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And Type the TITLE of YOUR WORK in All Caps GENETIC MECHANISMS OF VIRUS EVOLUTION AND EMERGENCE: RECOMBINATION, REASSORTMENT, OVERPRINTING AND MUTATION by ANDREW BROWNELL ALLISON (Under the Direction of David E. Stallknecht) ABSTRACT Although the emergence of a novel pathogen from an existing virus (or viruses) may be a multi-faceted process involving many interdependent viral, host, and/or environmental factors, the fundamental catalyst is genetic variation of the virus. For recombination and reassortment, both mechanisms involve the direct exchange of genetic material from two (or more) parental viruses, such that the novel virus is a genetic chimera of the parental viruses. For the recombinant or reassortant to replicate efficiently, be packaged and assembled correctly, and subsequently be competently transmitted in nature, the genetic elements derived from each parental virus must be structurally and functionally compatible in order for the novel virus to be viable. In the research on recombination in alphaviruses and reassortment in orbiviruses presented here, findings suggest this to be case, as both examples reinforce the notion that the genetic and/or structural compatibility between the parental viruses was likely a prerequisite for the emergence of the novel virus(es). In the two following examples of viral evolution involving overprinting and mutation, the emergence of the novel virus or variant was not dictated by the exchange of genes from different parental viruses, but rather by a change in existing sequence. For overprinting in rhabdoviruses, this involved the de novo synthesis of a novel protein through the use of an overlapping reading frame, thus increasing the coding capacity of the virus without incorporating any additional genetic elements. In the case of mutation in parvoviruses, the change in existing sequence allowed the new virus variant to jump species, thereby expanding the host range of the virus. In the description of the viruses presented within, genetic variability, whether through the process of change (overprinting or mutation) or exchange (recombination or reassortment), resulted in the emergence of a novel virus that was not only altered genetically, but also resulted in changes in the pathogenicity, antigenicity, ecology, and/or epidemiology of the virus relative to the parental virus(es), thereby shaping the evolutionary pathway of each novel virus. INDEX WORDS: virus evolution, viral genetics, recombination, reassortment, overprinting, overlapping reading frame, mutation, selection, alphavirus, Highlands J virus, Fort Morgan virus, orbivirus, epizootic hemorrhagic disease virus, serotype, rhabdovirus, Durham virus, canine parvovirus. GENETIC MECHANISMS OF VIRUS EVOLUTION AND EMERGENCE: RECOMBINATION, REASSORTMENT, OVERPRINTING AND MUTATION by ANDREW B. ALLISON B.S., Virginia Tech, 1996 M.S., University of Georgia, 2000 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2010 © 2010 Andrew B. Allison All Rights Reserved GENETIC MECHANISMS OF VIRUS EVOLUTION AND EMERGENCE: RECOMBINATION, REASSORTMENT, OVERPRINTING AND MUTATION by ANDREW B. ALLISON Major Professor: David E. Stallknecht Committee: Claudio L. Afonso Mark W. Jackwood Liliana Jaso-Friedmann Daniel G. Mead Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia May 2010 iv DEDICATION To my parents. v ACKNOWLEDGEMENTS I would like to thank my boss and advisor, David Stallknecht, for giving me the freedom to pursue this research. I would also like to thank my committee members, Daniel Mead, Mark Jackwood, Claudio Afonso, and Liliana Jaso-Friedmann for their support of this project and to those at SCWDS who made me laugh over the (many, many) years. vi TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .................................................................................................v LIST OF TABLES ...............................................................................................................x LIST OF FIGURES .......................................................................................................... xii CHAPTER 1 INTRODUCTION ............................................................................................1 References ..................................................................................................14 2 LITERATURE REVIEW ...............................................................................20 Virus Evolution ..........................................................................................20 Recombination ...........................................................................................23 Reassortment ..............................................................................................33 Overprinting ...............................................................................................48 Mutation .....................................................................................................55 References ..................................................................................................64 3 RECOMBINATION: PART I - A COMPARATIVE GENOMIC ANALYSIS OF HIGHLANDS J VIRUS WITH WESTERN AND EASTERN EQUINE ENCEPHALITIS VIRUSES .....................................................................78 Abstract .....................................................................................................79 Introduction ...............................................................................................80 vii Materials and Methods ...............................................................................83 Results and Discussion ..............................................................................86 Acknowledgements ..................................................................................112 References ................................................................................................113 PART II - THE EVOLUTIONARY GENETICS OF RECOMBINANT VIRUSES IN THE WESTERN EQUINE ENCEPHALITIS ANTIGENIC COMPLEX OF ALPHAVIRUSES .........................................................120 Abstract ....................................................................................................121 Introduction ..............................................................................................122 Materials and Methods .............................................................................127 Results and Discussion ............................................................................132 Acknowledgements ..................................................................................164 References ................................................................................................165 4 REASSORTMENT: DESCRIPTION OF A NOVEL REASSORTANT EPIZOOTIC HEMORRHAGIC DISEASE VIRUS CONTAINING RNA SEGMENTS DERIVED FROM BOTH EXOTIC AND ENDEMIC SEROTYPES ....174 Abstract ....................................................................................................175 Introduction ..............................................................................................176 Methods....................................................................................................179 Results ......................................................................................................184 Discussion ................................................................................................189 Acknowledgements ..................................................................................207 viii References ................................................................................................208 5 OVERPRINTING: CHARACTERIZATION OF DURHAM VIRUS, A NOVEL RHABDOVIRUS THAT ENCODES A C PROTEIN FROM AN OVERLAPPING OPEN READING FRAME (ORF) AND A SMALL HYDROPHOBIC PROTEIN FROM A NOVEL ORF ...........................213 Abstract ....................................................................................................214 Introduction ..............................................................................................215 Methods....................................................................................................218 Results ......................................................................................................226 Discussion ................................................................................................237 Acknowledgements ..................................................................................263 References ................................................................................................264 6 MUTATION: THE MOLECULAR EVOLUTION OF A SPECIES JUMP BY CANINE PARVOVIRUS ........................................................................................272 Abstract ....................................................................................................273 Introduction ..............................................................................................274 Materials and Methods .............................................................................279 Results ......................................................................................................286 Discussion ................................................................................................293 Acknowledgements ..................................................................................314
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