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Tripartite Interactions of Legumes with Arbuscular Mycorrhizal Fungi And South Dakota State University Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange Electronic Theses and Dissertations 2018 Tripartite Interactions of Legumes with Arbuscular Mycorrhizal Fungi and Rhizobial Bacteria: Insight into Plant Growth, Seed Yield, and Resource Exchange Arjun Kafle South Dakota State University Follow this and additional works at: https://openprairie.sdstate.edu/etd Part of the Agricultural Science Commons, Agriculture Commons, Microbiology Commons, and the Plant Biology Commons Recommended Citation Kafle, Arjun, "Tripartite Interactions of Legumes with Arbuscular Mycorrhizal Fungi and Rhizobial Bacteria: Insight into Plant Growth, Seed Yield, and Resource Exchange" (2018). Electronic Theses and Dissertations. 2947. https://openprairie.sdstate.edu/etd/2947 This Dissertation - Open Access is brought to you for free and open access by Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. For more information, please contact [email protected]. TRIPARTITE INTERACTIONS OF LEGUMES WITH ARBUSCULAR MYCORRHIZAL FUNGI AND RHIZOBIAL BACTERIA: INSIGHT INTO PLANT GROWTH, SEED YIELD, AND RESOURCE EXCHANGE BY ARJUN KAFLE A dissertation in partial fulfillment of the requirements for the Doctor of Philosophy Major in Biological Sciences Specialization in Microbiology South Dakota State University 2018 iii ACKNOWLEDGEMENTS I would like to express my humble and deepest appreciation to my advisor Dr. Heike Bücking for letting me to work in her lab, igniting to think critically for developing research questions, designing experiments, analyzing and interpreting data, and to be an avid scientific reader and writer. Her purposeful enduring guidance has helped me somehow to be an independent scientist. I will keep her working ethics forever with me. Besides a venerable mentor, she has a great sense of caring too. I would like to extend my heartful gratitude to my committee members Dr. Volker Brozel, Dr. Senthil Subramanian, Dr. Yajun Wu, and Dr. Heide Mennenga for their insights, and encouragement, generous advice, and caring during my graduate program at SDSU. I would like to thank Dr. Kevin Garcia, Dr. Philip Pfeffer, Dr. Xiurong Wang, Dr. Michael Hildreth, Dr. Radhey Kaushik, Dr. Donald Auger, Dr. Arvid Boe for their generous help and suggestions whenever needed during the program. I am equally thankful to the Department of Biology and Microbiology for providing me with the support to complete my degree. Many more thanks to Jan Matson, Carol Doyle, Sharon Ellens for their facilitation in my research and a lovely smile. I would also like to acknowledge the funding agencies USDA, NSF, SD Soybean Research and Promotion Council, and the Agriculture Experiment Station at South Dakota State University. I am thankful and lucky to have many nice colleagues Dr. Carl Fellbaum, Dr. Jerry Mensah, Dr. Brandon Monier, Dr. Suresh Damodaran, Dr. Charles Halfman, Dr. Laura White, Dr. Sajag Adhikari, Dr. Praveena Kanchupati, Dr. Devi Ram Kandel, Nina Herrera, iv Vincent Peta, Janice Eibensteiner, Alex Soupier, Jaya Yakha, Jessica Mediger, Sunita Pathak, Sadikshya Aryal, Paul Gaillard, Dinesh Phuyal, Jyotshana Paudel, Vivek Shrestha, Mani Awale, and many more. Finally, I would like to extend my sincere thanks to my family. This research would not have been possible without their encouragement and moral support. And special thanks to my beloved wife Gitanjali and our two adorable children Himesh and Omnima. v TABLE OF CONTENTS LIST OF ABBREVIATIIONS .......................................................................................... ix LIST OF FIGURES ........................................................................................................... xi LIST OF TABLES ........................................................................................................... xix ABSTRACT ...................................................................................................................... xx CHAPTER 1: LITERATURE REVIEW ............................................................................ 1 1. Introduction ................................................................................................................. 1 2. Beneficial plant microbe interactions of soybean plants ............................................. 3 2.1 Arbuscular mycorrhizal fungi................................................................................ 3 2.1.1 Importance of arbuscular mycorrhizal fungi for yield and nutrient uptake of soybeans ...................................................................................................................... 7 2.1.2. Importance of arbuscular mycorrhizal fungi for the stress resistance of soybean ........................................................................................................................ 9 2.2. Nitrogen fixing symbiosis with rhizobia ............................................................ 11 2.2.1. Significance of rhizobia for soybean agriculture ............................................. 14 2.3. Tripartite symbiosis with arbuscular mycorrhizal fungi and rhizobia................ 15 2.4 Symbiosis with endophytic bacteria or fungi ...................................................... 18 3. Important research gaps and future challanges ......................................................... 19 4. References ................................................................................................................. 21 CHAPTER 2: NUTRIENT DEMAND AND FUNGAL ACCESS TO RESOURCES CONTROL THE CARBON ALLOCATION TO THE SYMBIOTIC PARTNERS IN TRIPARTITE INTERACTIONS OF MEDICAGO TRUNCATULA ............................... 32 2.1 Abstract ................................................................................................................... 33 2.2 Introduction ............................................................................................................. 34 2.3 Material and methods .............................................................................................. 37 2.3.1 Plant, fungal, and bacterial material ................................................................. 37 vi 2.3.2 Experimental design ......................................................................................... 39 2.3.3 Biomass characteristics, and quantification of rhizobial and AM root colonization ............................................................................................................... 41 2.3.4 Measurements of nitrogenase activity .............................................................. 41 2.3.5 Quantification of P, 13C and 15N in plant tissues .............................................. 42 2.3.6 Gene expression analysis .................................................................................. 43 2.3.7 Statistical analysis ............................................................................................ 44 2.4 Results ..................................................................................................................... 46 2.4.1 Tripartite interactions can act synergistically on biomass and nutrient uptake of plants.......................................................................................................................... 46 2.4.2 Carbon allocation to root symbionts depends on the pathway for symbiotic nitrogen uptake .......................................................................................................... 51 2.4.3 Fungal access to nitrogen affects the expression of sucrose transporters in the roots of tripartite interactions .................................................................................... 52 2.4.4 Plants allocate carbon resources to their symbiotic partners depending on their nutrient demand ......................................................................................................... 55 2.4.5 The expression of plant SUT and SWEET transporters is consistent with the observed differences in carbon allocation under different nutrient demand conditions for the host ................................................................................................................. 57 2.5 Discussion ............................................................................................................... 62 2.6 References ............................................................................................................... 71 2.7 Supporting information ........................................................................................... 79 CHAPTER 3: NEUTRAL OR REDUCED GROWTH OF MEDICAGO TRUNCATULA IN TRIPARTITE INTERACTIONS: WAS IT ONLY CARBON COST? ...................... 93 3.1 Abstract ................................................................................................................... 93 3.2 Introduction ............................................................................................................. 94 3.3 Material and methods .............................................................................................. 98 vii 3.3.1 Plant, fungal and rhizobial materials ................................................................ 98 3.3.2 Experimental design and
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