Yellow Rust Epidemics Worldwide Were Caused by Pathogen Races from Divergent Genetic Lineages

Abstract

We investigated whether the recent worldwide epidemics of wheat yellow rust were driven by races of few clonal lineage(s) or populations of divergent races. Race phenotyping of 887 genetically diverse Puccinia striiformis isolates sampled in 35 countries during 2009–2015 revealed that these epidemics were often driven by races from few but highly divergent genetic lineages. PstS1 was predominant in North America; PstS2 in West Asia and North Africa; and both PstS1 and PstS2 in East Africa. PstS4 was prevalent in Northern Europe on triticale; PstS5 and PstS9 were prevalent in Central Asia; whereas PstS6 was prevalent in epidemics in East Africa. PstS7, PstS8 and PstS10 represented three genetic lineages prevalent in Europe. Races from other lineages were in low frequencies. Virulence to Yr9 and Yr27 was common in epidemics in Africa and Asia, while virulence to Yr17 and Yr32 were prevalent in Europe, corresponding to widely deployed resistance genes. The highest diversity was observed in South Asian populations, where frequent recombination has been reported, and no particular race was predominant in this area. The results are discussed in light of the role of invasions in shaping pathogen population across geographical regions. The results emphasized the lack of predictability of emergence of new races with high epidemic potential, which stresses the need for additional investments in population biology and surveillance activities of pathogens on global food crops, and assessments of disease vulnerability of host varieties prior to their deployment at larger scales.

Low pathotype diversity in a recombinant Puccinia striiformis population through convergent selection at the eastern Himalayan centre of diversity (Nepal)

“…Among the rare virulences, Vr3 , Vr4 , Vr25 and VrVic , though common in Europe (Hovmøller et al ., ; de Vallavieille‐Pope et al ., ), were present at a very low frequency only at two locations (Kathmandu and Dolakha); Vr17 and Vr32 were detected in only one isolate at Kathmandu and VrSd and VrSp were detected in only one isolate at Dolakha (Table ). The absence of virulence to Victo in more than 90% of the isolates and fixation of virulence to Suwon 92/Omar distinguished the Nepali Pst populations from other worldwide populations (Ali et al ., ).…”

“…In contrast, when the genotypic information for the clonal population of France was considered (Table ), 21 pathotypes were detected across more than a 25‐year period (based on hundreds of isolates), all of which represented a single North European clonal lineage, with no pathotype detected in more than one genetic group (Enjalbert et al ., ; de Vallavieille‐Pope et al ., ). However, the invasive strains such as 6E16‐type races and PstS2 races sampled in the south of France belonged to other genetic groups, all of which represented a particular genetic lineage (Walter et al ., ; Ali et al ., ).…”

“…The pathotypes found during 1985–1990 in Nepal had similar virulence spectra to those observed in 2008 with the virulences Vr1 , Vr2 , Vr6 , Vr7 , Vr8 and VrSu . The virulences Vr9 , Vr27 and VrA were acquired after the 1990s, which could be driven by the deployment of corresponding resistance genes in the region, as elaborated above (Karki et al ., ; Ali et al ., ). Comparison with the virulence structure during the same (2007–8) period (Sharma‐Poudyal et al ., ) confirmed both the fixation or high frequency of VrA , Vr2 , Vr6 and Vr7 , and the absence or low frequency of Vr5 , Vr15 , Vr24 , Vr32 and VrSp (Table ).…”

“…Wheat yellow/stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is an economically important wheat disease causing severe yield losses across the world (Chen, ; Hovmøller et al ., ; Hodson, ; Beddow et al ., ; Ali et al ., ). Worldwide analyses of the pathogen have revealed a clonal population structure in northwestern Europe, North and South America, Australia and the Mediterranean region (Chen et al ., ; Hovmøller et al ., ; Enjalbert et al ., ; Wellings, ; Bahri et al ., ), whereas a recombinant population structure was detected in the Himalayan and near‐Himalayan region, identifying this region as a centre of diversity (Ali et al ., ).…”

“…The recent worldwide epidemics have been reported to be caused by a few clonal lineages spread over large geographical regions in most of the clonal populations (Chen, ; Hovmøller et al ., ; Walter et al ., ; Ali et al ., ). In contrast, such a predominant prevalence of one or few pathotypes was absent in the recombinant populations in Pakistan and China (Mboup et al ., ; Ali et al ., , ). The Nepali Pst population has been shown to possess a high genetic diversity (Hovmøller et al ., ; Ali et al ., ) and recombination signature (Ali et al ., ).…”