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Can Very Rapid Adaptation Arise Without Ancestral Variation?

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Clemson University TigerPrints All Dissertations Dissertations 5-2014 Can Very Rapid Adaptation Arise Without Ancestral Variation? Insight from the Molecular Evolution of Herbicide Resistance in Genus Amaranthus Kristin Elizabeth Beard Clemson University Follow this and additional works at: https://tigerprints.clemson.edu/all_dissertations Recommended Citation Beard, Kristin Elizabeth, "Can Very Rapid Adaptation Arise Without Ancestral Variation? Insight from the Molecular Evolution of Herbicide Resistance in Genus Amaranthus" (2014). All Dissertations. 1797. https://tigerprints.clemson.edu/all_dissertations/1797 This Dissertation is brought to you for free and open access by the Dissertations at TigerPrints. It has been accepted for inclusion in All Dissertations by an authorized administrator of TigerPrints. For more information, please contact [email protected]. CAN VERY RAPID ADAPTATION ARISE WITHOUT ANCESTRAL VARIATION? INSIGHT FROM THE MOLECULAR EVOLUTION OF HERBICIDE RESISTANCE IN GENUS Amaranthus A Dissertation Presented to the Graduate School of Clemson University In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Genetics by Kristin Elizabeth Beard May 2014 Accepted by: Dr. Amy Lawton-Rauh, Committee Chair Dr. Kerry Smith Dr. Alex Feltus Dr. Hong Luo ABSTRACT In this dissertation I investigate the source and spread of adaptive resistance to the herbicide glyphosate by the weedy species Amaranthus palmeri. This is an ideal system for furthering scientific understanding of the dynamics of evolution because the adaptation is in response to a well understood selection pressure and is happening on an extremely short time scale. The plant genus Amaranthus contains several agriculturally important weeds, but is not closely related to any current model systems—the closest model system is Beta vulgaris (sugar beet). In the first part of this work I seek to determine the relationship between extant species of Amaranthus, particularly the relationship between weedy and non- weedy species, using Bayesian phylogenetic analysis of independent genomic loci. This phylogeny will provide context for investigating the dynamics of adaptation to glyphosate stress. The second chapter is an investigation of the sequence constraints and selection pressures acting on the gene that codes for 5-enolpyruvalshikimate-3-phosphate synthase (EPSPS) in the genus Amaranthus. The first population of A. palmeri verified as resistant to glyphosate was identified in Macon, Georgia in 2004. The mechanism of resistance was found to be proliferation in copy number of the gene encoding the enzyme target of glyphosate toxicity, EPSPS. The proliferation of genomic copies of the gene encoding a target enzyme is unique among mechanisms documented for herbicide resistance— ii though it has been observed as a resistance mechanism in other systems, including human cancer resistance to chemotherapy. Understanding EPSPS DNA sequence constraint will allow a better understanding of the evolutionary processes that led to a unique mechanism of herbicide resistance. In the final chapter I seek to determine if the same EPSPS copy number proliferation mechanism is responsible for glyphosate resistance in North Carolina A. palmeri and address the question of the source of the EPSPS copy number proliferation genotype. I investigate the potential of parallel evolution from ancestral variation as an explanation for observed spread of resistance by looking for genus-wide variation in EPSPS copy number and analyze population structure to determine the most probable number of adaptive events. Understanding the constraints on the EPSPS gene and protein that may have led to the observed resistance mechanism, how many times the mechanism evolved independently, and how it spread through the population(s) improves our understanding of how genomes are changed by adaptation to environmental stress. It also has the potential to provide important insights about the dynamics of herbicide resistance adaptation that can help growers make the best possible choices in weed management for protecting our food supply and our environment. iii ACKNOWLEDGMENTS There are quite a few people who I would like to thank: people who share credit for my completion of this degree. I would like first thank my family, or maybe blame them. Without their unfailing encouragement of critical thinking and exploration as a girl I might have never started this degree, and without their love and support throughout it I would not have finished. I also want to thank my husband; we met just before I chose a lab for my thesis work, and he has been there to support me for the last five years as my shoulder to cry on when experiments failed. Also, Liz Crouse and my fellow Genetics and Biochemistry grad students—particularly Krystal Cadle—for being the people to go have a drink with after I was done crying about failed experiments. I would like to thank Amy Lawton-Rauh for the opportunity to further my education and for her enthusiasm, her encouragement, and her resolute dedication my success. She helped me find a work ethic that I did not know existed and her tireless support and help will always be appreciated. I would also like to thank Kerry Smith, Alex Feltus and Hong Luo for serving on my graduate committee. I would also like to thank Jim Burton and Nilda Burgos for their assistance with the weed science parts of this work, David Brenner at the USDA for germplasm, and Billy Bridges for all the advice about statistics. I am also thankful for the hard work and advice given to me by Brad Rauh, and all the undergraduate interns who helped along the way: Steven Vensko, Thomas Lane, Caroline Thomas, Sarah Barfield, and Katerina Lay. And lastly, I owe much appreciation to Cotton Inc., Clemson University, and Wade Stackhouse for generous financial support. iv v TABLE OF CONTENTS Page TITLE PAGE .................................................................................................................... i ABSTRACT ..................................................................................................................... ii AKNOWLEDGEMENTS............................................................................................... iv LIST OF TABLES ........................................................................................................ viii LIST OF FIGURES ......................................................................................................... x PREFACE ........................................................................................................................ 1 INTRODUCTION HERBICIDE RESISTANCE IN Amaranthus AS A SYSTEM TO STUDY ADAPTIVE EVOLUTION: A REVIEW OF CURRENT LITURATURE ........................................................................................ 5 Literature Review ........................................................................................................ 6 References ................................................................................................................. 37 CHAPTER I THE PHYLOGENY OF Amaranthus (Amaranthaceae) WITH A FOCUS ON THE DISTRIBUTION OF AGRONOMICALLY IMPORTANT TRAITS ............................................................................................ 55 Abstract ..................................................................................................................... 56 Introduction ............................................................................................................... 57 Materials and Methods .............................................................................................. 60 Results ....................................................................................................................... 65 Discussion ................................................................................................................. 70 References ................................................................................................................. 87 vi Table of Contents (Continued) Page CHAPTER II A UNIQUE SOLUTION: HOW HAS SEQUENCE CONTEXT AND CONSTRAINT INFLUENCED THE ADAPTATION OF A. palmeri TO THE HERBICIDE GLYPHOSATE? ............................................... 91 Abstract ..................................................................................................................... 92 Introduction ............................................................................................................... 93 Materials and Methods .............................................................................................. 98 Results ..................................................................................................................... 102 Discussion ............................................................................................................... 106 References ............................................................................................................... 124 CHAPTER III GENETIC SIGNATURES OF POPULATION STRUCTURE SHOW EVIDENCE OF PARALLEL ADAPTATION OF NORTH CAROLINA A. palmeri TO GLYPHOSATE STRESS ........................... 129 Abstract ................................................................................................................... 130 Introduction ............................................................................................................. 131 Materials and Methods ...........................................................................................
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