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Terminal Differentiation of Symbiotic Rhizobia in Certain Legume Species And Terminal differentiation of symbiotic rhizobia in certain legume species and its implications for legume-rhizobia coevolution A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF THE UNIVERSITY OF MINNESOTA BY Ryoko Oono IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY R. Ford Denison Advisor August, 2010 © Ryoko Oono 2010 Acknowledgements I would like to give special thanks to Bruce A. Sorrie, Alan Weakley, Carol A. McCormick, Will Cook, Mark T. Buntaine and Troy Mielke for helping me find legume species in North Carolina and Minnesota. This thesis would also not be possible without the mentorship of my committee members, Ruth G. Shaw, George D. Weiblen, Peter Tiffin, and Imke Schmitt as well as the patience and guidance from my thesis advisor, R. Ford Denison, and senior lab graduate student, Will C. Ratcliff. Many thanks for supporting me these last five years and taking the time in fostering my research skills. Additional thanks to many of the undergraduate students working in our lab, including Carolyn G. Anderson, who contributed to Chapter 4 and Justin Bower, whose work will build upon this dissertation. I would also like to thank Toby E. Kiers for giving me the opportunity to write a Tansley Review with her for New Phytologist. Thank you to Janet I. Sprent for collaborating with me on the publication of Chapter 2 and Mike Sadowsky for many interesting discussions on rhizobia. Thank you to the University of Minnesota Plant Biological Sciences Program for supporting me as a graduate student for these past five years with teaching assistantships and summer fellowships. I would like to acknowledge the College of Biological Sciences' Imaging Center at the University of Minnesota for their assistance in fluorescence microscopy and the assistance of the Flow Cytometry Core Facility of the University of Minnesota Cancer Center, a comprehensive cancer center designated by the National Cancer Institute, supported in part by P30 CA7759. This material is based in part upon work supported by the National Science Foundation under Grant Number 0918986. i Dedication This dissertation is dedicated to my family, friends (especially from Minnesota) and Mark. ii Abstract The symbiotic association between legume plants (Fabaceae) and nitrogen-fixing rhizobia is a classic system of cooperation, but with largely unexplored differences among species in life history traits. Rhizobia transform physiologically and morphologically into nitrogen-fixing bacteroids inside host nodules. The transformation is terminal (bacteroids are swollen and apparently nonreproductive) in some legume host species but not others, regardless of rhizobial genotype. The phylogenetic distribution of this host trait in the Papilionoideae subfamily of legumes suggests that the common ancestor of the papilionoids did not host terminally differentiated bacteroids and there appear to have been at least five independent origins of hosts imposing terminal differentiation on bacteroids. To consider possible advantages of this host trait, I compared the symbiotic efficiency of terminally and non-terminally differentiated bacteroids of a single rhizobial strain with dual-host capabilities. In the two available dual-host cases, I found greater fixation efficiency (N2 fixation per CO2 respiration) as well as plant return (host biomass) on investment per nodule mass in the hosts with terminal bacteroid differentiation than in those without. This suggests that host traits leading to terminal bacteroid differentiation may have been derived multiple times because of increased net symbiotic benefits to the host. Lastly, I tested whether legumes hosting terminally differentiated bacteroids impose sanctions, i.e. reduce benefits to the undifferentiated reproductive clonemates of less-mutualistic bacteroids in the same nodule. Host sanctions could maintain the evolutionary stability of the symbiosis despite “cheaters” - less-mutualistic rhizobia that potentially benefit from the fixation by other rhizobia sharing the same individual plant host. Legume roots were split so that half of each nodulated root system was exposed to nitrogen-free atmosphere (Ar:O2) to simulate cheating and the other half was in normal air (N2:O2). Rhizobial fitness (rhizobia per nodule) was compared between the two halves. A clear host sanctions effect in peas and alfalfa demonstrated that terminal differentiation of bacteroids does not compromise a legume host’s ability to sanction. Differences in rhizobial life history suggest various rhizobial symbiotic traits for cooperation and cheating, perhaps leading to different mechanisms in different legume host species that maintain stability of the mutualism. iii Table of Contents Acknowledgements ............................................................................................................. i Dedication .......................................................................................................................... ii Abstract…………………………………………………………………………………...iii List of Tables……………………………………………………………………………..vi List of Figures……………………………………………………………………………vii Chapter 1: Introduction .......................................................................................................1 Reproductive potential of bacteroids depends on host species......................................2 Evolutionary history: Is host-imposed rhizobial dimorphism ancestral or derived in legumes? ............................................................................................................….4 No consistent relationship between nodule type and rhizobial dimorphism…………………………………………………………..……5 Are there immediate benefits to individual plants from rhizobial dimorphism? ...…...6 How might sanctions differ when bacteroids are nonreproductive.........................…..8 How can nonreproductive bacteroids enhance their inclusive fitness?......….10 Can nonreproductive bacteroids cheat?.......................................................... 11 Should hosts with nonreproductive bacteroids invest in sanctions?............... 13 Testing for sanctions by comparing rhizobial strains..................................... 15 Manipulating nitrogen fixation to test for sanctions…..……………..………20 Figures…......................................................................................................................22 Table............................................................................................................................25 Chapter 2: Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation.........................................................................................................26 Summary… .................................................................................................................26 Introduction .................................................................................................................27 Materials and Methods ............................................................................................... 32 Results ........................................................................................................................ 40 Discussion .................................................................................................................. 44 Tables & Figures ........................................................................................................ 50 Chapter 3: Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids ………………………………………..................................................60 Introduction .............................................................................................................…61 iv Materials and Methods ............................................................................................... 64 Results ........................................................................................................................ 69 Discussion .................................................................................................................. 71 Figures & Tables......................................................................................................... 76 Chapter 4: Failure to fix nitrogen (N2) by nonreproductive symbiotic rhizobia triggers fitness-reducing sanctions against their reproductive clonemates in two legume host species ….......................................................................................................83 Introduction .................................................................................................................83 Materials and Methods ............................................................................................... 88 Results ........................................................................................................................ 91 Discussion .................................................................................................................. 93 Figures ........................................................................................................................ 99 Bibliography………………………….…………………………………...……………103 v List of Tables Table 1-1 Bacteroid properties and nodule type in representative legume species. …….25 Table 2-1 Bacteroid morphology assessment, nodule type and sequence data sources for legume species in the ancestral character reconstruction analysis. ……………….50 Table 2-2
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