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Symbionts Associated with the Salivary Glands of the Potato Leafhopper, Empoasca Fabae, and Their Function When Feeding on Leguminous Hosts

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Symbionts Associated with the Salivary Glands of the Potato Leafhopper, Empoasca Fabae, and Their Function When Feeding on Leguminous Hosts ABSTRACT Title of dissertation: SYMBIONTS ASSOCIATED WITH THE SALIVARY GLANDS OF THE POTATO LEAFHOPPER, EMPOASCA FABAE, AND THEIR FUNCTION WHEN FEEDING ON LEGUMINOUS HOSTS Bridget Diane DeLay, Doctor of Philosophy, 2013 Dissertation directed by: Professor William O. Lamp Department of Entomology Many species of phloem feeding insects are host to symbiotic bacteria, which provide their hosts with nutrients lacking from phloem. The potato leafhopper, Empoasca fabae, feeds on the phloem and cell contents of a wide variety of plants. In this study, I identified two taxa of symbiotic bacteria present in the salivary glands, midgut, bacteriomes and saliva of the potato leafhopper: Sulcia muelleri and Wolbachia. Treatment of the leafhoppers with 0.01% oxytetracycline-HCl resulted in the creation of aposymbiotic leafhoppers. Longevity and fecundity of aposymbiotic leafhoppers on alfalfa, Medicago sativa, and fava bean, Vicia faba, were significantly lower than that of symbiotic leafhoppers. In addition, aposymbiotic leafhoppers caused less of a decrease in photosynthesis rates on both alfalfa and fava bean in comparison to symbiotic leafhoppers. The salivary gland transcriptome of the potato leafhopper revealed the presence of potential salivary components, including lipase, pectin lyase and alkaline phosphatase, all of which were expressed at higher levels in salivary glands than in midgut or hind femur tissue. In addition, transcripts attributed to Wolbachia were discovered in the sialotranscriptome, providing more evidence that this bacterium is present in the salivary glands of the potato leafhopper. Finally, expression of alfalfa wound response genes after exposure to potato leafhopper saliva was measured. Endo 1-3 ß-D-glucanase, isoflavone reductase, chalcone synthase and phenylalanine ammonia- lyase gene expression were higher in plants exposed to leafhopper saliva than in unexposed controls. Treatment of saliva with heat, filter sterilization, DTT, EDTA and K2HPO4 led to different plant wound response gene expression patterns. I conclude that the symbionts present in the potato leafhopper are necessary for the normal development and reproduction of this species, in addition to playing a potential role in plant wound response to feeding. SYMBIONTS ASSOCIATED WITH THE SALIVARY GLANDS OF THE POTATO LEAFHOPPER, EMPOASCA FABAE, AND THEIR FUNCTION WHEN FEEDING ON LEGUMINOUS HOSTS by Bridget Diane DeLay Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2013 Advisory Committee: Professor William O. Lamp, Chair Professor Daniel Gruner Professor David Hawthorne Professor Leslie Pick Professor Jian Wang Professor Jianhua Zhu Foreword With the recommendation of the dissertation director (William O. Lamp), and with the endorsement of the Entomology program Graduate Director (Paula M. Shrewsbury), chapter 4 of this dissertation is included as a previously published work. The citation for this publication is as follows: DeLay, B., Mamidala, P., Wijeratne, A., Wijeratne, S., Mittapalli, O., Wang, J., Lamp, W., 2012. Transcriptome analysis of the salivary glands of the potato leafhopper, Empoasca fabae. Journal of Insect Physiology 58(12), 1626-1634. As directed in the graduate catalog for chapters previously published as coauthored works, I state that I was responsible for the inception of the manuscript and the majority of the manuscript preparation. This work was reformatted to meet the requirements for dissertations, but all other aspects of the published manuscript, including the use of first person plural, were used in this document. A letter was sent to the Dean of the Graduate School certifying that inclusion of this previously published work in this dissertation has the approval of the dissertation committee, the dissertation advisor, and the Graduate Director. A copy of this letter is included in Appendix A. ii Dedication I dedicate this work to the two who call me ‘Gitte. To Nick: I can not imagine life without you, and am grateful for all of the support that you have shown to me thoughout the completion of this work. I could not have asked for a better husband, and count myself blessed to have met you. To Gpa: although you are no longer around, I owe so much of who I am to you. You showed me how to work with tools, instilled in me a sense of craftsmanship, and gave me unwavering love. I only wish that you were here to share this work with me – I know that it would have made you smile. iii Acknowledgements I would first like to thank my advisor, Bill Lamp. Bill has been instrumental in the production of this dissertation, through providing technical advice, his input on editing of this dissertation and our co-authored manuscripts, and in providing guidance throughout my graduate work. I am extremely grateful for his advice and critiques throughout my time in his lab. I would like to thank the members of the Lamp lab for all of their input and constructive critism: Robert Smith, Lauren Culler, Alan Leslie, Susan Lombardi, Ellie Stevens, Libby Sancomb, Sarah Au, Dilip Venugopal, Ryan Gott, Melanie Stevens, Scott Berg and Sadia Naseem. I would also like to acknowledge the members of my dissertation committee, Dave Hawthorne, Dan Gruner, Leslie Pick, Jian Wang, and Jianhua Zhu. Your guidance and support thoughout my graduate career has been instrumental in my achievements thus far. I would especially like to thank Dave Straney for agreeing to act as my Dean’s Representative at the last minute. In addition to working with the potato leafhopper, I have also worked on the symbionts present in the brown marmorated stink bug, Halyomorpha halys. I would like to specifically thank Sadia Naseem for her help with stink bug dissections and symbiont screening. In addition, I would like to thank Chris Taylor, Galen Dively and Karen Rane for their input with this project and for providing stink bugs for me. Finally, I would like to thank Leslie Pick, Jian Wang, Cerruti Hicks, Galen Dively, Chris Taylor, Ellie Stevens, Alan Leslie and Ryan Gott for reviewing the stink bug manuscript and providing recommendations on how to improve it. iv I have also been lucky to have taught for Patty Shields, Dave Straney, Ray St. Leger, Brett Kent and Bill Higgins. I am extremely grateful to Patty, who has helped me to grow in my capacity as a teacher, and who has provided me with an understanding of how to create course modules. In addition to those mentioned above, I would like to specifically thank Amy Beaven for her guidance in using the Zeiss LSM710 confocal microscope to produce the FISH images in Chapter 1. She also trained me in the use of the LightCycler 480 used for qRT-PCR in Chapters 4 and 5 of this dissertation, and in the use of the 3730xl DNA Analyzer used in Chapter 1. In addition to those mentioned above, I would like to specifically thank my coauthors for Chapter 4: Jian Wang, Omprakash Mittapalli, Praveen Mamidala, Asela Wijeratne and Saranga Wijeratne. Jianhua Huang helped with the salivary gland dissections, and funding for the transcriptome work was provided by the Maryland Agricultural Experiment Station Grant Program, 2010–11, and MAES Hatch Project MD- ENTM-1016. v TABLE OF CONTENTS Foreward ........................................................................................................................... ii Dedication ......................................................................................................................... iii Acknowledgements ........................................................................................................... iv List of Tables .................................................................................................................... ix List of Figures ................................................................................................................... x Chapter I: Characterization of potato leafhopper salivary symbionts .............................. 1 Abstract ............................................................................................................................. 1 Introduction ...................................................................................................................... 1 Materials and methods ......................................................................................... 5 Insect collection and rearing ................................................................... 5 Insect dissection and DNA extraction ...................................................... 6 PCR of symbiont genes ............................................................................ 7 Cloning and sequencing of symbiont genes ............................................. 8 Phylogenetic analysis ............................................................................... 9 Microscopy ............................................................................................... 10 Results .................................................................................................................. 11 Symbiont presence/absence ..................................................................... 11 Phylogenetics of potato leafhopper symbionts ........................................ 18 Microscopy ............................................................................................... 22 Discussion ...........................................................................................................
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