Terrell and Tayden, my niece and great-niece, Madison and Maleaha and my grandfather, Don Kelley, for their endless support, encouragement, and love in all endeavors. iii TABLE OF CONTENTS CHAPTER 1: LITERATURE REVIEW ................................................................... 1 Switchgrass .......................................................................................................... 1 Development of Switchgrass as a Dedicated Bioenergy Feedstock ................. 2 Insect Pests of Switchgrass: General Pests ....................................................... 7 Aphids ................................................................................................................ 13 Greenbug ........................................................................................................... 15 Yellow Sugarcane Aphid ................................................................................... 16 Cereal Aphid Screens on Switchgrass.............................................................. 17 Plant Resistance ................................................................................................ 21 References ......................................................................................................... 45 CHAPTER 2: EVALUATION OF GREENBUG AND YELLOW SUGARCANE APHID FEEDING BEHAVIOR ON RESISTANT AND SUSCEPTIBLE SWITCHGRASS CULTIVARS ............................................................................. 62 Introduction ........................................................................................................ 62 Materials and Methods ...................................................................................... 66 Results ............................................................................................................... 75 Discussion .......................................................................................................... 79 References ......................................................................................................... 85 Tables ................................................................................................................ 91 Figures ............................................................................................................... 95 iv CHAPTER 3: APHIDS INDUCE DIVERGENT DEFENSE RESPONSES IN HYBRID SWITCHGRASS (PANICUM VIRGATUM L.) ..................................... 100 Introduction ...................................................................................................... 100 Materials and Methods .................................................................................... 104 Results ............................................................................................................. 109 Discussion ........................................................................................................ 117 References ....................................................................................................... 126 Figures ............................................................................................................. 136 CHAPTER 4: TRANSCRIPTIONAL PROFILING OF GREENBUG AND YELLOW SUGARCANE APHID ON RESISTANT AND SUSCEPTIBLE SWITCHGRASS (PANICUM VIRGATUM L.) .................................................... 143 Introduction ...................................................................................................... 143 Materials and Methods ...................................................................................
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