A Dangerous Mix: From Natural Variation to Genetic Incompatibilities in Arabidopsis thaliana and Arabidopsis arenosa

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URI: http://hdl.handle.net/10900/110769
Dokumentart: Dissertation
Date: 2020-12-17
Language: English
Faculty: 7 Mathematisch-Naturwissenschaftliche Fakultät
Department: Biologie
Advisor: Weigel, Detlef (Prof. Dr.)
Day of Oral Examination: 2020-11-27
DDC Classifikation: 570 - Life sciences; biology
Keywords: Ackerschmalwand , Sand-Schaumkresse
Other Keywords:
Plant genetics
License: Publishing license including print on demand
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Plants and pathogens have co-evolved for millennia. As part of this long-term interaction, both the preservation of long-standing genetic variation, as well as the generation of novel genetic material is required from both the plant and the pathogen side to remain competitive when facing each other. As a consequence, some members of the plant immune system are highly diversified. Such is the case for plant NLRs, which act as intracellular receptors that recognize incoming pathogen effectors, thereby initiating a signalling cascade and ultimately resulting in cell death. The extensive variability of NLRs enables the recognition of a wide spectrum of pathogen effectors. However, sometimes this variability can backfire: When two divergent elements of the plant immune system, often two NLRs, or one NLR and another immune system component, meet in a hybrid plant – the progeny of a cross between two different accessions – they can trigger an immune response in the absence of a pathogen. This phenomenon is called hybrid incompatibility. Here, I study two sets of hybrid incompatibility cases in Arabidopsis thaliana and a case of inbreeding depression in its outcrossing relative Arabidopsis arenosa. In the first project, I study a set of A. thaliana incompatibility cases which are are the result of incompatible interactions between the NLR cluster RPP7, which confers strain-specific resistance to downy mildew, and RPW8, an atypical non-NLR resistance (R) gene cluster that confers broad-spectrum resistance to filamentous pathogens. I describe three independent cases where allele-specific interactions between these two loci result in incompatible hybrids. In addition, for two of these cases, I identify the causal genes for incompatibility from the RPW8 side: RPW8.1 and HR4. The resulting proteins of these two causal genes for incompatibility show length polymorphisms across different accessions which are characterized by 21- or 14- amino acid repeat number variations in their C terminal. I show that these C terminal repeats largely modulate the severity of the hybrid phenotype, and that only accessions carrying long RPW8.1 and short HR4 protein variants are incompatible when combined with particular RPP7 proteins. In the second project, I study a set of A. thaliana hybrid incompatibility cases where the hybrid is severely necrotic, does not develop past the cotyledon stage, and dies early on. I show that massive transcriptional changes take place in the hybrid, including the upregulation of most NLR genes, which likely contribute to its severely necrotic phenotype. I then identify the causal loci for incompatibility, DM10 and DM11, and show that DM10 is a singleton NLR that was relocated from an NLR gene cluster after A. thaliana speciation. I establish that the risk DM10 allele carries a premature stop codon, and although common and geographically widespread in the global A. thaliana population, co-occurrence with the risk DM11 allele is absent. In the third project, I screened for the presence of potential hybrid incompatibility cases occurring in natural A. arenosa populations, and show that heritable deleterious phenotypes are common, but, at least in some cases, likely the result of inbreeding depression. In short, my work presents a roadmap starting from identifying potential hybrid incompatibility cases to mapping and experimentally confirming the underlying causal loci, to establishing the underlying genetic and evolutionary processes building up to these incompatibilities.

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