Over the years, monitoring of virulence changes in Pst populations in the major wheat producing regions has revealed notable changes in pathogen movement and adaptation. These studies were based on pathogenicity surveys, which use sets of differential wheat lines carrying known resistance genes, either near isogenic lines or cultivars, for the characterisation of pathotypes at the seedling stage (Wellings et al. 2009). More recently, molecular and genomics techniques have been used to infer Pst population structure and genetic diversity, confirming patterns of adaptation hypothesised in pathotype-based approaches. Here, we summarise key findings and events from the past three decades, specifically focusing on patterns of spore dispersal and Pst evolution and adaptation.
Blowing in the wind
Pst urediniospores are windborne and can disperse at continental scales. Coupled with the obligate nature of the pathogen (requiring living tissue to survive), this has led to different scenarios for the observed seasonal and geographic patterns of dispersal. One such model is the local extinction and re-colonisation model, illustrated for example in China where regions of the Sichuan and Gansu provinces in which Pst prevails all year round act as a source of inoculum to the more northerly provinces in which wheat is predominantly grown as a winter crop (Brown & Hovmøller, 2002; Zeng & Luo, 2006). In this way, Pst populations re-establish at the beginning of each wheat cropping season in those regions where Pst spores are usually unable to over-winter. A similar pattern of spore movement according to prevailing winds and the seasonality of the cropping seasons has been speculated in North America, with spores migrating from southern central states of USA and Mexico to northern central states of USA and Canada (Chen, 2005). In North Western Europe, Pst spore dispersion appears to follow the continental-island model, first described by Hedrick (1985), and has been the predominant model of Pst spore dispersion in North Western Europe. In this region, urediniospores travel up to 1,700 km with prevailing winds, and migrating between UK, France, Germany and Denmark (Hovmøller et al 2002). Investigations of YR emergence events in countries where it was previously absent provide examples of rapid inter-continental foreign incursion. Australia has been subject to several known incursions, of which two were notably detrimental to the wheat industry due to their rapid spread: (i) the first occurrence of Pst, in 1979 (Wellings et al. 1987), and (ii) the 2002 incursion in Western Australia (Wellings et al. 2003), now known to have originated from the Middle East/East Africa (Ali et al. 2014a) and attributed to a single Pst isolate (Wellings et al. 2003). The more recent arrival of Pst isolates in South Africa in 1996 were related to the Mediterranean and Central Asian populations (Boshoff et al. 2002; Ali et al. 2014a), and was speculated to be due to wind dispersal or human activities (Ali et al. 2014a). In all three cases, human activity, most likely through accidental transport on clothing, has been either demonstrated or strongly speculated, highlighting the increasing role of globalised trade and international travel as a means for Pst urediniospore dispersal.
Pathogen evolution and adaptation
Prior to 2000, pathogenicity surveys and molecular studies using isolates collected across the main wheat-producing regions in Europe, Australia and America typically reported Pst populations were clonal in nature, and that pathotypes exhibited close-relatedness and low genetic variation - predominantly underpinned by single step-wise mutations (Hovmøller et al. 2002; Enjalbert et al. 2005; Chen, 2005; Steele et al. 2001; Chen et al. 2010; Ali et al. 2014a; Hubbard et al. 2015; Hovmøller et al. 2016). Such clonally-derived Pst mutations have caused several severe YR epidemics, due to the ‘breakdown’ of specific wheat Yr resistance genes present in large acreages across the agricultural landscape. Notable examples include breakdown of Yr17 in Northern Europe (Bayles et al. 2000), Yr27 in Ethiopia (Solh et al. 2012), and Yr9 in America, the Middle East and the Indian sub-continent (Chen et al. 2010; Singh et al. 2004). Before the year 2000, the only exceptions to such patterns of low Pst genetic variation were observed in isolates from the Himalayan (Nepal and Pakistan) and near Himalayan (China) regions, which exhibited high levels of genetic recombination, high ability for sexual reproduction and high genetic diversity (Duan et al. 2010; Mboup et al. 2009; Ali et al. 2014b). These areas were therefore classified the putative centres of Pst origin (Ali et al. 2014b). However, the last two decades have seen the emergence of unusual virulence profiles and aggressive strains across the world. The most noteworthy event was the rise of two strains, PstS1 and PstS2, across the USA (Chen et al. 2002; Markell & Milus, 2008), Europe (Hovmøller & Justesen, 2007) and Australia (Wellings, 2007) in the space of just three years in the early 2000s. A global study of pre- and post-2000 Pst races combining detailed virulence pathotyping and DNA fingerprinting found these while these two strains were genetically similar to each other, they were highly divergent from previous races in their respective geographic regions (Hovmøller et al. 2008). Their rapid spread was thought to be due to their increased aggressiveness (ability to yield more spores and for disease symptoms to occur more quickly) and high temperature adaptation - which was later demonstrated in the detailed study by Milus et al. (2009). In addition to PstS1 and PstS2, additional atypical occurrences of Pst races have since been reported. Enjalbert et al. (2005) demonstrated high levels of genetic divergence between the Pst population in northern France and a single clone specific to the South. What was atypical was that this single pathotype was maintained for a long time in this region, despite the presence of gene flow between Northern and Southern Pst populations. This isolate was later found to be more closely related to the Central Asian-Mediterranean population (Ali et al. 2014a). Similarly, instances of strong genetic divergence have also been revealed in North Western Europe (Flath & Barthels, 2002; Hovmøller & Justesen 2007a). Two groups of highly divergent pathotypes from the ‘old’ North-Western European population exhibited three to four times higher levels of genetic diversity (Hovmøller et al. 2007). In 2011, two novel Pst races disrupted the European Pst landscape (www.wheatrust.org). Named after the host varieties on which they were first detected, one race was virulent on wheat cv. ‘Warrior’ and the other was virulent on cv. ‘Kranich’. These were later characterised as PstS7 and PstS8 respectively (Ali et al. 2017), and were detected simultaneously across Europe and infected varieties that had exhibited durable adult plant resistance. Both races were distinct from the typical European isolates in that they produced an unusually high number of teliospores (Hubbard et al. 2015; Hovmøller et al. 2016). Additional Pst races have been characterised (PstS10 also known as ‘Warrior (-)’, PstS4 ‘Triticale aggressive’) and together with the other new genetically diverse Pst races, have come to largely dominate within Europe (Ali et al. 2017; Hovmøller et al. 2016; Hubbard et al. 2015). Collectively, these atypical observations, further supported by genetic diversity studies, have led to speculation of an aerial-induced foreign incursion, which would be the first of its kind in Europe since the establishment of Pst in Europe during the 19th century. Beyond Europe, rapid invasions and the subsequent Pst population changes have been responsible for a number of YR epidemics in Central Asia, North and East Africa (Ali et al. 2017).