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Lavergne Colostate 0053N 151 THESIS UNDERSTANDING THE MOLECULAR BASIS OF INSECT PEST RESISTANCE IN TRITICUM AESTIVUM USING MASS SPECTROMETRY Submitted by Florent D. Lavergne Department of Horticulture and Landscape Architecture In partial fulfillment of the requirements For the Degree of Master of Science Colorado State University Fort Collins, Colorado Fall 2018 Master’s Committee: Advisor: Adam Heuberger Corey Broeckling Stephen Pearce Courtney Jahn Copyright by Florent D. Lavergne 2018 All Rights Reserved ABSTRACT UNDERSTANDING THE MOLECULAR BASIS OF INSECT PEST RESISTANCE IN TRITICUM AESTIVUM USING MASS SPECTROMETRY Bread wheat (Triticum aestivum L.) is a global staple crop and controlling for environmental stress that impacts grain yield is critical. Recently, Wheat Stem Sawfly (Cephus cinctus, hereafter WSS) has emerged as a new pest of wheat and is expanding across the Great Plains and southern United States. WSS is difficult to control using chemical, cultural or biological pest management methods. Currently, wheat breeders utilize a solid-stem trait to inhibit larval feeding and reduce lodging, however this trait only confers partial resistance and is thought to reduce grain yield. Models of metabolic-based resistance with demonstrated impact on reduction of insect pest fitness have been documented. Here, I investigate the broader hypothesis that wheat resistance to WSS is mediated by shifts in metabolism that promote avoidance and toxicity towards WSS. Four cultivars with contrasting phenotypes are used in our studies: Hatcher (resistant to WSS, hollow-stem, winter wheat); Conan (resistant, semi-solid- stem, spring); Denali (susceptible, hollow-stem, winter); and Reeder (susceptible, hollow-stem, spring). The first part of this work involved gas chromatography-mass spectrometry (GC-MS) metabolomics methods to provide a comprehensive characterization of the chemical composition of wheat cuticular waxes. A total of 263 putative compounds were detected among the four abovementioned wheat cultivars and comprised 58 wax compounds including alkanes and fatty acids. Many of the detected wax metabolites have known associations to important biological functions such as insect pest and drought resistance. Uni- and multivariate statistics were used to ii evaluate metabolite distribution between tissue types (leaf, stem) and cultivars. Leaves contained more primary alcohols than stems such as 6-methylheptacosan-1-ol and octacosan-1-ol. The metabolite data were complemented using scanning electron microscopy of epicuticular wax crystals which detected wax tubules and platelets. Conan (resistant to WSS) was the only cultivar to display alcohol-associated platelet-shaped crystals on its abaxial leaf surface. The second part of this study aimed at evaluating a selection of wheat cultivars in a WSS- infested field. Cultivars with increased yield and reduced WSS infestation values were found. The molecular basis of this resistance was evaluated in a greenhouse study that characterized proteomic and metabolomic signatures of wheat stems associated with WSS infestation. Stem proteins (1832) and metabolites (1823) were detected in the same four wheat cultivars using liquid chromatography-mass spectrometry. During infestation with WSS, 62 proteins and 29 metabolites were differentially regulated in the hollow-stem resistant cultivar Hatcher. Metabolic processes that were associated with resistance included enzymatic detoxification, proteinase inhibition, and anti-herbivory compound production, specifically the benzoxazinoids, neolignans, and phenolics. Compared to the semi-solid and resistant cultivar Conan, hollow-stem Hatcher had increased abundance of proteins and metabolites with known roles in plant defense against insects. These results will be invaluable to plant breeders as they contribute to the understanding of wax composition and metabolic regulation associated with important phenotypic traits in a major crop, including passive and active defense mechanisms to WSS. iii ACKNOWLEDGEMENTS First, I wish to thank all my committee members, Adam L. Heuberger, Courtney E. Jahn, Corey D. Broeckling, and Stephen Pearce, for their unlimited support and for providing all the help I needed to achieve my goals. Adam and Courtney both greatly contributed to making this journey a reality and graduate from CSU, and I am profusely grateful for their support and investment. Likewise, I want to thank the Colorado Wheat Research Foundation, the Colorado State University Agricultural Experiment Station, and more specifically Scott D. Haley who provided funding and supported my research. These years spend in Fort Collins have been punctuated with beautiful encounters with people from all horizons, both professionally and in my personal life. These people include my lab/research teammates, Harmonie M. Bettenhausen, Nate M. Sindt, Sahar Bagheri Toulabi, Jackie M. Chaparro, and many others. I also had the chance to mingle with foreigners from various cultures and I would like to thank Denis, Eliakim, Tom, and Marc for opening my mind and helping me see things from a different perspective. And all those I have met during the last three years and will always have a place in my heart and memories, thank you. I wish to acknowledge all members of my family, specifically my mom and dad, Martine and Francis, who always have and always will support my decisions should I decide to leave hometown for a place far, far away. My childhood friends also, especially Morgan that I might soon rejoin with in Germany. This work is dedicated to my passed grandmother, Paulette, whom nothing would give greater joy than witnessing our personal achievements. iv TABLE OF CONTENTS ABSTRACT .................................................................................................................................... ii ACKNOWLEDGMENTS ............................................................................................................ iv LIST OF TABLES ........................................................................................................................ vii LIST OF FIGURES .................................................................................................................... viii CHAPTER 1 – INTRODUCTION ..................................................................................................1 1.1. Bread Wheat Is an Important Global Food Crop ...............................................................1 1.2. The Wheat Stem Sawfly Is a Major Pest of Triticum aestivum .........................................1 1.2.1. Wheat Stem Sawfly Rapid Expansion Is Associated with Severe Wheat Yield Losses ................................................................................................................................1 1.2.2. Development of Larvae Inside Stems Limits the Efficacy of Control Strategies ...........................................................................................................................................3 1.2.3. The Widely Used Solid-Stem Trait Is Associated with Inconsistent Field Performance .......................................................................................................................5 1.3. Wheat Molecular Resistance to Biotic Stress Is Both Passive and Active ........................6 1.3.1. The Plant Cuticle as a Natural Barrier: Composition, Structure and Function .......6 1.3.2. Enzymes and Metabolites Are Critical Actors of the Molecular Defense Response ...........................................................................................................................................7 1.4. Mass Spectrometry-Based Methods Enable the Detection of Defense Compounds .........9 1.4.1. Detection of Semi-Volatile Waxes Using Gas Chromatography-Mass Spectrometry ......................................................................................................................9 1.4.2. Detection of Proteins and Metabolites Using Liquid Chromatography-Mass Spectrometry ......................................................................................................................9 1.5. Preliminary Studies ..........................................................................................................10 1.5.1. Wheat Cultivars Assessed in Preliminary Studies and Further Explored in the Present Work ...................................................................................................................10 1.5.2. Behavior of WSS on a Resistant Cultivar Suggests Presence of Repelling Cuticular Structures and/or Volatile Emissions ..............................................................11 1.5.3. Wheat Active Responses to WSS Involve Complex Molecular Networks ...........11 1.6. Overview ..........................................................................................................................12 REFERENCES ..............................................................................................................................17 CHAPTER 2 – GC-MS METABOLOMICS TO EVALUATE THE COMPOSITION OF PLANT CUTICULAR WAXES FOR FOUR TRITICUM AESTIVUM CULTIVARS ................22 2.1. Summary ..........................................................................................................................22 2.2. Introduction ......................................................................................................................23 2.3. Methodology ....................................................................................................................26
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