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Natural and CRISPR-Induced Genetic Variation for Plant Immunity

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Natural and CRISPR-Induced Genetic Variation for Plant Immunity Natural and CRISPR-induced genetic variation for plant immunity Baptiste CASTEL Thesis submitted to the University of East Anglia for the degree of Doctor in Philosophy The Sainsbury Laboratory February 2019 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. 1 2 Abstract Our understanding of the genetic basis of a trait primarily relies on analysing heritable phenotypic diversity. For instance, different accessions of Arabidopsis thaliana (Arabidopsis) can either be resistant or susceptible to a given strain of Albugo candida, an oomycete that causes the white rust disease. The virulent Albugo candida race Exeter1 (AcEx1) can grow on most Arabidopsis accessions. Using the resistant Arabidopsis Oy-0, I mapped and cloned the gene responsible for AcEx1 resistance: White Rust Resistance 4A (WRR4A). Arabidopsis Col-0 also contains WRR4A but does not resist AcEx1. I found that WRR4ACol-0 has an early stop codon, which is responsible for the recognition specificity of some effector candidates from Albugo candida. This example illustrates how natural diversity can be used to identify Resistance-genes and reveal components of the plant immune system. However, natural diversity is not always available. Clustered and regularly interspaces short palindromic repeats (CRISPR) from bacterial genomes defines an immune system, re-invented for genome editing. I optimized a CRISPR-Cas9 method to generate null alleles in Arabidopsis. Using this method, I produced a double mutant of two immunity- related gene candidates that are in tandem in the genome: AtNRG1A and AtNRG1B. I confirmed the 7-year-old hypothesis that NRG1A and NRG1B are redundantly required for signalling downstream of multiple Resistance-genes, mainly from the TIR-NLR immune receptor family. So far very few genes required for immunity upon Resistance-protein activation were defined. This second example illustrates that CRISPR can be used to generate variation to unravel redundant genetic pathways. The widespread adoption of CRISPR tools is likely to lead to a better understanding of the plant immune system. Ultimately, it will result in solutions to deploy genetics-based resistance to protect our crops from disease, reducing the need for chemicals. 3 Table of contents Abstract ............................................................................................................................... 3 Table of contents ................................................................................................................ 4 Acknowledgments .............................................................................................................. 8 Major abbreviations ............................................................................................................ 9 List of publications ............................................................................................................ 10 Chapter 1 : General Introduction ........................................................................................... 11 1.1 Molecular Plant-Microbe Interactions ......................................................................... 11 1.1.1 The plant immune system ...................................................................................... 11 1.1.2 NLRs: Structure ....................................................................................................... 13 1.1.3 NLRs: Activation ..................................................................................................... 17 1.1.4 NLRs: Signalling ..................................................................................................... 20 1.2 Albugo candida, a plant pathogen oomycete ............................................................. 25 1.2.1 Taxonomy .............................................................................................................. 25 1.2.2 Life cycle ................................................................................................................ 25 1.2.3 Impact and management ..................................................................................... 26 1.2.4 Virulence ................................................................................................................ 26 1.2.5 White Rust Resistance-genes discovery ............................................................... 28 1.3 CRISPR for genome editing ......................................................................................... 29 1.3.1 CRISPR: a bacterial immune system ..................................................................... 29 1.3.2 CRISPR for genome editing .................................................................................. 30 1.3.3 CRISPR for plant immunity ................................................................................... 37 Chapter 2 : Materials and methods ...................................................................................... 39 2.1 Material ........................................................................................................................ 39 2.1.1 Plant material ......................................................................................................... 39 2.1.2 Microbial material ................................................................................................. 39 4 2.1.3 Media ..................................................................................................................... 40 2.1.4 Antibiotics ............................................................................................................. 41 2.2 Methods ....................................................................................................................... 41 2.2.1 Molecular Biology ................................................................................................. 41 2.2.2 Plant biology ......................................................................................................... 45 2.2.3 Pathology assay .................................................................................................... 47 Chapter 3 : Allelic variation in the TIR-NLR WRR4 defines white rust resistance specificity ............................................................................................................................................... 50 3.1 Introduction ................................................................................................................. 50 3.2 Results........................................................................................................................... 51 3.2.1 Col-0 displays a weak WRR4A-dependent response to AcEx1 ............................ 51 3.2.2 Oy-0 resists AcEx1 via two loci WRR13 and WRR11 .............................................. 52 3.2.3 Fine mapping of WRR13 ........................................................................................ 52 3.2.4 Fine mapping of WRR11 ........................................................................................ 54 3.2.5 WRR4AOy-0 confers full resistance to AcEx1 ......................................................... 55 3.2.6 An early stop codon in WRR4A confers specificity in Albugo candida secreted protein recognition ....................................................................................................... 56 3.2.7 WRR4AOy-0 resistance can be transferred in the crop Camelina sativa ............... 60 3.3 Discussion .................................................................................................................... 62 3.3.1 WRR11 QTL on chromosome 3 remains unrevealed ............................................ 62 3.3.2 An early stop codon in a TIR-NLR causes loss of recognition of AcEx1 ............. 62 3.3.3 Crops can be protected using R-genes from Arabidopsis .................................. 62 Chapter 4 : Optimization of CRISPR-Cas9 method in Arabidopsis ..................................... 64 4.1 Introduction ................................................................................................................. 64 4.1.1 Aspiration .............................................................................................................. 64 4.1.2 Current status of CRISPR in Arabidopsis ............................................................. 64 4.2 Results ......................................................................................................................... 66 4.2.1 T-DNA assembly is facilitated by the Golden Gate cloning method ................... 66 5 4.2.2 Allyl alcohol enables to select CRISPR-induced Arabidopsis mutations ........... 68 4.2.3 An overdrive sequence at the T-DNA right border does not affect the CRISPR activity ........................................................................................................................... 70 4.2.4 UBI10, YAO or RPS5a promoter-controlled Cas9 expression enhances mutation rates ............................................................................................................................... 72 4.2.5 Codon optimization of Cas9 and presence of an intron elevate mutation rates ......................................................................................................................................
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