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Mitochondrial Genomes of Plant Pathogenic Fungi

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Mitochondrial Genomes of Plant Pathogenic Fungi Research Collection Doctoral Thesis Mitochondrial genomes of plant pathogenic fungi Author(s): Torriani, Stefano F.F. Publication Date: 2008 Permanent Link: https://doi.org/10.3929/ethz-a-005807786 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Diss. ETH No. 18123 MITOCHONDRIAL GENOMES OF PLANT PATHOGENIC FUNGI A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH For the degree of DOCTOR OF SCIENCE Presented by STEFANO F. F. TORRIANI Dipl. Natw. ETH Born 17 January 1980 Citizen of Switzerland Accepted on recommendation of Prof. Dr. Bruce A. McDonald, examiner Prof. Dr. Alexander Widmer, co-examiner 2008 Table of contents SUMMARY 1 RIASSUNTO 3 CHAPTER 1 5 General introduction CHAPTER 2 25 The mitochondrial genome of Mycosphaerella graminicola CHAPTER 3 51 The evolutionary history of Mycosphaerella spp. mitochondrial genome CHAPTER 4 75 The mitochondrial genome of Phaeosphaeria nodorum CHAPTER 5 123 QoI resistance evolution in European populations of Mycosphaerella graminicola CHAPTER 6 143 Screening for QoI resistance in a global sample of Rhynchosporium secalis CHAPTER 7 159 General conclusions ACKNOWLEDGEMENTS 167 CURRICULUM VITAE 169 PUBBLICATIONS 169 To all those who manage to read from start to finish Summary The mitochondrial genomes of plant pathogenic fungi was the leitmotiv of this work that 1) completely annotated the mitochondrial genomes of two wheat-infecting pathogens, Mycosphaerella graminicola and Phaeosphaeria nodorum, 2) inferred the mitochondrial evolutionary history of M. graminicola and 3) studied the evolutionary mechanisms influencing the occurrence and spread of strobilurin (QoI) fungicide resistances. The two obtained mitochondrial genomes were the first analyzed from any species from the class Dothideomycetes, including more than 6000 known species and some of the most economically important plant pathogenic fungi. The fungal mitochondrial genomes displayed some common characteristics interspecifically, including a standard set of genes involved in oxidative phosphorylation, two genes for the large and the small ribosomal subunits and a set of tRNAs genes, which often clustered in groups showing conservation in gene order between organisms in the large Pezizomycotina subphylum of Ascomycota. The mitochondrial tRNA gene order was proposed as an additional criterion in phylogenetic analyses to distinguish between fungal classes. Another distinctive feature of fungal mitochondrial genomes is the variable number of introns. The evolutionary history of the M. graminicola mitochondrial genome was inferred using four sequence loci, dating the divergence from the ancestral Mycosphaerella populations, between 10,000 and 9,000 years ago, coinciding with the domestication of wheat and essentially confirming the analysis based on nuclear markers. The insertion/deletion polymorphisms distinguishing the mitochondrial haplotypes were characterized. A putative gene predicted to encode protein acting as virulence factor proposed to increase the pathogenicity to durum wheat (Triticum turgidum), was identified exclusively in mitochondrial RFLP haplotype 4. To provide better fungicide management strategies the evolutionary mechanisms driving the emergence and spread of resistance need to be studied. QoIs target the protein encoded by the mitochondrial gene cytochrome b. M. graminicola and the barley-infecting pathogen Rhynchosporium secalis were therefore screened for QoI resistance. All 841 tested R. secalis isolates from a global collection were completely sensitive with an estimated naïve resistance frequency less than 0.12%. M. graminicola populations displayed high QoI resistance 1 frequencies in Europe, ranging from 30% to 100%. In M. graminicola, selection, parallel genetic adaptation and migration were identified as the principal forces shaping the evolution of fungicide resistances. The same evolutionary pattern of QoI resistance in M, graminicola could be extended to other fungal pathosystems or fungicides having different modes of action. 2 Riassunto Il genoma mitocondriale dei funghi fitopatogeni è stato il filo conduttore di questo lavoro durante il quale: 1) è stato annotato l’intero genoma mitocondriale di due patogeni del frumento Mycosphaerella graminicola e Phaeosphaeria nodorum, 2) è stata dedotta la storia evolutiva di M. graminicola, 3) sono stati investigati i meccanismi evolutivi responsabili dello sviluppo e diffusione della resistenza ai fungicidi analoghi delle strobilurine. I due genomi mitocondriali ottenuti sono i primi analizzati di specie appartenenti alla classe Dothideomycetes, che comprende più di 6,000 specie e alcuni fra i funghi fitopatogeni economicamente più dannosi. I genomi fungini mitocondriali mostrano alcune caratteristiche comuni a livello interspecifico, come l’espressione di un gruppo di geni dedicati alla fosforilazione ossidativa, due geni codificanti per altrettanti RNA ribosomiali (rRNA) e una gamma di RNA di trasporto (tRNA), i quali sovente sono raggruppati in clusters e mostrano una conservazione nell’ordine genico fra gli appartenenti alla suddivisione Pezizomycotina. Questo lavoro propone di usare l’ordine genico dei tRNA mitocondriali quale criterio aggiuntivo in analisi filogenetiche per differenziare classi fungine. Un numero variabile di introni fra un organismo e l’altro è una caratteristica distintiva dei genomi mitocondriali dei funghi. La storia evolutiva del genoma mitocondriale di M. graminicola è stata dedotta usando quattro loci genetici datando la separazione di questa specie dalle popolazioni ancestrali di Mycosphaerella fra 10,000 e 9,000 anni fa, simultaneamente alla domesticazione del frumento; ciò che conferma i risultati di una precedente analisi basata su loci nucleare. Le inserzioni e delezioni di DNA, che distinguono gli aplotipi mitocondriali di M. graminicola, sono state caratterizzate identificando un gene putativo (esclusivo dell’aplotipo 4) che si suppone codifichi un fattore di virulenza in grado di aumentare la patogenicità verso il grano duro (Triticum durum). L’analisi dei meccanismi evolutivi alla base dello sviluppo e diffusione delle resistenze è di fondamentale importanza per fornire migliori strategie di gestione dei fungicidi. M. graminicola e Rhynchosporium secalis, un patogeno dell’orzo, sono stati dunque esaminati alla ricerca d’isolati resistenti ai fungicidi analoghi delle strobilurine che agiscono sul 3 citocromo b, codificato da un gene mitocondriale. Tutti gli 841 isolati di R. secalis provenienti dai cinque continenti sono risultati sensibili e la frequenza di resistenza stimata è inferiore a 0.12%. Le popolazioni europee di M. graminicola invece mostrano frequenze di resistenza variabili fra 30-100%. Dall’analisi di M. graminicola si deduce che selezione, adattamento genetico parallelo e migrazione sono le principali forze che modellano l’evoluzione delle resistenze. Questa interpretazione probabilmente può essere estesa ad altri sistemi patologici fungini e a fungicidi aventi modi d’azione differenti da quello dei fungicidi analoghi delle strobilurine. 4 CHAPTER 1 General introduction Chapter 1 General introduction 6 Chapter 1 General introduction Agriculture and pathogens - Past, Present and Future About 12,000 years ago humanity began the slow development from a hunter-gatherer to an agricultural society. Archeological and genetic findings support the origin of the agriculture in the Fertile Crescent of the Middle East between 10,000 and 12,000 years ago (Gopher et al. 2002; Salamini et al. 2002). This step, also known as the Neolithic revolution (Childe 1953), was crucial for shaping the human society we know today. Without agriculture the earth would be different, probably characterized by a reduced technology, political organization, no or little urbanization, less pollution and more biodiversity. The wild progenitors of the major Neolithic founder crops e.g. wheat (Triticum spp.), barley (Hordeum vulgare) and pea (Pisum sativum) have been identified in the Middle East (Diamond 1997; Haudry 1997). The continuous selection of desirable morphological traits has driven the slow process of wild grass domestication, creating the crop species we know today (Sharma and Waines 1980; Elias et al. 1996; Taenzler et al. 2002). The first crops were probably composed of species mixtures, but over time Neolithic farmers of the Middle East preferred planting crop species monocultures that subsequently spread to other regions in Europe and Asia (Diamond 1997). The invention of agriculture caused the simultaneous evolution of those pathogens infecting the wild progenitors of the founder crops. With agriculture intensification the landscape was modified, changing from a natural to an agricultural ecosystem, characterized by greater environmental homogeneity, lower species diversity and higher density of more host-specialized pathogens (Stukenbrock and McDonald 2008). The evolution of all three pathogens studied in this work, (Mycospharella graminicola, Phaeosphaeria nodorum and Rhynchosporium secalis) was shaped by human mediated environmental changes that created agricultural ecosystems. Stukenbrock and McDonald (2008) identified the four more likely scenarios for the evolutionary mechanisms by which plant pathogenic fungi have emerged in agricultural ecosystem; 1) host-tracking, when pathogen and host coevolved during host domestication
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