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Allopolyploidy and Root Nodule Symbiosis in Glycine

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Allopolyploidy and Root Nodule Symbiosis in Glycine TWO TO TANGO: ALLOPOLYPLOIDY AND ROOT NODULE SYMBIOSIS IN GLYCINE SUBGENUS GLYCINE 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 Adrian Federico Powell January 2017 © 2017 Adrian Federico Powell TWO TO TANGO: ALLOPOLYPLOIDY AND ROOT NODULE SYMBIOSIS IN GLYCINE SUBGENUS GLYCINE Adrian Federico Powell, Ph.D. Cornell University 2017 Polyploidy (or whole genome duplication) and root nodule symbioses with bacteria (termed ‘rhizobia’) have both been important phenomena in the evolutionary history of the legume family (Leguminosae). Recently, it has been proposed that polyploidy may have played a critical role in the development or refinement of nodulation. Given the varied potential impacts of polyploidy, effects on biotic interactions are plausible. However, direct studies of the interactions between these phenomena in symbiotic, nodule-forming species are lacking. In this dissertation, using a complex of recently formed allopolyploids in Glycine subgenus Glycine, the perennial relatives of soybean, we examined (1) the root metabolites and symbiotic signaling capacity of multiple allopolyploid species relative to the diploid progenitor species that hybridized to form each allopolyploid, (2) the nodulation-related responses of allopolyploids and diploid progenitors to rhizobia and (3) the transcriptome-level responses to inoculation in allopolyploid G. dolichocarpa (T2) and its diploid progenitors. These objectives were pursued using a variety of approaches including root metabolite profiling, inoculation trials, and RNA sequencing. We found that, while there were no common transgressive patterns in the root metabolite profiles of allopolyploids in the complex, one of the progenitors of T2 had distinctive root metabolite and exudate profiles; profiles of symbiotic signaling metabolites were also altered in the allopolyploid. In addition, T2 demonstrated an enhanced symbiotic capacity when inoculated with rhizobia compared to its diploid progenitors. Finally, transcriptomic analyses revealed patterns of non-additive expression in T2, with evidence of transcriptional responses to inoculation that were distinct from one or both progenitors and that highlighted differences in hormonal signaling responses. Taken together, our findings highlight effects of hybridity, and the properties of diploid progenitors, in determining the symbiotic capabilities of allopolyploids in Glycine subgenus Glycine. However, the combination of features from progenitors can enhance symbiotic responses in allopolyploids in ways that deviate from expectations of additivity. Such effects provide potential explanations for the apparent abilities of allopolyploids in Glycine subgenus Glycine to colonize novel habitats beyond their native ranges. BIOGRAPHICAL SKETCH Adrian Federico Powell is a plant biologist whose work focuses on using variety of metabolomic, transcriptomic and genomic approaches to explore the diversity of plant biotic interactions. He completed his B.Sc. degree at Trent University in 2008 and an M.Sc. at the same institution in 2010. Prior to commencing his studies at Cornell University, he also conducted research at the RIKEN Plant Science Center in Yokohama, Japan. Upon completion of his dissertation, he will continue his training in bioinformatics as a postdoctoral researcher at the Boyce Thompson Institute. iii ACKNOWLEDGEMENTS First, I want to acknowledge my dissertation committee for supporting me throughout this endeavor. To Jeff Doyle, my main dissertation advisor: thank you for providing me a fantastic opportunity for exploration and learning on this journey, for the innumerable insightful discussions and for your patience and continuing belief in me and my abilities – without your support none of this would have been possible. To André Kessler and Dan Buckley, thank you for your keen interest in teaching, for your willingness to share time and resources, and for your enthusiasm for my work. Many thanks to all members of the Doyle and Kessler labs over the years, with special thanks to Sue Sherman-Broyles. At Cornell, I would also like to thank Steve Vanek, Lynn Johnson and the Cornell Statistical Consulting Unit, and Alejandra Gandolfo for their guidance and willingness to help. Throughout my time at Cornell I have been supported by NSERC, NSF, 3CPG, the Presidential Life Sciences Fellowship, the Barbara McClintock Award, the SIPS Section of Plant Biology and teaching assistantships through the Office of Undergraduate Biology. I am grateful for the support of all these programs, institutions and organizations. Finally, I wish to thank all my friends at Cornell and elsewhere for making my time in graduate school a wonderful experience. Thanks also to my family members in Argentina and North America for their support. To Norma Pattuelli and Daniel Powell, my mother and father: thank you for all your support throughout my many years of study; I have only made it this far because of your constant love and encouragement. Finally, I would like to thank my partner, Elizabeth Fox, for all her support and love. iv TABLE OF CONTENTS Biographical Sketch ....................................................................................................................... iii Acknowledgements ........................................................................................................................ iv Chapter 1. Introduction ................................................................................................................... 1 Chapter 2. The Implications of Polyploidy for the Evolution of Signaling in Rhizobial Nodulation Symbiosis ..................................................................................................................... 5 Chapter 3. Effects of Allopolyploidy and Rhizobial Inoculation on Root Metabolite Profiles, Diversity, Exudation and Biosynthetic Gene Expression in Glycine subgenus Glycine .............. 46 Chapter 4. Enhanced Rhizobial Symbiotic Capacity in an Allopolyploid Species of Glycine (Leguminosae) .............................................................................................................................. 91 Chapter 5. Non-Additive Transcriptomic Responses to Inoculation with Rhizobia in Allopolyploid Glycine dolichocarpa .......................................................................................... 122 Chapter 6. Conclusions ............................................................................................................... 160 Appendix 1 .................................................................................................................................. 168 Appendix 2 .................................................................................................................................. 170 Appendix 3 .................................................................................................................................. 172 References ................................................................................................................................... 174 v CHAPTER 1 INTRODUCTION 1 The use of nitrogen fertilizers in agriculture has increased greatly since the 1960s, contributing to substantial yield gains in that time, and this use is expected to increase globally over the next several decades (Sutton and Bleeker 2013). However, fertilizer use presents a number of challenges. Nitrogen fertilizers contribute to atmospheric pollution through the release of NOx, which leads to the formation of ground level ozone, and N2O, which is itself a potent greenhouse gas (Reay et al. 2012; Winiwarter et al. 2013). Nitrogen fertilizer use in agricultural systems is also linked to algal blooms and eutrophication (Diaz and Rosenberg 2008; Sutton et al. 2011). In addition, the fossil fuels required in the production and use of nitrogen fertilizers are environmentally costly (Jensen et al. 2012). Given the estimated costs, initiatives and opportunities to manage better or reduce the use and impact of nitrogen fertilizers are highly desirable (Beatty and Good 2011; Sutton and Bleeker 2013). Legumes offer opportunities to address these challenges, because they engage in a process known as nodulation, which involves symbiosis with phylogenetically diverse soil bacteria collectively called rhizobia; these bacteria fix atmospheric nitrogen and make it available to the plant host (van Hameren et al. 2013). Legumes thus have the capacity to be an important source of nitrogen in sustainable agricultural systems (Crews and Peoples 2004). Knowledge of nodulation is being developed further and applied to agricultural practices through a variety of projects, including the N2Africa program funded by the Bill and Melinda Gates Foundation (Sprent 2012). How the nodulation symbiosis originated remains an important evolutionary question (Doyle 2011, 2016). Several researchers, noting the strong correlation between nodulation and a whole genome duplication (WGD) event approximately 50 Ma in an ancestor of papilionoid legumes, have suggested that polyploidy played a significant role in either the origin or the 2 refinement of this key symbiosis (Young et al. 2011; Kim et al. 2013b; Li et al. 2013). The ability of polyploidy to generate evolutionary novelty is widely accepted (Freeling and Thomas 2006; Madlung 2013; Wendel 2015) because whole genome duplication affects every aspect of plant biology,
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