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Seeding Multi-omic Improvement of Apple Thesis Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Emma Bilbrey Graduate Program in Horticulture and Crop Science The Ohio State University 2020 Thesis Committee Jessica L. Cooperstone, Advisor Jonathan Fresnedo Ramirez Diane Miller Emmanuel Hatzakis 1 Copyrighted by Emma Bilbrey 2020 2 Abstract Apples are one of the most commonly consumed fruits in America, and “an apple a day keeps the doctor away” is a well-known adage. The commercial and nutritional importance of apples has prompted interest in varietal improvement. However, progress is limited by a long juvenile period, which delays fruit evaluation for quality traits, such as phytochemical composition. To minimize this drawback, apple breeders have begun using marker-assisted selection (MAS) for some traits, but breeding strategies for fruit phytochemicals have yet to be developed. In response, we have developed an integrated genomic-metabolomic platform to better understand gene-phytochemical associations in breeding-relevant apple germplasm. Phytochemicals that are potentially health beneficial, contribute disease resistance, or improve fruit quality can be characterized using metabolomics, providing a foundation to study apple’s breeding potential. The platform is based on high-throughput genomic and metabolomic assessment of 173 unique apples, including members of three pedigree-connected families alongside diverse and wild selections. Single nucleotide polymorphism (SNP) data was obtained from the 20K SNP array for apple and integrated with metabolomic datasets from high-resolution mass spectrometry and nuclear magnetic resonance (NMR) spectroscopy analyses of polar/semi-polar apple fruit extracts. Metabolite genome-wide association studies (mGWAS) were conducted with 11,165 ii SNPs for two LC-MS data sets of 4,000+ features each and an NMR data set of 756 bins. Novel schemes for prioritizing results from mGWAS indicated 519 (LC-MS (+)), 726 (LC-MS (-)), and 177 (NMR) significant marker-trait associations across the apple genome (LC-MS: p < .00001, NMR: p < .0001). These results were then sifted to select features to analyze with a more powerful pedigree-based analysis (PBA) in FlexQTL™ with 6,034 SNPs to identify metabolite quantitative trait loci (mQTL), genomic areas exerting genetic control over phytochemical production. An mQTL for chlorogenic acid was identified on the bottom of chromosome 17 across all three metabolomic data sets and was used as a proof-of-concept example to demonstrate the applicability of the platform. Determining gene-phytochemical relationships in apple will inform breeding and facilitate future MAS for improved nutrition along with attributes related to flavor and disease resistance etiology. iii Dedication To my family, friends, and, above all, to the Creator who has furnished the world with wonders beyond worthy of our study. iv Acknowledgments To my advisor Dr. Jessica Cooperstone, I owe much in terms of skills and scientific understanding. More important I owe her great gratitude for her support and encouragement throughout the course of my master’s work. Her passion and strong resolve as a woman in science is unmatched. I would like to thank my committee thoroughly for their integral involvement in this highly collaborative project. Dr. Jonathan Fresnedo Ramírez receives credit for honing my understanding of tree crop genomics and pushing me to dig deep in my understanding of the concepts and their implications. I thank Dr. Diane Miller for her dedicated collection of apple germplasm and insight into commercial apple breeding and its origins. Dr. Emmanuel Hatzakis, I thank for his NMR expertise and kindness throughout the project. A group that deserves so much thanks is the Cooperstone Lab. It was ever a pleasure to work alongside them and enjoy many Brassica lunches. My thanks also goes to Katie Williamson in the Hatzakis Lab for running my NMR samples and helping me process them with Dr. Matthias Klein. I am grateful for the Midwest Apple Improvement Association (MAIA) for providing all of the apple germplasm studied here. We could not have answered any of these questions without their support. Additionally, I am thankful for Ohio State’s Foods v For Health Discovery Theme for funding this project. I would not have received this degree without the financial support of the University Fellowship from the Graduate School along with the OARDC Director’s Associateship Award. Finally, to my family, friends, and our Athens home of Brookfield Church, I owe unending gratitude for their love throughout these years of my life. To my husband Clark I owe thanks for the title “Apple Scientist” and enduring support. vi Vita June 2013 ............................................................. Valparaiso High School June 2016 – August 2016 .................................... Forestry and Horticulture Internship, Taltree Arboretum and Gardens, Valparaiso, IN June 2017 ............................................................. B.S. General Biology, Summa cum Laude, Union University, Jackson, TN July 2017 – July 2018 .......................................... Manufacturing Technician II, Bioreagents Department, Quidel Corporation, Athens, OH August 2018 – July 2019 ..................................... University Fellow, The Ohio State University, Columbus, OH August 2019 – Present ......................................... OARDC Director’s Award Recipient, Columbus, OH August 2018 – Present ......................................... Graduate Research Associate, Department of Horticulture and Crop Science, The Ohio State University vii Fields of Study Major Field: Horticulture and Crop Science viii Table of Contents Abstract ............................................................................................................................... ii Dedication ........................................................................................................................... iv Acknowledgments ............................................................................................................... v Vita ................................................................................................................................... vii Fields of Study ................................................................................................................. viii List of Tables ................................................................................................................... xiii List of Figures ................................................................................................................... xiv Chapter 1. Literature Review .............................................................................................. 1 1.1 Apples in History ....................................................................................................... 1 1.2 Traditional Apple Breeding ....................................................................................... 2 1.3 Apples and Human Health ......................................................................................... 4 1.3.1 Cancer ................................................................................................................. 5 1.3.2 Cardiovascular Disease ...................................................................................... 6 1.3.3 Cognitive Decline ............................................................................................... 8 1.3.4 Polyphenols ........................................................................................................ 9 1.3.4.1 Anthocyanins ............................................................................................. 10 1.3.4.2 Dihydrochalcones ...................................................................................... 10 1.3.4.3 Flavonols ................................................................................................... 12 1.3.4.4 Flavanols (Flavan-3-ols) ............................................................................ 13 1.4 Nutrition-Driven Breeding ...................................................................................... 13 1.5 Apples and Genomics .............................................................................................. 16 1.6 Apples and Metabolomics ....................................................................................... 19 1.7 Multi-omic Integration ............................................................................................ 21 1.7.1 Bi-Parental Mapping Populations ..................................................................... 22 1.7.2 Metabolite Genome Wide Association Studies (mGWAS) ............................. 24 ix 1.7.3 Pedigree-Based Analysis .................................................................................. 25 1.7.4 Apple Integrated Genetic Linkage Map (iGLmap) .......................................... 27 1.8 Specific Aims .......................................................................................................... 28 Chapter 2. Seeding Multi-omic Apple Improvement ........................................................ 31 2.1 Abstract .................................................................................................................... 32 2.2 Introduction ............................................................................................................
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