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The Evolution of Nitrogen-Fixing Root Nodules, Analysis of Conserved The Evolution of Nitrogen-fixing root Nodules Luuk Rutten 2020 The Evolution of Nitrogen-fixing root Nodules Luuk Rutten The Evolution of Nitrogen-fixing root Nodules Analysis of conserved signalling modules in legumes and Parasponia Luuk Rutten Propositions 1. Multi-functionality, rather than high stringency, represents the ancestral function of the LYK-I clade LysM-type receptor kinases (This thesis). 2. The duplication of the NOD FACTOR PERCEPTION (NFP) gene was a driver for the evolution of nodule symbiosis (This thesis). 3. A priori equal weights for gains and losses in evolutionary rate models is a flawed assumption (Werner et al. 2014). 4. Engineered Honeybee symbionts, which combat the varroa destructor mite, cannot solve the global pollinator decline (Leonard et al. 2020). 5. Improvisation is to be preferred over detailed planning. 6. The ignorance for lab safety increases with the number of safety rules in place. Propositions belonging to the thesis, entitled: The evolution of Nitrogen-fixing root Nodules; analysis of conserved signalling modules in legumes and Parasponia Luuk Rutten, 21st of October 2020 Leonard, Sean P., J. Elijah Powell, Jiri Perutka, Peng Geng, Luke C. Heckmann, Richard D. Horak, Bryan W. Davies, Andrew D. Ellington, Jeffrey E. Barrick, and Nancy A. Moran. 2020. “Engineered Symbionts Activate Honey Bee Immunity and Limit Pathogens.” Science 367 (6477): 573–76. Werner, Gijsbert D. A., William K. Cornwell, Janet I. Sprent, Jens Kattge, and E. Toby Kiers. 2014. “A Single Evolutionary Innovation Drives the Deep Evolution of Symbiotic N2-Fixation in Angiosperms.” Nature Communications 5 (January): 4087. Evolution of Nitrogen-fixing root Nodules Analysis of conserved signalling modules in legumes and Parasponia Lukas Johannes Joseph Rutten Thesis committee Promotor Prof. Dr Ton A.H.J Bisseling Professor of Molecular Biology Wageningen University & Research Co-promotor Dr Rene Geurts Associate professor, Laboratory of Molecular Biology Wageningen University & Research Committee members Prof. Dr Toby Kiers, VU Amsterdam, Department of Ecological Science. Prof. Dr Dolf. Weijers, Wageningen University & Research, Laboratory of Biochemistry Prof. Dr ir. Bart. P.H.J Thomma, Wageningen University & Research, Laboratory of Phytopathology Dr. Kasper Røjkjær Andersen, Aarhus University, Department of Molecular Biology and Genetics This research was conducted under the auspices of the Graduate School Experimental Plant Sciences. DOI: https://doi.org/10.18174/517889 ISBN: 978-94-6395-350-4 Evolution of Nitrogen-fixing root Nodules Analysis of conserved signalling modules in legumes and Parasponia Lukas Johannes Joseph Rutten Thesis Submitted in the fulfilment of the requirements for the degree of doctor at Wageningen university by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board. To be defended in Public on Wednesday 21 October 2020. 16:00 Authored by: Lukas Johannes Joseph Rutten. Phd Thesis with references, with summary in English. Entitled: Evolution of Nitrogen-fixing root nodules; Analysis of conserved signalling modules in Legumes and Parasponia Wageningen University, Wageningen, The Netherlands (2020) DOI: 10.18174/517889 ISBN: 978-94-6395-350-4 Table of contents Chapter 1. General Introduction 6 Chapter 2. Commonalities in symbiotic plant-microbe signalling 34 Chapter 3. Comparative genomics of the non-legume 66 Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses Chapter 4. Duplication of symbiotic Lysin Motif-receptors 94 predates the evolution of nitrogen-fixing nodule symbiosis Chapter 5. Analysis of Nodulation correlated Receptor like 134 kinases of Parasponia reveals novel phenotypes in the infection process Chapter 6. A remote cis-Regulatory Region is required for NIN 176 expression in the pericycle to initiate nodule primordium formation in Medicago Truncatula Chapter 7. General Discussion 206 Thesis Summary 226 List of Publications 229 Acknowledgements 230 Curriculum Vitae 233 CHAPTER 1 General Introduction 8 | Chapter 1 Plant-microbe symbiosis as nitrogen acquisition strategy One of the largest challenges of a plant in a non-aqueous environment is the acquisition of key nutrients to support growth. The first colonization of land by vascular plants is correlated with the origin of plant resource acquisition structures such as roots (Raven and Edwards 2001). A major strategy for resource acquisition strategies is the formation of symbiotic interactions with bacteria or fungi, which have originated earlier than the formation of plants roots. The earliest forms of plant life on land faced a continuous struggle to find symbionts for nutrient acquisition (Selosse and Le Tacon 1998; Brundrett 2002; Wang et al. 2010; Yue et al. 2012). Symbiotic associations occur in different levels of intimacy, from loosely attached bacteria or fungi at the plant surface to endosymbiosis inside plant cells. One of the hallmarks of plant-microbe symbioses is the nitrogen-fixing nodule endosymbiosis, mostly known because of economically important legume species such as peas and beans. In this interaction bacteria are housed intracellularly in so-called nodules; specialized organs formed on the plant root or stems. Inside the nodules plants provide the optimal conditions for the bacteria to convert atmospheric nitrogen into ammonia, which they provide to the plants in exchange for photosynthates. This interaction is however limited to a relatively small number of plant species. Only about 2.5% of the angiosperm families is able to form a nitrogen-fixing nodule endosymbiosis. The overapplication of chemical fertilizer in agriculture leads to major environmental problems in terrestrial and aquatic ecosystems. For example nitrogen deposition causes a loss of biodiversity in natural habitats by competitive exclusion of characteristic species by more nitrophilic plants (Bobbink, Hornung, and Roelofs 1998; Choudhury and Kennedy 2005). While leaching of nitrogen into aquatic ecosystems may cause algal blooms, which can reach toxic levels for existing plant and animal life (Camargo and Alonso 2006). Therefore scientist have considered it a major objective to engineer a nitrogen fixing endosymbiosis in major crop plants (Myriam Charpentier and Oldroyd 2010; Mus et al. 2016). However in order to engineer a crop plant one must first answer the question how this intricate nitrogen- fixing nodule endosymbiosis evolved, to know the adaptations required to engineer into crops such as rice or maize. A nitrogen-fixing endosymbiosis can occur with three different types of bacteria: i. Filamentous Actinobacteria form the genus Frankia, nodulating a paraphyletic assembly of 25 genera distributed of 8 taxonomic families. ii. Rhizobia a paraphyletic group of - α, β and γ-Proteobacteria, nodulating Legumes (Fabaceae) and Parasponia (Cannabaceae) and iii. Nostoc spp., a cyanobacterium infecting plants of the genus Gunnera (Gunneraceae). Common to these three types of symbiosis is that bacterial General Introduction | 9 entry is preceded by host cell divisions and that once inside the cell the bacteria are enveloped by a host derived membrane. The Gunnera-Nostoc symbiosis is relatively unstudied and occurs only in the Gunnera genus the single member of the Gunnerales order. Cyanobacterial associations such as with Cyanobacteria Anabaena and Nostoc are usually known to occur extracellularly in like leaf cavities of the fern Azolla and coralloid roots of different Cycad species. The signalling cues 1 on how the intracellular accommodation in Gunnera is achieved is unknown. Rhizobium and/or Frankia nodulation occurs in several taxonomic lineages and has received more attention than cyanobacterial associations. These nodulating lineages are relatively closely related, with a distribution over four taxonomic orders; Fabales, Fagales, Cucurbitales and the Rosales. These orders are known as the Nitrogen- Fixing Clade (NFC) (Soltis et al. 1995). However, outside of the legume dominated Fabales order, nodulation is relatively rare. Thus even within the NFC, nodulation seems to be the exception rather than the rule. The nitrogen fixing endosymbiosis in this clade of plants have fascinated researchers for decades. Due to their economic importance, most studies towards nodulation have been conducted on rhizobium-legume symbiosis. The development of two model legume systems Medicago truncatula (Medicago) and Lotus japonicus (Lotus), chosen for their small genome sizes and diploid genome, has greatly increased the speed of discoveries of genetic components required for symbiosis. Unfortunately, there is still a severe lack of knowledge on other nodulation systems, such as Frankia- based nodulation. In this introduction, I will summarize the essentials of these discoveries, with a focus on symbiotic signalling and signal transduction. In order to finally come to a strategy for providing insight in the evolutionary requirements for the evolution of nitrogen fixing symbiosis. What are root Nodules and are they Novel? The root nodules in the nitrogen fixing endosymbiosis serve four essential functions. (i) Nodules contain a population of cells that are permissive for intracellularly infection by the symbiont. (ii) Selective access to the nodule interior allows hosting of a clonal population of the symbiotic partner of choice. (iii) Nodules are optimized for nutrient exchange between host and microsymbiont. (iv) Nodules provide the optimal physiological
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