Some of the most striking and extreme consequences of rapid, long-distance aerial dispersal involve pathogens of crop plants. Long-distance dispersal of fungal spores by the wind can spread plant diseases across and even between continents and reestablish diseases in areas where host plants are seasonally absent. For such epidemics to occur, hosts that are susceptible to the same pathogen genotypes must be grown over wide areas, as is the case with many modern crops. The strongly stochastic nature of long-distance dispersal causes founder effects in pathogen populations, such that the genotypes that cause epidemics in new territories or on cultivars with previously effective resistance genes may be atypical. Similar but less extreme population dynamics may arise from long-distance aerial dispersal of other organisms, including plants, viruses, and fungal pathogens of humans.

Wheat is grown worldwide in diverse geographical regions, environments, and production systems. Although many diseases and pests are known to reduce grain yield potential and quality, the three rusts and powdery mildew fungi have historically caused major crop losses and continue to remain economically important despite the widespread use of host resistance and fungicides. The evolution and fast spread of virulent and more aggressive race lineages of rust fungi have only worsened the situation. Fusarium head blight, leaf spotting diseases, and, more recently, wheat blast (in South America and Bangladesh) have become diseases of major importance in recent years largely because of intensive production systems, the expansion of conservation agriculture, undesirable crop rotations, or increased dependency on fungicides. High genetic diversity for race-specific and quantitative resistance is known for most diseases; their selection through phenotyping reinforced with molecular strategies offers great promise in achieving more durable resistance and enhancing global wheat productivity.

Race Ug99 (TTKSK) of Puccinia graminis f. sp. tritici, detected in Uganda in 1998, has been recognized as a serious threat to food security because it possesses combined virulence to a large number of resistance genes found in current widely grown wheat (Triticum aestivum) varieties and germplasm, leading to its potential for rapid spread and evolution. Since its initial detection, variants of the Ug99 lineage of stem rust have been discovered in Eastern and Southern African countries, Yemen, Iran, and Egypt. To date, eight races belonging to the Ug99 lineage are known. Increased pathogen monitoring activities have led to the identification of other races in Africa and Asia with additional virulence to commercially important resistance genes. This has led to localized but severe stem rust epidemics becoming common once again in East Africa due to the breakdown of race-specific resistance gene SrTmp, which was deployed recently in the ‘Digalu’ and ‘Robin’ varieties in Ethiopia and Kenya, respectively. Enhanced research in the last decade under the umbrella of the Borlaug Global Rust Initiative has identified various race-specific resistance genes that can be utilized, preferably in combinations, to develop resistant varieties. Research and development of improved wheat germplasm with complex adult plant resistance (APR) based on multiple slow-rusting genes has also progressed. Once only the Sr2 gene was known to confer slow rusting APR; now, four more genes—Sr55, Sr56, Sr57, and Sr58—have been characterized and additional quantitative trait loci identified. Cloning of some rust resistance genes opens new perspectives on rust control in the future through the development of multiple resistance gene cassettes. However, at present, disease-surveillance-based chemical control, large-scale deployment of new varieties with multiple race-specific genes or adequate levels of APR, and reducing the cultivation of susceptible varieties in rust hot-spot areas remains the best stem rust management strategy.

Stripe rust (yellow rust) of wheat, caused by Puccinia striiformis f. sp. tritici, has become more severe in eastern United States, Australia, and elsewhere since 2000. Recent research has shown that this coincided with a global spread of two closely related strains that were similar based on virulence phenotype and amplified fragment length polymorphism. The objective of this research was to quantify differences in aggressiveness among isolates representative of the pre-2000 and post-2000 populations. Representative isolates were evaluated at low (10 to 18°C) and high (12 to 28°C) temperature regimes for latent period, lesion length, lesion width, lesion area, and spore production on adult plants of a susceptible wheat cultivar with no known genes for resistance to stripe rust. “New” isolates (since 2000) were significantly more aggressive than “old” isolates (before 2000) for all variables. At the low temperature regime, new isolates sporulated 2.1 days (16%) sooner, grew 0.3 mm per day (18%) faster, produced 999 (140%) more spores per inoculation site per day, and produced 6.5 (71%) more spores per mm² of lesion per day compared with old isolates. At the high temperature regime, new isolates sporulated 3 days (26%) sooner, grew 0.2 mm per day (18%) and 2.2 mm² per day (88%) faster, grew 1.2 mm (50%) wider, produced 774 (370%) more spores per inoculation site per day, and produced 6.2 (159%) more spores per mm² of lesion per day than old isolates. New isolates showed significant adaptation to the warm temperature regime for all variables. Based on these results and previously published models for stripe rust epidemics, recent severe stripe rust epidemics were most likely enhanced by the pathogen's increased aggressiveness, especially at higher temperature. Furthermore, these results demonstrate that wheat rust fungi can adapt to warmer temperatures and cause severe disease in previously unfavorable environments.

Analyses of large-scale population structure of pathogens enable the identification of migration patterns, diversity reservoirs or longevity of populations, the understanding of current evolutionary trajectories and the anticipation of future ones. This is particularly important for long-distance migrating fungal pathogens such as Puccinia striiformis f.sp. tritici (PST), capable of rapid spread to new regions and crop varieties. Although a range of recent PST invasions at continental scales are well documented, the worldwide population structure and the center of origin of the pathogen were still unknown. In this study, we used multilocus microsatellite genotyping to infer worldwide population structure of PST and the origin of new invasions based on 409 isolates representative of distribution of the fungus on six continents. Bayesian and multivariate clustering methods partitioned the set of multilocus genotypes into six distinct genetic groups associated with their geographical origin. Analyses of linkage disequilibrium and genotypic diversity indicated a strong regional heterogeneity in levels of recombination, with clear signatures of recombination in the Himalayan (Nepal and Pakistan) and near-Himalayan regions (China) and a predominant clonal population structure in other regions. The higher genotypic diversity, recombinant population structure and high sexual reproduction ability in the Himalayan and neighboring regions suggests this area as the putative center of origin of PST. We used clustering methods and approximate Bayesian computation (ABC) to compare different competing scenarios describing ancestral relationship among ancestral populations and more recently founded populations. Our analyses confirmed the Middle East-East Africa as the most likely source of newly spreading, high-temperature-adapted strains; Europe as the source of South American, North American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. Although most geographic populations are not markedly affected by recent dispersal events, this study emphasizes the influence of human activities on recent long-distance spread of the pathogen. Domestication of ecosystems, climate change and expanding global trade have accelerated the pace of disease emergence, caused by their introduction into new areas with susceptible hosts or the spread of new damaging pathogen genotypes. The wheat yellow rust pathogen (PST) is a pathogen with recent reports of invasions, significantly affecting worldwide wheat production. However, its origin and ancient migration routes remained unclear and the source areas of newly spreading strains were largely unknown. This information is important to understand the trajectories of current invasions and forecast the future spread, and more generally develop risk-assessment models of pathogen emergence. We analyzed a set of worldwide representative isolates of PST, which enabled to identify six different area-specific populations. Using population genetics tools, we identified its centre of diversity in the Himalayan and near Himalayan region. We also identified the source of the recently emerged populations; Middle East-East Africa as the source of high-temperature-adapted strains spreading worldwide; Europe as the source of American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. We demonstrate the influence of human activities on the recent long-distance spread of the disease, though most geographic populations are not markedly affected by recent dispersal events.

Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from wild emmer wheat, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in wheat. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Ug8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). The presence of kinase-pseudokinase structure in both plant TKPs and the animal Janus kinases sheds light on the molecular evolution of immune responses across these two kingdoms.