M. Leconte

Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France

Puccinia striiformis f. sp. tritici (PST), a clonal basidiomycete causing yellow rust disease on wheat, has a long record of ‘overcoming’ cultivar resistance introduced by breeders. Despite the long dispersal capacity of its spores, the French population of PST presents a strong geographical structure, with the presence of a specific pathotype (array of avirulence genes) at high frequencies in the south of France. The genetic diversity underlying this differentiation was analysed by microsatellite and AFLP markers. A total of 213 French isolates belonging to 10 pathotypes collected over a 15‐year period were investigated. For each of the 12 microsatellites used, polymorphism resulted from a unique allelic variant associated to the south‐specific pathotype. This pathotype was characterized by 40 specific markers over the total of 63 polymorphims detected using 15 AFLP primer combinations. Phylogeographical analysis indicated a strictly clonal structure of the population, and a strong genomic divergence between the northern population and a south‐specific clone. Both virulence and molecular data show that the northern French population belongs to the northwestern European population, whereas the southern clone is most likely related to a Mediterranean population, the two subpopulations resulting from the ancient divergence of two clonal lineages. While the virulence complexity in the northern population may be explained by the successive introduction of corresponding resistance genes in cultivars, the maintenance of a simple virulence type in southern France, despite gene flow between the two populations, may be explained in terms of host cultivars repartition and local adaptation to specific host or climatic conditions.

Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici.

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.

Puccinia striiformis f.sp. tritici presents high diversity and recombination in the over-summering zone of Gansu, China

Puccinia striiformis f.sp. tritici (PST), a basidiomycota responsible for wheat yellow rust, has a strict clonal behavior and a low genetic diversity in European and Australian populations. On the other hand high diversity has been reported in Chinese populations. Moreover it is thought that in China yellow rust epidemics start recurrently from the western highlands where over-summering occurs. To compare PST genetic diversity in this area to the one described in France seven AFLP primer combinations were used to analyze a sample of 160 isolates collected in 2001 in five counties of Gansu Province. The AFLP data revealed 40 polymorphic bands, discriminating 139 AFLP genotypes. Linkage disequilibrium and phylogeographic analyses support the hypothesis of a reproductive mode that is not strictly clonal. In this regard Chinese isolates from Gansu strongly contrast with the European studies using the same markers. Genetic diversity of this 1 y sampling in Gansu is found to be seven times higher than the one observed in France over 20 y and exhibits lower linkage disequilibrium. The effective population size of the French sample was estimated to be 1000 times smaller than the Gansu population. These results support the hypothesis of large population size as well as the occurrence of genetic recombination, while the importance of Gansu as a main over-summering area requires assessment through larger scale studies.

Inferring the contribution of sexual reproduction, migration and off‐season survival to the temporal maintenance of microbial populations: a case study on the wheat fungal pathogen Puccinia striiformis f.sp. tritici

Understanding the mode of temporal maintenance of plant pathogens is an important domain of microbial ecology research. Due to the inconspicuous nature of microbes, their temporal maintenance cannot be studied directly through tracking individuals and their progeny. Here, we suggest a series of population genetic analyses on molecular marker variation in temporally spaced samples to infer about the relative contribution of sexual reproduction, off‐season survival and migration to the temporal maintenance of pathogen populations. We used the proposed approach to investigate the temporal maintenance of wheat yellow rust pathogen, Puccinia striiformis f.sp. tritici (PST), in the Himalayan region of Pakistan. Multilocus microsatellite genotyping of PST isolates revealed high genotypic diversity and recombinant population structure across all locations, confirming the existence of sexual reproduction in this region. The genotypes were assigned to four genetic groups, revealing a clear differentiation between zones with and without Berberis spp., the alternate host of PST, with an additional subdivision within the Berberis zone. The lack of any differentiation between samples across two sampling years, and the very infrequent resampling of multilocus genotypes over years at a given location was consistent with limited over‐year clonal survival, and a limited genetic drift. The off‐season oversummering population in the Berberis zone, likely to be maintained locally, served as a source of migrants contributing to the temporal maintenance in the non‐Berberis zone. Our study hence demonstrated the contribution of both sexual recombination and off‐season oversummering survival to the temporal maintenance of the pathogen. These new insights into the population biology of PST highlight the general usefulness of the analytical approach proposed.

Preinoculation Effects of Light Quantity on Infection Efficiency of Puccinia striiformis and P. triticina on Wheat Seedlings.

ABSTRACT In a previous study under controlled conditions, a model was developed to predict the infection efficiency for the wheat leaf and stripe rust fungi based on temperature and dew period during the 24 h after inoculation. The two pathogens differed in their maximum infection efficiency under controlled conditions for temperature and dew period, the infection efficiency was 12 times greater for Puccinia triticina than for P. striiformis. In the present study, the model was validated by field results to predict P. triticina infection efficiency as a function of temperature and dew period only. However, this model failed to predict infection efficiency caused by P. striiformis in the field. The model was adapted to include the effects of light quantity on infection efficiency. Wheat seedlings, grown in climate-controlled rooms and exposed to various regimes of light duration and intensity for 24 h in either field or controlled conditions, were inoculated and incubated in climate-controlled rooms under optimal dew and temperature conditions. Quantity of natural or artificial light (light intensity x duration) received by the plants prior to inoculation enhanced infection efficiency of wheat seedlings inoculated by P. striiformis. Infection efficiency increased from 0.4 to 36% depending on the light quantity according to a Richards function. For stripe rust, three environmental variables, preinoculation light quantity received by the plants, postinoculation temperature, and postinoculation dew period, were used for fitting a model for infection efficiency measured in the field.

Durable resistance to stripe rust is due to three specific resistance genes in French bread wheat cultivar Apache

Quantitative resistance is postulated to be more durable than qualitative (R-gene mediated) resistance, which is usually quickly overcome by the pathogen population. Despite its wide use for nearly 10xa0years in France, the French bread wheat cultivar Apache remains resistant to stripe rust. Here, we investigated the genetic architecture of cv. Apache resistance to examine whether its durability could be explained by quantitative characteristics. We identified quantitative trait loci (QTL) by composite interval mapping of disease progress data recorded throughout 4xa0years of field assays. These assays included inoculation with three different pathotypes on a segregating population originating from a cross between cv. Apache and cv. Taldor, a French cultivar susceptible to stripe rust. Three QTLs derived from Apache, QYr.inra-2AS, QYr.inra-2BL and QYr.inra-4B, were detected. Each of these QTLs contributed between approximately 15 and 69xa0% of the phenotypic variance and corresponds to a race-specific resistance gene. We showed that QYr.inra-2AS and QYr.inra-2BS map to the positions of Yr17 and Yr7, respectively, whereas QYr.inra-4B corresponds to an adult plant resistance gene. Our results demonstrate that a combination of two or more race-specific resistance genes can confer durable resistance provided that it is properly managed at a continental level. Race-specific resistance genes should not be removed from breeding programs provided that they are properly managed.

A high virulence and pathotype diversity of Puccinia striiformis f.sp. tritici at its centre of diversity, the Himalayan region of Pakistan

Information on the pathogen virulence profile and diversity across locations is crucial for host germplasm improvement and deployment. The rapid acquisition of virulence to host resistance by the wheat yellow/stripe rust pathogen (Puccinia striiformis f.sp. tritici: PST), makes it crucial to know about its virulence and pathotype diversity. Recent studies have shown the plausible centre of origin of the pathogen in the Himalayan region, with Pakistan being the most ancestral to all other worldwide populations. To assess the status of virulence and pathotype diversity in the Himalayan region of Pakistan, a set of 127 PST infected wheat samples from eight locations were collected, multiplied and pathotyped using a set of 36 differential lines from the world set, European and Chinese sets, and 9 Avocet Yr isolines. Virulence (Vr) was recorded to 18 out of 24 tested yellow rust resistance (Yr) genes, while a total of 53 pathotypes were detected out of 127 isolates tested. Virulence was found to the resistance genes rarely deployed in Pakistan (Vr8) or even worldwide level (Vr5), while virulence to Vilmorin 23 (Yr3+) was absent in Pakistan, which is common in Europe. None of the pathotypes was dominant across all locations, however, no clear spatial structuring was observed for the studied locations. Our results suggested a high virulence and pathotype diversity in line with the previously proposed potential role of sexual recombination in the temporal maintenance of PST in the Himalayan region of Pakistan. This information should be useful in host resistance gene improvement and deployment.