Austropuccinia psidii (myrtle rust).

Austropuccinia psidii is a rust fungus with a wide and expanding host range within the Myrtaceae, with over 440 host species currently known (Carnegie and Lidbetter, 2012; Morin et al., 2012; Pegg et al., 2014). Like many rusts, urediniospores of A. psidii can be wind-dispersed over long distances. Viable spores have been detected on clothing and personal effects following visits to rust-affected plantations (Langrell et al., 2003), and this is a viable pathway for dispersal. Furthermore, there are several instances of (accidental) long-distance movement of A. psidii on diseased plants, both within and between continents (Loope et al., 2007; Kawanishi et al., 2009; Carnegie and Cooper, 2011; Zambino and Nolan, 2012). Under sub-optimal conditions, the rust can remain un-symptomatic within plants for more than a month (Carnegie and Lidbetter, 2012). This combination of wide host range and ease of long-distance dispersal make A. psidii a successful invasive pathogen. It has spread quickly once established in new countries, including Jamaica (MacLachlan, 1938), Hawaii (Uchida and Loope, 2009), Australia (Carnegie and Cooper, 2011; Pegg et al., 2014) and New Caledonia (DAVAR Nouvelle-Calédonie, 2014). Severe impact on a range of Myrtaceae has been recorded in amenity plantings, commercial plantations and the native environment. A. psidii was first identified as an invasive pathogen in the 1930s when it caused extensive damage to allspice (Pimenta dioica) plantations in Jamaica (Smith, 1935; MacLachlan, 1938). A. psidii has been identified as a quarantine risk for some time in many countries including Australia (Australian Quarantine Service, 1985; Grgurinovic et al., 2006), South Africa (Coutinho et al., 1998) and New Zealand (Kriticos and Leriche, 2008).

Peronosclerospora sorghi (sorghum downy mildew).

P. sorghi causes sorghum downy mildew, which can result in severe economic losses of both sorghum and maize. It has been a particularly invasive pathogen: it was introduced to the Americas where it has spread on both sorghum and maize causing considerable damage (Frederiksen et al., 1973). Quarantine restrictions probably maintained the USA free of sorghum downy mildew until the early 1960s (Reyes et al., 1964; Frederiksen, 1980a). Information on the spread of the disease and the damage it causes is available in the literature reporting its spread in the USA (Frederiksen et al., 1970) and elsewhere in the Americas (Frezzi, 1970; Grobman, 1975; Burtica et al., 1992).

Spread of the invasive pathogen Lecanosticta acicola on species of Pinus in Bulgaria

The brown spot needle blight, caused by the fungal pathogen Lecanosticta acicola, has been the most serious and damaging disease on needles of Pinus spp. in recent years. In Bulgaria, the pathogen was reported for the first time in 2017 in a generative plantation of Pinus sylvestris in the region of the State Forestry Ardino, the Eastern Rhodopes. The newly- established invasive pathogen is considered highly adaptable to new hosts and environmental conditions. The life cycle and symptoms of the disease strongly suggest that the new emerging pathogen has the potential to cause severe damages and is a serious threat to naturally distributed species of Pinus in the country. In the period 2018-2019, a spread of L. acicola from the initial outbreak was established throughout stands of P. sylvestris and P. nigra on the territory of Kardzhali District.

Emergence and populations genomics of the highly invasive chestnut blight pathogen

Invasive pathogens are a threat to forest and agroecosystems, as well as animal and human health. Identifying genomic determinants of pathogen evolution, as well as investigations into the genetic structure of invasive pathogen populations provide fundamental insights to why species can emerge as invasive pathogens. In this PhD project I investigated the emergence and population genomics of the invasive chestnut blight fungus Cryphonectria parasitica, using comparative and population genomic approaches. C. parasitica recently emerged as an invasive bark pathogen on non-Asian Castanea species in North America and Europe. In the first chapter, I investigated genomic determinants of lifestyle transitions in the genus Cryphonectria, by genome comparisons of C. parasitica and its sister species. The study uncovered a striking loss of genes associated with carbohydrate metabolism in the invasive pathogen C. parasitica, which may have promoted its pathogenicity on Castanea species. The second chapter explores the emergence and diversification of a highly invasive chestnut blight lineage across south-eastern Europe. By analyzing the genome-wide diversity of a large set of C. parasitica isolates of predominantly European origin, the study showed that a highly successful clonal pathogen lineage can emerge from a recombinant bridgehead population within Europe. Interestingly, the emergence of this clonal lineage was accompanied by an evolutionary transition from mixed mating type populations to single mating type outbreak populations. Lastly, in the third chapter I investigated temporal changes in genetic diversity of established C. parasitica populations in southern Switzerland, as well as potential links between the presence of the deleterious hyperparasitic mycovirus Cryphonectria hypovirus 1 (CHV1) and fungal genome-wide diversity. The results indicate increased mating among related fungal individuals, resulting in high genetic similarity of genotypes and facilitated CHV1 transmission. There were no substantial changes in fungal population structure and after ˜30 years and no detectable impact of CHV1 presence on fungal genome-wide diversity. Although our results show stable CHV1 incidence in fungal populations over three decades, the short-term interaction dynamics are likely highly volatile. The overall findings of this PhD thesis highlight the relevance of genomic determinants facilitating pathogen emergence and invasions. C. parasitica is a useful model to study fundamental questions of pathogen evolution and invasive processes, as well as antagonistic pathogen-hyperparasite interactions.