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Understanding the Genetic Basis for Competitive Nodule Formation by Clover Rhizobia

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Understanding the Genetic Basis for Competitive Nodule Formation by Clover Rhizobia Understanding the genetic basis for competitive nodule formation by clover rhizobia Shaun Ferguson (MSc) A thesis submitted for the degree of Doctor of Philosophy Department of Microbiology and Immunology, The University of Otago, Dunedin New Zealand December 31st, 2018 Abstract Clovers enter a symbiotic relationship with particular rhizobia through a highly specific and complex signal exchange culminating in the formation of nitrogen-fixing root nodules. Legumes exude flavonoids that are perceived by compatible rhizobia through a LysR-type regulator NodD. Activated NodD mediates expression of the nodulation (nod) genes, which produce a cocktail of signalling molecules known as Nod factors (NF). Recognition of NF by compatible legumes initiates nodule formation. Distinct strains of the clover-nodulating species, Rhizobium leguminosarum bv. trifolii (Rlt), vary in their ability to nodulate different clover species effectively, and to form nodules in competition with other strains. This is important agriculturally as indigenous strains often outcompete added inoculum strains that are superior at nitrogen fixation. We investigated the genetic determinants of varying host responses between three Rlt strains that differed in their ability to form efficient symbioses on white, red and subterranean clovers. To determine whether differences in nod gene expression contributed to this host specificity or competitive ability, we investigated the induction of nodA and nodF promoters from the three strains. The studies revealed significant variation in nod gene expression in response to flavonoid 7,4’-dihydroxyflavone, due to both the host strain background and the particular promoter. The strength of promoter expression of nodA or nodF also appeared to correlate with the competitive ability of the Rlt strain. We also showed that expression of the nodF operon had a non-equal influence on symbiotic proficiency depending on the Rlt strain, and elevated nodF expression appeared to enhance nodulation of annual clover species. Distinct phenological barriers exist that generally limit efficient Rlt symbiosis to either annual or perennial clover hosts. We found that Rlt nod gene expression profiles correlate with success on a specific type of host. We suggest that a two receptor system exists in clover, where following entry via a broad-spectrum receptor, a stringent cortical receptor distinguishes the NF profile produced, providing greater compatibility scrutiny by the host. Previously Rhizobium leguminosarum species were considered to contain a single copy of nodD. However we showed that some strains of Rlt contain a second copy of nodD, designated nodD2. Single and double nodD1 and nodD2 markerless deletion mutants i were constructed in Rlt strain TA1. The nodD1 deletion mutant revealed only a slight reduction in nodulation on white clover, whereas deletion of both copies of nodD resulted in abolished nodulation, which was restored by complementation with either nodD1 or nodD2. Together these results provided evidence of a functional NodD2 in some strains of Rlt. Moreover, we demonstrated that NodD1 and NodD2 show significant differences in their capacity to induce nod gene expression and infection thread (IT) formation. NodD1 and NodD2 protein structure predictions suggested variation in their flavonoid binding pockets, and furthermore NodD2 appeared to confer the ability to nodulate a broader range of hosts. Significantly, competition studies revealed an important role for NodD2 in competitive nodule formation on white clover. nodD2 was found in the genomes of eight out of 13 strains of Rlt investigated, and was absent from the 13 strains with genome sequence available of another biovar of the same species, Rhizobium leguminosarum bv. viciae (Rlv). It appeared that nodD2 arose via two distinct genetic mechanisms, duplication in some strains and horizontal acquisition in others. Phylogenetic analysis of the Rlt NodD sequences revealed distinct clustering relating to the phenological distinction of the hosts. There was a correlation between the presence of NodD2 and the ability to form effective symbiosis with perennial clover hosts. We propose that NodD2 responds to a different inducer than NodD1 that is produced in the cortical cells of the host, and results in a specific NF profile that is perceived by the stringent cortical receptor, required for efficient and competitive infection of perennial clovers. A pipeline for transcriptomic analysis of clover rhizosphere-grown Rlt was developed with promising early results. Despite a limited exploratory investigation, two of three genes chosen for investigation revealed a slight competitive disadvantage when deleted. This RNA-seq analysis has provided a basis for future large scale in-depth transcriptomic analysis to determine genetic traits contributing to rhizosphere competence. In summary, we have determined several genetic traits to be utilised as selection criteria for highly competitive inoculant strains. Furthermore, the transcriptomic pipeline developed will enable identification of further genetic factors contributing to successful symbiosis to also be used as selection criteria for high-quality clover inoculants in NZ. ii Acknowledgements The first person I would like to thank is my Supervisor Professor Clive Ronson. I have spent years working in his lab and I am extremely grateful for his constant support throughout my studies. His knowledge and insight has helped guide me to where I am now. I would like to thank the members of the Department of Microbiology and Immunology, and in particular, the 6th floor crew. I would especially like to thank members of lab 607, specifically Anthony Major, whom I worked closely with throughout this project, and Dr John Sullivan for putting up with my constant questions and for teaching me most of what I know in the lab. Additionally I would like to thank Dr. Josh Ramsay for his processing of the RNA-seq data, and Ben Perry for giving up his time to teach me how to perform these analyses for myself in the future. I am grateful that I could be a part of the MBIE collaboration and work towards a meaningful and practical goal, and for the knowledge and advice that came from our correspondence. Furthermore my studies would not have been possible without the financial assistance provided by the fund, for which I am extremely thankful. I am also very thankful for the financial support provided by the Department of Microbiology and Immunology which supported me at the end of my work and also helped me attend conferences which were amazing experiences I would have otherwise never had. I am very appreciative for the opportunity provided by Professor Philip Poole to spend time at the University of Oxford, and a special thanks to Dr Vinoy Ramachandran for all the time he put in to pass on his expertise on RNA-seq. Finally I am eternally grateful for the love and support of my family throughout, and for my partner Emily for constantly being there when I needed her. I could not have achieved this without them. iii Table of contents Abstract ................................................................................................................................................. i Acknowledgements ........................................................................................................................ iii Table of Figures ................................................................................................................................ix Table of Tables ............................................................................................................................... xiii List of Abbreviations...................................................................................................................... xv 1 General Introduction ............................................................................................................... 1 1.1 Overview ........................................................................................................................................ 2 1.2 Nitrogen fixation ............................................................................................................................ 4 1.2.1 Biological nitrogen fixation ..................................................................................................... 4 1.3 Agriculture in New Zealand ........................................................................................................... 4 1.3.1 Costs associated with nitrogen fertiliser use .......................................................................... 5 1.3.2 Issues with the current commercial exploitation of the rhizobium-legume symbiosis ......... 6 1.4 Rhizobium leguminosarum ............................................................................................................ 7 1.4.1 Classification and features...................................................................................................... 7 1.4.2 Rhizobium leguminosarum bv. trifolii strains of interest in this study ................................... 7 1.4.3 Variation in symbiotic proficiency .......................................................................................... 8 1.5 Trifolium legumes .......................................................................................................................... 8 1.5.1 The main Trifolium species of interest in this study ..............................................................
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