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Grapevine Fanleaf Virus: Biology, Biotechnology and Resistance

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Grapevine Fanleaf Virus: Biology, Biotechnology and Resistance GRAPEVINE FANLEAF VIRUS: BIOLOGY, BIOTECHNOLOGY AND RESISTANCE A Dissertation Presented to the Faculty of the Graduate School of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by John Wesley Gottula May 2014 © 2014 John Wesley Gottula GRAPEVINE FANLEAF VIRUS: BIOLOGY, BIOTECHNOLOGY AND RESISTANCE John Wesley Gottula, Ph. D. Cornell University 2014 Grapevine fanleaf virus (GFLV) causes fanleaf degeneration of grapevines. GFLV is present in most grape growing regions and has a bipartite RNA genome. The three goals of this research were to (1) advance our understanding of GFLV biology through studies on its satellite RNA, (2) engineer GFLV into a viral vector for grapevine functional genomics, and (3) discover a source of resistance to GFLV. This author addressed GFLV biology by studying the least understood aspect of GFLV: its satellite RNA. This author sequenced a new GFLV satellite RNA variant and compared it with other satellite RNA sequences. Forensic tracking of the satellite RNA revealed that it originated from an ancestral nepovirus and was likely introduced from Europe into North America. Greenhouse experiments showed that the GFLV satellite RNA has commensal relationship with its helper virus on a herbaceous host. This author engineered GFLV into a biotechnology tool by cloning infectious GFLV genomic cDNAs into binary vectors, with or without further modifications, and using Agrobacterium tumefaciens delivery to infect Nicotiana benthamiana. Tagging GFLV with fluorescent proteins allowed tracking of the virus within N. benthamiana and Chenopodium quinoa tissues, and imbuing GFLV with partial plant gene sequences proved the concept that endogenous plant genes can be knocked down. Infectivity of the viral vector depended on the identity of the GFLV strains or reassortants, on co- application of heterologous silencing suppressors and on lower ambient temperatures. No natural sources of resistance to GFLV exist within Vitis spp., but certain herbaceous hosts such as N. tabacum (tobacco) are resistant. This author used tobacco, its wild relatives, and hybrids between tobacco and wild relatives to evaluate the genomic and physiological basis of resistance. Resistance to GFLV in tobacco is governed by systemic recovery from virus infection that is additively inherited and likely multi-allelic. This research has opened new avenues to understand virus and plant evolution, and furnishes geneticists with a new tool to functionally characterize host genes. This dissertation also includes a history of pathogen-derived resistance with specific reference to plant virus resistance. BIOGRAPHICAL SKETCH John was raised in Lubbock, Texas and attended Texas Tech University as an undergraduate. At Texas Tech, he worked with Dr. Robert Wright on cotton breeding and biotechnology. John’s research interests include transgenic technologies for plant stress resistance, breeding for durable plant resistance and plant functional genomics tools. John has been the first author/ co-author on seven publications and primary investigator or project director on two grants focused on plant biology and biotechnology. He has taken a variety of leadership roles in the Plant Pathology Graduate Student Association at Cornell including treasurer (2009-2011), the Student Association of the Geneva Experiment Station including garden coordinator (2010- 2012), has led a collaborative Cornell colloquium (2012) and has coordinated invited lectures of multiple students and faculty from around the United States. John has served as ad hoc reviewer for Crop Science and Transgenic Research, assisted teaching the Cornell course Magical Mushrooms, Mischievous Molds, and has participated in extension work for grapevine virus control in the Finger Lakes. When John is not doing research, he enjoys pretending to fish with his friend Ben and dancing a very serious two-step with his beautiful wife Kelly. v Dedicated to Hussein Alzubi vi ACKNOWLEDGMENTS First and foremost, I thank my major advisor Marc Fuchs for his support and professionalism. I extend my appreciation to committee members Lisa Earle and Sunny Power for their suggestions, advice and never-wavering support. I thank Stewart Gray for hosting me in his laboratory and believing in me from day one. I offer special thanks to Corinne Keichinger and family, Christophe Ritzenthaler, Gérard Demangeat, Emmanuelle Vigne and family, Peggy Andret-Link, Veronique Komar and Olivier Lemaire for entertaining me in beautiful Alsace, France. Luz Marcela Yepes, Ramsey Lewis, Mei Cheung, David MacUmber, Pat Marsella- Herrick, Mamta Srivastava, Dawn Smith, Jason Ingram and Tai Wei Guo each gave critical assistance to parts of this research. Ben Bartlett, Dana Lapato, Halli Gutting, Léa Ackerer, Rossella Labarile, Keiran Cantilina, Larissa Osterbaan, Libby Cieniewicz and Melanie Isganitis also contributed significantly. Thanks to those who contributed to my education in virology and molecular biology including John Hart, Ben Orcheski, Jonathan Oliver, Jason Cavatorta, Jean-Michel Hily, Ho-Jong Ju, Balaji Vasudevan, Stacy Singer, Kamal Hlebieh, Caroline Hemmer, Batiste Monsion and Francois Berthold, Kerik Cox for statistics help, and Seiya Saito for his statistics help and friendship. Thanks to the Cornell Plant Virology Group and students and faculty at North Carolina State, Ohio State and Penn State universities for their stimulating and helpful dialog. The research was funded in part by a USDA-AFRI-NIFA pre- doctoral grant, a Grape Research Coordination Network Grant, assistantships from Cornell Department of Plant Pathology and Plant-Microbe Biology, and the College of Agriculture and Life Sciences through the New York State Agricultural Experiment Station. Thanks to my wife Kelly Voll for her love and to Kemal Ozbek for being a great roommate, too. vii PREFACE Grapevine fanleaf virus (GFLV) is a small pathogen in size. It encodes only eight individual proteins and is encapsidated in 30nm particles, but its interactions with plant hosts are extraordinarily complex. This dissertation encompasses reviews and primary research of GFLV biology including its genetic diversity, host range, inoculation methods, evolutionary biology and uses in biotechnology. In Chapter 1, this author reviews GFLV biology and discuss its relationship with other viruses of the genus Nepovirus, family Secoviridae. In Chapter 2, this author discusses the natural history, evolutionary biology, and host and helper virus interactions of the nepovirus subgroup A satellite RNA. In Chapter 3, this author presents proofs-of-concept that GFLV is engineered into a vector for plant functional genomics and other uses. In Chapter 4, this author describes variables that are associated with reliable plant systemic infection when GFLV is inoculated through Agrobacterium tumefaciens. In Chapter 5, this author reviews the history of pathogen-derived resistance applied to viruses through 2009. In Chapter 6, this author presents an assessment of the GFLV host range within Nicotiana and a theory of how allopolyploids impact evolution of basal virus resistance. Finally, in Chapter 7, this author suggests research projects to better understand the GFLV satellite RNA, improve the GFLV vector, and an overview of how plant resistance to viruses can be improved. Readers of this dissertation will gain an appreciation of the complex yet elegant nature of GFLV biology and insights into broader issues in plant virology, viral vectors for plant functional genomics and plant resistance to viruses. viii TABLE OF CONTENTS CHAPTER 1: GRAPEVINE FANLEAF VIRUS AND FANLEAF DEGENERATION ...................................................................................................................................... 17 THE DISEASE .................................................................................................... 17 PATHOGEN BIOLOGY ..................................................................................... 18 DISEASE MANAGEMENT ............................................................................... 25 BIOTECHNOLOGY ........................................................................................... 27 REFERENCES .................................................................................................... 29 CHAPTER 2: GENETIC VARIABILITY, EVOLUTION AND BIOLOGICAL EFFECTS OF GRAPEVINE FANLEAF VIRUS SATELLITE RNAS ...................... 39 ABSTRACT ........................................................................................................ 39 INTRODUCTION ............................................................................................... 41 MATERIALS AND METHODS ........................................................................ 43 RESULTS ............................................................................................................ 50 REFERENCES .................................................................................................... 71 CHAPTER 3: A VIRAL VECTOR COMPOSED OF GRAPEVINE FANLEAF VIRUS .......................................................................................................................... 77 ABSTRACT ........................................................................................................ 77 INTRODUCTION ............................................................................................... 78 MATERIALS AND METHODS .......................................................................
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