Abstract
Key message
Stem rust resistance was mainly based on a few, already known resistance genes; for yellow rust resistance there was a combination of designated genes and minor QTLs.
Abstract
Yellow rust (YR) caused by Puccinia striiformis f. sp. tritici (Pst) and stem rust (SR) caused by Puccinia graminis f. sp. tritici (Pgt) are among the most damaging wheat diseases. Although, yellow rust has occurred regularly in Europe since the advent of the Warrior race in 2011, damaging stem rust epidemics are still unusual. We analyzed the resistance of seven segregating populations at the adult growth stage with the parents being selected for YR and SR resistances across three to six environments (location–year combinations) following inoculation with defined Pst and Pgt races. In total, 600 progenies were phenotyped and 563 were genotyped with a 25k SNP array. For SR resistance, three major resistance genes (Sr24, Sr31, Sr38/Yr17) were detected in different combinations. Additional QTLs provided much smaller effects except for a gene on chromosome 4B that explained much of the genetic variance. For YR resistance, ten loci with highly varying percentages of explained genetic variance (pG, 6–99%) were mapped. Our results imply that introgression of new SR resistances will be necessary for breeding future rust resistant cultivars, whereas YR resistance can be achieved by genomic selection of many of the detected QTLs.
Avoid common mistakes on your manuscript.
Introduction
Yellow rust (YR) caused by Puccinia striiformis f. sp. tritici (Pst) and stem rust (SR) caused by Puccinia graminis f. sp. tritici (Pgt) are among the most damaging wheat diseases in Germany and on a global scale, respectively (Serfling et al. 2016). Their control is by fungicides and genetic resistances. No active fungicide ingredient is currently approved for control of SR in Germany. The availability of fungicides, especially the widely used azoles approved for control of YR, is more and more restricted by the European Union (Jess et al. 2014). Following the European guidelines for integrated pest management, chemical control is considered an inferior choice and preventive measures such as resistance should be preferred (DIRECTIVE 2009/128/EC). Consequently, resistance breeding must be intensified to maintain effective disease management for European wheat production.
Until 2011 Pst populations in Europe were mostly endemic with clonal propagation and slow adaptation; however, the situation changed with the appearence of the Warrior race (Hovmøller et al. 2016). Due to the broad virulence combination of this race, some formerly resistant varieties became susceptible. In contrast to the earlier European races, the Warrior race had a clear upwards shift in temperature optimum for infection and thus could become established under warmer conditions, exemplified by its occurrence in Italy and Spain (Miedaner and Juroszek 2021). These events created a strong motivation for breeding programs to shift to YR resistance based on adult-plant resistances reputed for durable protection. For SR, local stem rust outbreaks across Europe occurred in Central Germany in 2013 after more than 50 years (Olivera Firpo et al. 2017). This put breeding for stem rust resistance back in focus (Flath et al. 2014; Saunders et al. 2019). In 2016, there was a severe stem rust outbreak in durum and bread wheat in Sicily (Bhattacharya 2017) and in the following year stem rust occurred on late-maturing wheat and barley in Central Sweden (Berlin 2017). Saunders et al. (2019) predicted a re-occurrence of stem rust as common disease in Western Europe. Recently, even in Ireland with its maritime climate, stem rust was detected in experimental plots at several locations (Tsushima et al. 2022).
The irregular occurrence of Pgt compared to Pst is likely due to two factors: a higher optimal infection temperature for Pgt and the dominance of early-maturing winter wheat varieties, that shorten the window for Pgt infection coming from the alternate host (Berberis spp.), whereas the source of Pst is overwintering infection of cereals (Flath et al. 2018). However, this might fundamentally change due to predicted higher temperatures in future (Miedaner and Juroszek 2021). Flath et al. (2014) showed that only Sr31 remained effective against most isolates collected during the stem rust outbreak in Germany 2013. Sr31 was introduced into wheat from “Petkus” rye in the 1930s (Schlegel and Korzun 1997) and was one of the most frequently used resistance genes used worldwide (Pathan and Park 2007; Olivera Firpo et al. 2017). In 1999, Sr31 became ineffective due to a new race first identified in Uganda. The race called Ug99 (or TTKSK) was virulent for Sr31 and to some other widely used Sr genes (Singh et al. 2015). It or its descendants subsequently spread to all countries in eastern Africa and were also found in Yemen, Iran, and in 2023, Nepal (Patpour et al. 2024). Sr31 remains effective in Central Europe (Flath et al. 2018; Zelba et al. 2022). Additionally, stem rust resistance of cultivars with Sr38 ranged from fully resistant to moderately susceptible, while Sr24 was fully effective in field experiments with German winter wheat cultivars (Flath et al. 2018).
Rust resistance is often inherited by monogenic, race specific all-stage resistance (ASR; synonym seedling resistance) that usually proves to have low durability (McIntosh et al. 1995; Chen 2005). Alternatively, resistance is expressed only at the post-seedling or adult plant stages (APR). APR is often conferred quantitatively by multiple genes or QTL conferring only partial resistance (Ellis et al. 2014; Miedaner 2016). More than 300 regions in the wheat genome have been associated with YR resistance (Bouvet et al. 2022a). Kumar et al. (2023) condensed 505 YR QTLs from 101 linkage-based interval mapping studies to 67 meta-QTLs (MQTLs) and further refined them to 29 high-confidence MQTLs. This result was confirmed by Pal et al. (2022) who claimed 368 QTLs for leaf rust resistance, 291 QTLs for SR resistance, and 487 QTLs for YR resistance from 152 studies. Among the QTL plethora 28 MQTLs provided resistance to all three rusts, each of the other 43 MQTLs provided resistance to combinations of two rusts. Similar results were recently reported by Tong et al. (2024).
More than 80 resistance genes for YR and 56 genes for SR have been permanently assigned (McIntosh et al. 2013, 2014, 2020) and several more, temporarily named. The majority of those genes confer race-specific ASR and have, or had, limited durability (McDonald and Linde 2002). Pyramiding major R-genes with partial APR has increased the durability of ASR-genes, whereas combinations of only ASR genes were questioned in regard to durability (Mundt 2018). A recent survey of SR resistance found three ASR genes in German and Czech winter wheat panels, namely Sr24, Sr31, and Sr38/Yr17/Lr37 (Flath et al. 2018; Zelba et al. 2022). Some cultivars without ASR genes still showed substantial resistance in the field suggesting the presence of quantitatively inherited APR in German breeding material.
The objectives of this study were to: (1) identify already known and unknown APR genes/QTL for yellow rust and stem rust resistance in the available mapping populations of European elite winter wheat, and (2) to investigate whether there are genes that confer resistance to both YR and SR. Seven mapping populations with a total of 600 progenies were phenotyped across several environments artificially inoculated with Pst and Pgt.
Materials and methods
Plant material and pathogen isolates
Trials were conducted in cooperation with the Institute of Plant Protection in Field Crops and Grassland, Julius Kühn-Institut (JKI) in Kleinmachnow, LIMAGRAIN GmbH, Strube Research GmbH and Co. KG and Secobra Saatzucht GmbH. Mapping populations were constructed and provided by the three breeding companies (Table 1).
Mapping populations
This study was conducted mainly for mapping of SR and YR resistance genes in commercially grown German elite winter wheat material. Parents were chosen after conducting association studies on two German winter wheat diversity panels. The first panel consisting of 79 varieties was screened for stem rust resistance at the seedling and adult plant stages (Flath et al. 2018). The second panel of 270 varieties was screened for yellow rust and stem rust resistance at the adult-plant stage (Miedaner et al. 2020). Seven populations (Pop1–Pop7) were developed from biparental crosses. Their parents had different seedling responses to SR and/or YR (Table 2). In total, there were 11 parents including two unreleased lines and nine registered varieties; some populations shared one parent (Table 1). Doubled-haploid (DH) lines were produced from F1 plants. Population 1 (Pop1) was a recombinant inbred line (RIL) population derived from the F4 individuals. Pop2 to Pop4 had same susceptible parent (Mocca). Pop5 to Pop7 were tested only in the second year. Each population had 68–97 genotypes (entries) tested in field trials with 72–97 entries per population genotyped. However, based on marker data some genotypes from the respective populations appeared to be identical (correlation based on marker data ≥ 0.99) and each group of identical genotypes was considered as one genotype. The high number of identical genotypes was probably caused by the DH production procedure. During regeneration, calli induced from anthers (microspores) can break into multiple pieces that give rise to genetically identical genotypes. Parents were always tested together with their respective progeny.
Experimental design
The materials were tested in multi-environment trials (MET) at five locations, namely Berlin-Dahlem in Eastern Germany (DAL, 52.44° N, 13.27° E, 45 m above sea level [a.s.l.]), Stuttgart-Hohenheim in Southern Germany (HOH, 48.80° N, 9.20° E; 401 m a.s.l.), Lemgo in Western Germany (LEM, 52.2° N, 8.55° E, 100 m a.s.l.), Rosenthal-Peine (ROS, 52.18° N, 10.10° E; 73 m a.s.l.) and Söllingen in Northern Germany (SOL, 52.06° N, 10.55° E, 90 m a.s.l.) in two seasons, namely 2020 and 2021. Because the segregating populations were breeding material and proprietary to the respective breeding companies, the complete set of genotypes was only grown at locations managed by the University of Hohenheim (HOH) and the Julius-Kühn Institute (DAL). Only material of the respective proprietary populations was grown at breeding stations LEM, ROS, and SOL (Table S1). The material of each breeding company (Limagrain, Secobra, Strube) was randomized in separate trials using a resolvable incomplete block design with two complete replicates. Only Pop2 to Pop4 were tested at locations HOH and ROS in 2020 using a single complete replicate across locations (p-rep design) due to shortage of seed. Each entry was grown in two-row plots of 1–1.2 m length and 0.4 m width and sown with 40–60 kernels per row. In DAL, the materials were grown in four-row 0.5-m plots.
Pathogen isolates and seedling tests
Segregating populations were inoculated with specific races that distinguished the respective parental lines based on a previous seedling test conducted by Institute of Plant Protection in Field Crops and Grassland, Julius Kühn-Institut (JKI) in Kleinmachnow (Tables 2 and S2). Not all pairs of parents showed a significant difference in a specific seedling test. Pst and Pgt inoculum for all populations and environments was produced by JKI as described in Hovmøller et al. (2017) and Olivera et al. (2015). The Pgt isolates used were identified as races TKTTF and HFCLB (nomenclature according to Roelfs and Martens 1988, actualized by FAO 2024) and the Pst isolates were identified as the Warrior (PstS7) and Warrior (–) Benchmark (PstS10) races (Table S2) (nomenclature according to GRRC 2023a; Hovmøller et al. 2022).
Seedling tests were performed as previously described by Jin et al. (2007), Olivera et al. (2015), and Hovmøller et al. (2017). In short, fully expanded primary and secondary leaves of six to ten seedlings per line were inoculated 10 days after planting. All assessments were repeated in separate experiments. Seedling infection types were determined 18 days after inoculation for Pst following a 0–9 scale (Hovmøller et al. 2017): 0 = no visible disease symptoms (immune), 1 = minor chlorotic and necrotic flecks, 2 = chlorotic and necrotic flecks without sporulation, 3–4 = chlorotic and necrotic areas with limited sporulation, 5–6 = chlorotic and necrotic areas with moderate sporulation, 7 = abundant sporulation with moderate chlorosis, 8–9 = abundant and dense sporulation without notable chlorosis and necrosis. Infection types 7 to 9 were categorized as susceptible, 4 to 6 as moderately resistant, and 0 to 3 as resistant. For Pgt a 1–6 scale was used: 1 = no visible disease symptoms (immune), 2 = hypersensitive flecks, 3 = small uredinia with hypersensitive reactions, 4 = small to medium-sized uredinia surrounded by chlorosis, 5 = medium-sized uredinia with/without chlorosis, 6 = large uredinia without chlorosis. Infection types 5 to 6 were categorized as susceptible, 3 to 4 as moderately resistant, and 1 to 2 as resistant.
Inoculation and data collection
Field trials were artificially inoculated twice with Pst at two-week intervals at early tillering (plant stage BBCH 21–23). Pgt was also inoculated twice at the end of heading and mid-flowering (BBCH 59–65). Urediniospores (100 mg per 100 m2) of Pst and Pgt spores were suspended in a 0.1% agar and applied by a microsprayer (Micron Ulva, Bromyard, Herefordshire, UK) across the entire plot area.
Rust response data were collected by visual scoring at several scoring dates to ensure at least one optimum date with maximum trait differentiation. Scoring was as the percentage area of infection per plot; leaf area for YR, and for SR, the area second uppermost leaf (Flag-1) and the node. Scoring of YR started when most genotypes showed mild symptoms. SR was scored at BBCH 87–89, when uredinia and telia were well developed. The number of scoring dates varied between trials and ranged from one to four for YR and from one to three for SR. Disease development differed between environments. In some environments SR reactions were not recorded due to low infection (Table S1).
Phenotypic data analyses
Phenotypic analysis was conducted in a two-stage approach. The statistical models were computed using asreml-R ver. 4.1.0.160 (Butler 2021).
First stage
Best linear unbiased estimators (BLUEs) with standard errors (SEs) were calculated for each trait assessed in the tth environment l based on the following mixed model:
The plot value is modeled by the general intercept μ, the ith genotype g, the kth replicate r, the lth block b and the residual error e. To estimate BLUEs, g was modeled as fixed effect and all other effects as random. To assess repeatability (location-wise entry-mean heritability) by \(Rep=\frac{{\sigma }_{G}^{2}}{{\sigma }_{G}^{2}+\frac{\overline{v}}{2} }\) the mean variance of a difference \(\overline{v }\) was calculated and in a separate model the genotype was fitted as random to estimate genetic variance \({\sigma }_{G}^{2}\) (Piepho and Möhring 2007). In case of SR and YR, the same model was run for each assessment, but in the final analysis only the mean (or in single cases only one assessment) of all assessments with BLUEs > 15% and Rep > 0.4 were used. Special attention was paid on the analysis of percentage data. Model fits often resulted in non-normally distributed genotype means (right skewed), increasing residual variance with increasing scores and negative BLUEs and thus it was decided to use a generalized mixed linear model (GLMM). We chose a logit link-function with binomial variance. Ideally not only the link function but also the variance function can be specified in the model calculation function, but to the best of our knowledge it was not possible to fit with ASReml-R 4.1.0.160 (Butler 2021). However, by default the asreml function with the argument “family = list(asr_binomial(link = “logit”, dispersion = NA))” calculates overdispersion and directly corrects for it. Except this additional argument in the function call, data were modeled likewise to a mixed model with normal link function. Outliers were detected by using method 2 (Bonferroni-Holm using studentized residuals) described in Bernal-Vasquez et al. (2016), where for the GLMM the deviance residuals were used.
Second stage
BLUEs \({g}_{tij}\) with standard errors from the first stage were used to calculate BLUEs \({g}_{i}\) across environments by
with effects for the tth environment l, the genotype-environment interaction \({gl}_{it}\) and the residual error e. To account for the errors from the first stage the reciprocal of the squared standard error of the BLUES was used as weights (method 2, Möhring and Piepho 2009). Consequently, the error variance of the residual was restricted to 1. To estimate variances, all effects were fitted as random. To estimate BLUEs and \(\overline{v }\) for heritability calculation (H2 = Rep), the genotype was fitted as fixed effect.
Despite the advantages of the GLMM analysis, BLUEs for SR and YR were also back-transformed on a percentage scale to better compare them with a previous study (Miedaner et al. 2020). Thus, values on percentage scale refer to back-transformed values, all statistics like mapping or correlations were based on the logit scale because error estimates cannot easily be back-transformed.
Marker analysis
All material was genotyped by TraitGenetics (SGS Institut Fresenius GmbH, TraitGenetics Section, Seeland OT Gatersleben, Germany) using a 25 K Infinium iSelect arraySNP chip. Marker data from the biparental populations were filtered for minor allele frequency (maf) > 0.2, call rate (CR) > 0.95 and for heterozygosity < 0.05 in case of the DH populations (Pop2–Pop7). Based on marker data several genotypes appeared to be identical (correlation > 0.99) and each group of identical genotypes was considered a single genotype and this already for phenotypic data analysis. Additionally, 4, 2, 4, 2 and 4 genotypes were dropped due to average marker heterozygosity > 0.1 in the DH populations Pop2, Pop4, Pop5, Pop7 and Pop8, respectively. Heterozygosity was attributed to spontaneous cross pollination during seed multiplication. After filtering, marker data from the biparental populations were converted into ABH and numeric format (A = − 1 = allele from parent 1, B = 1 = allele from parent 2, H = 0 = heterozygous).
Validation of the presence of major SR resistance genes postulated in the study (Sr24, Sr31, Sr38) and absence of Yr5, Yr10 and Yr15 was done by PCR marker tests that detect the alien chromatin where the first three genes come from. Markers used were Sr24#12 (Sr24), Xbarc71 (Sr24), iag95 (Sr31) and Ventriup-LN2 (Sr38) for SR and Yr5_ins (Yr5), ES1100 (Yr10) and barc8 (Yr15) for YR, respectively. Conditions for PCR and marker sequences for iag95 were obtained from (https://maswheat.ucdavis.edu/) www.maswheat.ucdavis.edu as well as, from the GrainGenes database (https://wheat.pw.usda.gov). Differential lines harboring the respective resistance genes were used as positive controls, whereas Avocet S and Cartago served as negative controls.
QTL mapping
Linkage mapping was based on regressing each marker on the BLUEs estimated in the second stage:
where \(\alpha\) denotes the regression coefficient of marker x coded for the allele of parent 1 (-1), the heterozygote (0) and parent 2 (1). The genetic variance was structured based on a kinship matrix K calculated from all markers by \(K=Z{Z}{\prime}/2\sum {p}_{j}(1-{p}_{j})\), where Z is a n × m matrix with n genotypes and m markers scaled for the allele frequency \({z}_{ij}={x}_{ij}-2{p}_{j}\) and \({x}_{ij}\) the allele for genotype i and marker j of marker matrix M (VanRaden 2008). Like the second stage phenotypic model, the reciprocals of the squared standard errors of the BLUEs were used as weights in the regression model. After a first mapping run, single significant markers were fitted as fixed cofactors, but only if the distance was not smaller than 20 cM. Pairwise recombination R between markers m × m was estimated. For DH populations this was calculated by
For each single marker fit, P-values were extracted from Wald-test statistics and to adjust for multiple testing the global significance threshold was calculated using the simpleM method (Gao et al. 2008), but instead of splitting the marker matrix into several chromosomes, singular value decomposition was applied for the whole marker matrix at once. The package RSpectra was used for computation (Qiu and Mei 2019). The explained genetic variance (pG) was calculated by the difference of estimated genetic variances of model 3 and model 2, divided by the genetic variance estimated by model 2.
Results
Phenotypic data
Both SR and YR data showed a pronounced right skew in the scoring data in all environments (Fig. S1). Thus, trait differentiation was small leading to low mean infection levels at the individual locations (Tables S3 and S4). Logit transformation was used throughout. In all cases the last scoring date showed the highest trait differentiation and hence also the highest estimated repeatability.
Genotypic variances were in all cases, except Pop6 SR resistance, larger than genotype-environment interaction variance (Tables S5 and S6). In the latter population both parents were moderately susceptible. Overall, the highest genetic variance was observed in Pop2 for SR and in Pop5 and Pop7 for YR. Entry-mean heritabilities ranged between 0.37 (Pop6) and 0.84 (Pop1) for SR and 0.58 (Pop6) and 0.90 (Pop1) for YR.
After logit transformation, histograms displayed normal distributions (Fig. 1). Four of seven populations had a significant trait correlation between SR and YR, namely Pop1, Pop2, Pop3, and Pop7 (Fig. 1), although the correlation was negative in Pop1.
Genotypic data and QTL mapping
For SR, across all populations except Pop6 one to three major Sr genes were detected (Table 3, Fig. 2), namely Sr24 on chromosome 3D (Pop2, Pop4, Pop5), Sr31 on chromosome 1B (Pop1, Pop5), and Sr38/Yr17 on chromosome 2A (Pop2, Pop3, Pop5, Pop7) either alone or in different combinations. Additionally, in Pop4 there was a major gene on chromosome 4B. One to two QTLs were additionally detected in Pop1, Pop2, and Pop4. They made only small contribution to SR response. All genes/QTLs together explained up to > 90% of the genetic variance summing in all populations. No QTL for SR response was found in Pop6. The postulated SR resistance genes were supported by additional PCR marker tests except forSr38/Yr17 in Pop6 (Table 5) where the respective SR gene was not detected by linkage mapping.
For YR, two (Pop1) to four (Pop5) QTLs per population were identified across environments, with explained genetic variances ranging from about 1 to 99% indicating that both major QTLs/genes and minor QTLs were involved (Table 4, Fig. 3). In five populations, markers probably linked with Sr38/Yr17 were detected on chromosome 2A. Their contribution to genotypic variance ranged from 13 to 99% depending on the number of QTLs detected in the same population (Table 4). Of the other QTLs, those on chromosome 3A (Pop1), 6A (Pop2, Pop5) and 2D (Pop5, Pop6, Pop7), made major contributions to genotypic variance in some populations. Additionally, there were eight minor QTLs for YR response. Markers linked with the known and (in Europe) still effective resistance genes Yr5, Yr10, and Yr15 were not detected in any marker analysis.
Effects of individual and combined genes/QTL
Sr31 and Sr24 had large effects on SR response in both populations where they showed no overlapping 50% quantiles between plants with the resistant and the susceptible allele (Fig. 4). This was also the case for Sr38/Yr17 in three populations (Pop2, Pop3, Pop7), but not in the remaining two (Pop4, Pop5). For YR, the multiple resistance alleles in each population except for Pop 7 were near-additive. Where two genes/QTL had large effects the disease responses approached zero (Fig. 5). In four populations two resistance-associated markers were enough to reduce YR severity to zero.
The Sr38/Yr17 locus resulting in partial resistance to both YR and SR had very different effects depending on the cross (Fig. 6). In Pop3 and Pop7, the effect was large for both diseases, whereas in Pop4 the effect was only large for YR and in Pop2 only for SR. No significant effect for YR response was detected in Pop5.
Discussion
Methodological aspects
Multiple YR epidemics in Central Europe from 2014 to 2016, caused by the emergence of the Pst Warrior race, led to numerous mapping studies (e.g., Beukert et al. 2020; Shahinnia et al. 2022; Bouvet et al. 2022b; Lin et al. 2023). However, this is the first study to examine the inheritance of both SR and YR resistances in segregating populations. The populations provided by three plant breeding companies represent current breeding material. In contrast to other studies, we used artificial inoculation by individual Pst and Pgt races selected from the current race composition in Central Europe (GRRC 2023a,b). Although the disease responses were evaluated at the adult-plant stage, we also tested the parental lines at the seedling stage (Table 2). Thus, in the field each population was inoculated with the isolate showing the most differentiation based on the seedling test. For Pop1, we used race HFCLB in 2020 and race TKTTF in 2021; both races showed similar responses with Axioma being susceptible and Memory being resistant (Table 2). Especially for yellow rust natural infection with other races was possible but we believe this had little effect.
In general, population sizes were small, but in this study we expected mainly major resistance genes. With small population size the resolution of QTL mapping is limited and large linkage blocks lead to a high number of redundant markers and limited precision of estimated QTL positions (Xu 2003; Beavis 1998). A small population size also limits the detection of a major gene when other major genes are available in the same germplasm. Nonetheless, in contrast to genome-wide association studies (GWAS), biparental QTL studies have a higher QTL detection power even at lower marker densities due to balanced allele frequencies. In addition, common markers for the alien chromatin from which the SR resistances are derived were used to verify the resistances across parents (Table 3 and 4). Throughout this study, major QTLs are defined to have explained genetic variance pG > 25%.
Marker-based studies cannot prove the identity of a linked marker with a known resistance gene, at least until the resistance gene is cloned. Only the physical location of the two loci can be compared and this is what is done below. The new ‘Genome Atlas’ for rust resistance loci (Tong et al. 2024) does not help in this respect, but for the first time, physical positions are given for 920 leaf rust, yellow rust, and stem rust resistance genes/QTLs allowing a better comparison among studies. Concerning older QTL publications it should be noted that their precision is about 10 Mbp (Tong et al. 2024). Another problem in this respect could be that the linked marker(s) might not remain in the same LD block with the causal gene across generations due to recombination, thus comparison among studies also gets difficult (Tong et al. 2024). We could circumvent this problem in some cases by addressing SR genes from alien introgression events where PCR-based markers are available for the detection of the introgressed segment (Table 5).
All-stage versus adult-plant resistance in the parents
For the release of cultivars in Central Europe only adult-plant data are recorded. Seedling tests are an important tool for breeders to accelerate selection of resistance if they desire, but more important to dissociate all stage resistance from adult plant resistance with its reputed higher durability. We selected the parents in this study based on seedling tests especially those resistant to both YR and SR (Memory, Stamm 1, Stamm 2, LG Character, Spontan) or only to YR (Axioma, Bonanza, KWS Montana). Our adult-plant stage results largely paralleled the seedling results, with only Spontan proving to be moderately susceptible to SR and KWS Montana more resistant to SR than predicted from seedling tests.
In a previous study, no Sr gene was postulated for Memory because it was resistant to all isolates from a worldwide collection including the highly virulent races TTKSK, TRTTF, TKTTF, TTTTF (Flath et al. 2018). Hence, Memory was included in the present study twice. Its pedigree is complex and resistant parents like Kronjuwel and Amigo, but also Piko, Atlantis, and Cardos are included (Kempf, pers. commun.). Amigo is a 1AL/1RS translocation with Sr1RSAmigo, Pm17 and, in some plants, Lr24 (McIntosh et al. 1995). However, wheat cultivars Kronjuwel and Atlantis have the 1BL/1RS translocation (http://wheatpedigree.net/) and Kronjuwel is reported to have Sr31 (Porceddu et al. 1988). As we identified a QTL for SR resistance on chromosomes 1A and 1B in Pop1, we cannot decide whether Sr1RSAmigo or Sr31 is present in Memory because the marker iag95 identifies rye chromatin. However, the 1B QTL explained a much higher proportion of explained genotypic variance than the 1A QTL (79% vs. 12%, Table 3). According to our results, Memory contains all three Sr genes (Sr38, Sr31 or Sr1RSAmigo, and Sr24) as shown from Pop5 and supported by our PCR marker analysis, and additionally four QTLs explaining 11 to 52% of genotypic variation. This and the occurrence of the additional QTLs explain why no Sr gene could be postulated for Memory in the earlier study by Flath et al. (2018). In Pop1, Sr38 was not detected in Memory by mapping, because the other parent Axioma carried the same gene (Table 5). In the field test, Memory showed only 1.0% and 1.4% SR severity, respectively, whereas the most susceptible cultivar, Gedser, had 37% severity. An example of an adult-plant SR resistance source might be the parent KWS Montana, which was susceptible (IT 5) at the seedling stage, but displayed only 5% severity in the field.
For YR, all parents except Mocca and Edward were resistant or moderately resistant at seedling and adult-plant stages (Table 2). Gedser was seedling-susceptible, but moderately resistant in the field. Compared to field trials, Memory was resistant in Pop5, but rather susceptible in Pop1 (Table 2). The latter might be caused by the extremely high infection pressure at the LEM location in both years (Table S4).
Three major SR genes present in the tested breeding material
Across all populations, there were three major QTL on chromosomes 2A, 1B and 3D for SR resistance. The physical positions reported for these three genes corresponded to alien chromosome segments bearing Sr38/Yr17/Lr37 (chromosome 2A), Sr31 (chromosome 1B), and Sr24 (chromosome 3D). We also verified the respective alien segments in the parental lines (Table 5). It was already known that these three genes are present in different combinations in German and Czech winter wheat varieties (Flath et al. 2018; Zelba et al. 2022). Six SR resistance QTLs that were not overlapping between populations were also found.
Sr24 derived from Thinopyron ponticum was located on chromosome 3D (McIntosh et al. 1977). Walkowiak et al. (2020) reported the Th. ponticum introgression segment on the long arm of 3D to have a size of approximately 60 Mbp. Mago et al. (2005a) developed several markers for mapping of Sr24. Using primer sequence Sr24#12 showed the presence of this gene in Memory, LG Stamm 1, and LG Stamm 2 (Table 5). Sr24 was frequently used in Australian, South and North American and South African breeding material (Jin et al. 2008). The presence of Sr24 in European breeding material is due to selection of leaf rust resistance gene Lr24 (Flath et al. 2018).
Sr31 and/or Sr1RSAmigo was present in two populations (Pop1, Pop5) with the same, most significant marker located at 9.56 Mbp on the physical map and verified by PCR-based marker Iag95-STS (Mago et al. 2002). Both genes were derived from wheat-rye translocations including additional resistance genes against leaf rust (Lr26), yellow rust (Yr9) and powdery mildew (Pm8) (Mago et al. 2005b; Ren et al. 2009). Due to the extensive use of the yield-enhancing wheat-rye translocation in European wheat, Sr31 is frequently present in wheat varieties by chance. Sr31 was effective against all isolates collected during the local stem rust epidemic in 2013 in Central Germany, where in total six different races (TKTTF, TKKTF, TKPTF, TKKTP, PKPTF, MMMTF) were detected from only 17 samples that also differed in molecular markers (Olivera Firpo et al. 2017).
Interestingly, we detected a fourth prominent QTL for stem-rust resistance on chromosome 4B in the Mocca × LG Stamm 2 population with a physical position at 665.5 Mbp and of high explained genetic variance, however, the P-value was rather high (Table 3). The metaQTL study by Pal et al. (2022) found two MQTLs for stem rust resistance in the same region (4B.3 at 671.7–677.9 Mbp and 4B.6 at 660.7–663.1 Mbp) that were based on four and two QTLs, respectively. This QTL should get more attention by further fine-mapping and validation in different genomic backgrounds. In future, it should be determined if this QTL is Sr8.
Major resistance cluster Sr38/Yr17 provides resistance to stem rust and yellow rust
The major QTL on chromosome 2A found in Pop2, Pop3, Pop5, Pop7 for both SR and YR resistances and additionally in Pop4 for YR resistance corresponds to the rust resistance gene cluster Sr38/Yr17/Lr37 introgressed from Aegilops ventricosa chromosome arm 2NS (Seah et al. 2001; Helguera et al. 2003).
For Pop2, Pop3, and Pop4 we used a Pgt isolate that was avirulent for Sr38 (WSR-55/13-8, Table S2), however, the isolate inoculated on Pop5, Pop6, and Pop7 was virulent for this gene and we still detected Sr38 in Pop5 and Pop7. The resistant parents inoculated with this isolate reacted in seedling stage either resistant (Memory), moderately resistant (Spontan) or even susceptible (KWS Montana) to this race. We could not detect this gene in Spontan (Pop6) where no SR resistance QTL was detected, probably due to low disease development. In Pop1 we could not detect this gene by QTL mapping because both parents carry it as shown by the PCR-based markers (Table 5).
The fact that Sr38 still shows SR resistance at the adult plant stage in field trials, even though the inoculated SR races were virulent for this gene, has been described several times. In the study of Zhang et al. (2014), Sr38 was the most effective gene in the field test in the USA. Nine cultivars with Sr38 displayed strong resistance (0.55–3.42% SR severity) although a high virulence frequency for this gene was found in the inoculated Pgt population. In Europe, Flath et al. (2018) found that varieties with Sr38 in the field had a SR severity of 0.6–16%, while the most susceptible variety had a value of 41.5%. Similarly, Zelba et al. (2022) reported that varieties with only Sr38 had a field resistance of 3.2 on a scale of 1–9, although most pathotypes were virulent for it, while varieties without any Sr gene had 7.1. Obviously, a residual resistance for this gene is still effective in the adult-plant stage in terms of reduced infection as it has also been found for the SR resistance genes Sr6, Sr8 and Sr9a (Brodny et al. 1986).
The yellow rust resistance gene Yr17 is known to be overcome by several races of Pst in the adult-plant stage, at least by conducting seedling tests (Bayles et al. 2000). Pop2, Pop3, Pop4, and Pop7 showing this gene were inoculated with isolates of the original Warrior race (PstS7) and the Warrior (–) race (PstS10) ‘Benchmark’, which were assessed as virulent to Yr17 (Table S4). Although Yr17 was described as all-stage resistance the decision to assess a Pst isolate as avirulent or virulent can be arbitrary based on the differential line, test environment and assessor and more recent publications by Liu et al. (2020) and Li et al. (2023) showing a second gene for APR in lines with the 2NS-2A translocation. The question then is whether the adult plant resistance phenotype is due to residual effects of Yr17 or to the second gene. All populations had mean YR response levels ranging from 0.6 to 10.5% (Table S4). Milus et al. (2015) observed that some genotypes with Yr17 were susceptible to Pst at the seedling stage but reached medium to highly resistant infection types during adult-plant stage. They also observed that only partially virulent isolates during seedling stage were not able to cause disease on adult plants in the field, but this was prior to current evidence that lines with the translocation had an additional resistance gene. This gives a further explanation why lines with the 2A-2NS translocation still contributed a significant resistance effect during adult plant stage and hence was mapped in this study. Such residual resistance was described for several defeated YR resistance genes including Yr17 (Singh et al. 2022). In summary, Sr38/Yr17 was present in all resistant parents investigated in our study (Table 5).
Phenotypically, we found positive significant correlations between YR and SR resistances in Pop2, Pop3 and Pop7 (Fig. 1). No significant phenotypic correlation was found in Pop4 and Pop5 where the Sr38/Yr17 markers had been detected. However, correlation was likely masked by Sr24 or other YR resistance QTLs, especially in Pop5 where the genetic variance explained by Yr17 was 13%.
Known genes for YR resistance
Five different major YR QTLs were mapped on chromosomes 2A, 3A, 6A, 3B, and 2D. Additionally, seven population-specific, minor effect QTLs for YR were detected across six chromosomes. The genes with major effects described here might already be mapped in other wheat populations given the high number of reported QTLs for this pathosystem (Pal et al. 2022; Kumar et al. 2023; Tong et al. 2024). The major genes Yr10 and Yr15 on chromosome arm 1BS that are widely distributed in some parts of the world (e.g., Kazakhstan, Kokhmetova et al. 2021) were not detected in this study. The same was true for Yr5. Although we found a QTL on chromosome 2B in Pop 2, its physical position of 158.6 Mbp was quite distal to the position of Yr5 (110.2–110.9 Mbp, Kumar et al. 2023).
A QTL for YR resistance was detected on chromosome arm 6AL in Pop2 and Pop5 with an explained genetic variance of 61% and 47%, respectively. This coincides well with a minor QTL associated with marker wsnp_Ex_rep_c101766_87073440on 6A reported by Bouvet et al. (2022b). This marker was also present on the 25 k chip used in this study but monomorphic in the populations segregating for the 6A-QTL. A QTL at approximately the same position was mapped by Cheng et al. (2022). Wang et al. (2021) placed the same locus at 609.38 Mbp and found a second QTL for seedling response at 595.67 Mbp in Chinese landraces. Both studies classified the QTL to be new and effective during all growth stages (ASR). Miedaner et al. (2020), Beukert et al (2020), Rollar et al. (2021), Shahinnia et al. (2022), Kale et al. (2022), and Lin et al. (2023) detected resistance QTLs at a similar position. All mapping studies placed this 6A QTL in a small interval ranging from 598 to 612 Mbp, encompassing the position of our most closely linked marker at 610.35 Mbp. Lin et al. (2023) found the same linked marker (GENE 4021_496 at 610 Mbp) and identified 18 annotated disease resistance genes in a ± 1 Mbp interval around this marker. However, none of the genes cloned in this segment code for a NLR motif (Hafeez et al. 2021). In summary, the 6AL QTL is an environmentally highly stable YR resistance gene that is frequent in modern wheat breeding materials (Lin et al. 2023) comprising a good field resistance. It is yet not clear whether one or more genes are responsible and whether it is a ASR or APR locus. In future, it would be worthwhile to clone this gene from one source and use the sequence for analyzing the other populations.
A major QTL on chromosome 3A was mapped at 13 Mbp in Pop1. Bouvet et al. (2022b) reported a major QTL for YR on chromosome arm 3AS in a MAGIC mapping population that captured > 80% of the genetic variation in UK wheat. The physical position of the peak SNP marker in our study was about 0.77 Mbp distant from the position (Kukri_c28650_111, 7.921 Mbp) mapped by Bouvet et al. (2022b). This marker was on the 25 k chip used for genotyping in this study but was monomorphic in Pop1.
The major QTL on chromosome 3B was mapped at 741.3 Mbp in Pop6. The minor QTL on the same chromosome in Pop1 is unlikely to be the same. Wang et al. (2021) found a QTL for APR between 739.04 and 743.51 Mbp on chromosome 3B, as well as an ASR-associated QTL at 772.47 Mbp. Further research e.g., using fine-mapping approaches with increased population sizes, is needed to determine if the major QTL of our study coincides with already known APR resistance gene Yr80.
Another QTL for YR was mapped on the long arm of chromosome 2D at 636.60 Mbp in Pop6 and Pop7. In Pop5 the same marker made only a minor contribution to YR resistance. Bouvet et al. (2022b) found a YR QTL at 638.38 Mbp on chromosome 2D (Ra_c21099_1781). Yr54 is known to be distally located on chromosome 2D (Basnet et al. 2014) and may coincide with a major YR QTL found by Jagger et al. (2011) in the German variety Alcedo, although they have no known ancestral relationship (Basnet et al. 2014). Marker Xgwm301 0.5 cM from APR gene Yr54 apart that Basnet et al. (2014) located at ~ 648.88 Mbp falls into the interval of significant markers in the present study. In Basnet et al. (2014) Yr54 explained 49–54% of the phenotypic variation. Another resistance gene, Yr55, is also located on 2D at 614.15 Mbp, and linked to marker Xmag4089 (Xue et al. 2008; McIntosh et al. 2014). Hence it is possible that the QTL in our study corresponds to either of the two known YR resistance genes.
Conclusions
YR resistance in our study was inherited in a quantitative manner by several QTL with major or minor effects. Most populations had one major QTL and one to three minor QTL segregating for YR resistance adding to 12 loci in seven populations. The diversity of resistance genes in the few parents in our study is likely underestimated due to the small population size, but might explain why 73% of the seed multiplication area in Germany includes varieties that are resistant to YR (score 1–3 on the 1–9 scale, where 1 = totally resistant, BSL 2024). Each cross analyzed here segregated at several loci. The combined action of these genes many of which conferred APR with reputed durability is expected to confer more durability.
The durability of the three mapped SR resistance genes is questionable. Sr24 is known to be effective against many Pgt races including the original Ug99 (TTKSK) but has been overcome by Ug99 variants such as TTKST (Jin et al. 2007) as well as by race TKKTP in the 2013 German epidemic (Olivera Firpo et al. 2017; Flath et al. 2018). Hence it is still conferring resistance in Europe but should be considered vulnerable wherever cultivars with this gene are grown. Sr31 is still a valuable resistance source in Europe but heed must be taken from the Ug99 events and the recent warning that virulent races could emerge from sexual hybridization (Olivera et al. 2022; Patpour et al. 2022). However, virulence surveys always focus on seedling resistance, whereas breeders score resistances only in the adult-plant stage within their field trials. A good example of this study is the Sr38/Yr17/Lr37 gene cluster, where we could detect partial but effective disease reduction in the field for both rust diseases although according to virulence studies it should have been overcome by some of the rust races we inoculated.
With the threat of increasing environmental temperatures and the recent outbreaks of stem rust in Europe there is a need to have defined resistance sources for the region. This study clearly shows that the resistance variation in a selected group of current German varieties is limited to three or four all-stage resistance genes that are vulnerable to virulence changes in the pathogen population. It will be necessary to look beyond European winter wheat germplasm for resistance sources, either by identifying and transferring resistance from related species (resistance that is most likely to be ASR, because of the technical difficulties involved) or sourcing resistant materials from other countries or programs, the most obvious of which is CIMMYT. Wheat with durable stem rust resistance largely based on the classic APR gene Sr2 (or ‘Sr2 complex’ that still remains ill-defined). There are also so-called multi-pathogen resistance genes Lr34+, Lr46+and Lr67+ for which repeated analyses have identified small QTL effects on stem rust response. Each of these genes have added morphological effects such a pseudo black chaff and excessive leaf tip necrosis that breeders will need to address, but if durable resistance is to be a national objective they are the currently best understood targets with well proven genetic markers to support their exploitation.
Yellow rust resistance is a different issue—almost every quantitative genetics study worldwide has shown that any acceptable level of APR (e.g., MR or below in repeated tests) is based on the additive effects of a few chromosomal regions that either have common genes or clusters of multiple genes such the chromosome 6AL effect discussed above. Moreover, if heed is taken of the above multi-pathogen resistance genes there will be the added benefits coming from those genes. While for stem rust, new resistance sources must be urgently introgressed in European wheat breeding, for yellow rust, marker-based selection techniques like genomic selection (GS) might be a more efficient approach to accumulate minor and major resistance QTLs in single genotypes. Still, with resistances from more distant germplasm field trials remain necessary in the adult-plant stage and are the gold standard for resistance data generation.
References
Basnet BR, Singh RP, Ibrahim AMH, Herrera-Foessel SA, Huerta-Espino J, Lan C, Rudd JC (2014) Characterization of Yr54 and other genes associated with adult plant resistance to yellow rust and leaf rust in common wheat Quaiu 3. Mol Breed 33:385–399. https://doi.org/10.1007/s11032-013-9957-2
Bayles R, Flath K, Hovmøller M, de Vallavieille-Pope C (2000) Breakdown of the Yr17 resistance to yellow rust of wheat in northern Europe. Agronomie 20:805–811. https://doi.org/10.1051/agro:2000176
Beavis WD (1998) QTL analyses: power, precision, and accuracy. In: Paterson AH (ed) Molecular dissection of complex traits. CRC Press, New York, pp 145–162
Berlin A (2017) Stem rust attacks in Sweden heralds the return of a previously vanquished foe. SLU news. https://www.slu.se/en/ew-news/2017/11/stem-rust-attacks-in-sweden-heralds-the-return-of-a-previously-vanquished-foe. Accessed 19 April 2024
Bernal-Vasquez A-M, Utz H-F, Piepho H-P (2016) Outlier detection methods for generalized lattices: a case study on the transition from ANOVA to REML. Theor Appl Genet 129:787–804. https://doi.org/10.1007/s00122-016-2666-6
Beukert U, Liu G, Thorwarth P, Boeven PH, Longin CFH, Zhao Y, Ganal M, Serfling A, Ordon F, Reif JC (2020) The potential of hybrid breeding to enhance leaf rust and stripe rust resistance in wheat. Theor Appl Genet 133:2171–2181. https://doi.org/10.1007/s00122-020-03588-y
Bhattacharya S (2017) Deadly new wheat disease threatens Europe’s crops. Nature 542:145–146. https://doi.org/10.1038/nature.2017.21424
Bouvet L, Holdgate S, James L, Thomas J, Mackay IJ, Cockram J (2022a) The evolving battle between yellow rust and wheat: implications for global food security. Theor Appl Genet 135:741–753. https://doi.org/10.1007/s00122-021-03983-z
Bouvet L, Percival-Alwyn L, Berry S, Fenwick P, Campos Mantello C, Sharma R, Holdgate S, Mackay IJ, Cockram J (2022b) Wheat genetic loci conferring resistance to stripe rust in the face of genetically diverse races of the fungus Puccinia striiformis f. sp. tritici. Theor Appl Genet 135:301–319. https://doi.org/10.1007/s00122-021-03967-z
Brodny U, Nelson RR, Gregory LV (1986) Residual and interactive expressions of" defeated" wheat stem rust resistance genes. Phytopathology 76:546–549
BSL (2024) Descriptive variety list. Cereal, maize, large grained pulse crops, root crops (except potato) (In German). Bundessortenamt, Hannover. Internet: https://www.bundessortenamt.de/bsa/media/Files/BSL/bsl_getreide_2024.pdf. Accessed 20 Aug 2024
Butler D (2021) Asreml: fits the linear mixed model. R package version 4.1.0.160. VSN International Ltd, Hemel Hempstead, HP1 1ES, UK. https://asreml.kb.vsni.co.uk/knowledge-base/asreml/. Accessed 26 April 2024
Chen XM (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Can J Plant Pathol 27:314–337. https://doi.org/10.1080/07060660509507230
Cheng B, Gao X, Cao N, Ding Y, Chen T, Zhou Q, Gao Y, Xin Z, Zhang L (2022) QTL mapping for adult plant resistance to wheat stripe rust in M96–5 × Guixie 3 wheat population. J Appl Genet 63:265–279. https://doi.org/10.1007/s13353-022-00686-z
DIRECTIVE 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. OJ L 309, 24.11.2009, pp 71–86. http://data.europa.eu/eli/dir/2009/128/oj. Accessed 26 April 2024
Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN, Joly DL (2014) The past, present and future of breeding rust resistant wheat. Front Plant Sci 5:641. https://doi.org/10.3389/fpls.2014.00641
FAO (2024) Rust spore. A Global Wheat Rust Monitoring Sysxtem. Stem Rust Race Nomenclature. https://www.fao.org/agriculture/crops/rust/stem/stem-pathotypetracker/stem-racenomenclature/en/. Accessed 11 July 2024
Flath K, Miedaner T, Olivera PD, Rouse MN, Jin Y (2018) Genes for wheat stem rust resistance postulated in German cultivars and their efficacy in seedling and adult-plant field tests. Plant Breed 137:301–312. https://doi.org/10.1111/pbr.12591
Flath K, Sommerfeldt-Impe N, Schmitt AK (2014) Occurrence of wheat stripe and stem rust in Germany and consequences for breeders and growers. In: BGRI 2014 Technical Workshop, Abstract 15. Obregón, p 15
Gao X, Starmer J, Martin ER (2008) A multiple testing correction method for genetic association studies using correlated single nucleotide polymorphisms. Genet Epidemiol 32:361–369. https://doi.org/10.1002/gepi.20310
Global Rust Reference Center (2023a) Global Rust Reference Center. Yellow Rust Tools—maps and charts. Races—Changes across years. https://agro.au.dk/forskning/internationale-platforme/wheatrust/yellow-rust-tools-maps-and-charts/races-changes-across-years. Accessed 26 April 2024
Global Rust Reference Center (2023b) Global Rust Refernce Center. Stem Rust Tools—maps and charts. Races—Changes across years. https://agro.au.dk/forskning/internationale-platforme/wheatrust/stem-rust-tools-maps-and-charts/races-changes-across-years. Accessed 26 April 2024
Hafeez AN, Arora S, Ghosh S, Gilbert D, Bowden RL, Wulff BB (2021) Creation and judicious application of a wheat resistance gene atlas. Mol Plant 14:1053–1070. https://doi.org/10.1016/j.molp.2021.05.014
Helguera M, Khan IA, Kolmer J, Lijavetzky D, Zhong-qi L, Dubcovsky J (2003) PCR assays for the Lr37-Yr17-Sr38 cluster of rust resistance genes and their use to develop isogenic hard red spring wheat lines. Crop Sci 43:1839–1847. https://doi.org/10.2135/cropsci2003.1839
Hovmøller MS, Walter S, Bayles RA, Hubbard A, Flath K, Sommerfeldt N, Leconte M, Czembor P, Rodriguez-Algaba J, Thach T, Hansen JG, Lassen P, Justesen AF, Ali S, de Vallavieille-Pope C (2016) Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. Plant Pathol 65:402–411. https://doi.org/10.1111/ppa.12433
Hovmøller MS, Rodriguez-Algaba J, Thach T, Sørensen CK (2017) Race typing of Puccinia striiformis on Wheat. In: Periyannan S (ed) Wheat rust diseases. Methods in molecular biology, vol 1659. Humana Press, New York, pp 29–40. https://doi.org/10.1007/978-1-4939-7249-4_3 Accessed 26 April 2024
Hovmøller MS, Patpour M, Rodriguez-Algaba J, Thach T, Søren-Sen CK, Justesen AF, Hansen JG (2022) GRRC report of yellow and stem rust genotyping and race analyses 2021, Aarhus University. https://agro.au.dk/forskning/internationale-platforme/wheatrust/news-and-events/news-item/artikel/grrc-report-of-yellow-and-stem-rust-genotyping-and-race-analyses-2021. Accessed 26 April 2024
Jagger LJ, Newell C, Berry ST, MacCormack R, Boyd LA (2011) The genetic characterisation of stripe rust resistance in the German wheat cultivar Alcedo. Theor Appl Genet 122:723–733. https://doi.org/10.1007/s00122-010-1481-8
Jess S, Kildea S, Moody A, Rennick G, Murchie AK, Cooke LR (2014) European Union policy on pesticides: implications for agriculture in Ireland. Pest Manag Sci 70:1646–1654. https://doi.org/10.1002/ps.3801
Jin Y, Singh RP, Ward RW, Wanyera R, Kinyua M, Njau P, Fetch T, Pretorius ZA, Yahyaoui A (2007) Characterization of seedling infection types and adult plant infection responses of monogenic Sr gene lines to race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 91:1096–1099. https://doi.org/10.1094/PDIS-91-9-1096
Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch T (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92:923–926. https://doi.org/10.1094/PDIS-92-6-0923
Kale SM, Schulthess AW, Padmarasu S, Boeven PH, Schacht J, Himmelbach A, Steuernagel B, Wulff BBH, Reif JC, Stein N, Mascher M (2022) A catalogue of resistance gene homologs and a chromosome-scale reference sequence support resistance gene mapping in winter wheat. Plant Biotechnol J 20:1730–1742. https://doi.org/10.1111/pbi.13843
Kokhmetova A, Rsaliyev A, Malysheva A, Atishova M, Kumarbayeva M, Keishilov Z (2021) Identification of stripe rust resistance genes in common wheat cultivars and breeding lines from Kazakhstan. Plants 10:2303. https://doi.org/10.3390/plants10112303
Kumar S, Saini DK, Jan F et al (2023) Comprehensive meta-QTL analysis for dissecting the genetic architecture of stripe rust resistance in bread wheat. BMC Genomics 24:259. https://doi.org/10.1186/s12864-023-09336-y
Li Y, Liu L, Wang M, Ruff T, See DR, Hu X, Chen X (2023) Characterization and molecular mapping of a gene conferring high-temperature adult-plant resistance to stripe rust originally from Aegilops ventricosa. Plant Dis 107:431–442
Lin M, Dieseth JA, Alsheikh M, Yang E, Holzapfel J, Schürmann F, Morales L, Michel S, Buerstmayr H, Bhavani S, Lillemo M (2023) A major yellow rust resistance QTL on chromosome 6A shows increased frequency in recent Norwegian spring wheat cultivars and breeding lines. Theor Appl Genet 136:164. https://doi.org/10.1007/s00122-023-04397-9
Liu L, Wang M, Zhang Z, See DR, Chen X (2020) Identification of stripe rust resistance loci in US spring wheat cultivars and breeding lines using genome-wide association mapping and Yr gene markers. Plant Dis 104:2181–2192
Mago R, Spielmeyer W, Lawrence GJ, Lagudah ES, Ellis JG, Pryor A (2002) Identification and mapping of molecular markers linked to rust resistance genes located on chromosome 1RS of rye using wheat-rye translocation lines. Theor Appl Genet 104:1317–1324. https://doi.org/10.1007/s00122-002-0879-3
Mago R, Bariana HS, Dundas IS, Spielmeyer W, Lawrence GJ, Pryor AJ, Ellis JG (2005a) Development of PCR markers for the selection of wheat stem rust resistance genes Sr24 and Sr26 in diverse wheat germplasm. Theor Appl Genet 111:496–504. https://doi.org/10.1007/s00122-005-2039-z
Mago R, Miah H, Lawrence GJ, Wellings CR, Spielmeyer W, Bariana HS, McIntosh RA, Pryor AJ, Ellis JG (2005b) High-resolution mapping and mutation analysis separate the rust resistance genes Sr31, Lr26 and Yr9 on the short arm of rye chromosome 1. Theor Appl Genet 112:41–50. https://doi.org/10.1007/s00122-005-0098-9
McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379. https://doi.org/10.1146/annurev.phyto.40.120501.101443
McIntosh RA, Dyck PL, Green GJ (1977) Inheritance of leaf rust and stem rust resistances in wheat cultivars Agent and Agatha. Aust J Agric Res 28:3745. https://doi.org/10.1071/AR9770037
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publications, East Melbourne
McIntosh R, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Appels R, Xia X (2013) Catalogue of gene symbols for wheat. In: Ogihara Y (ed) Proceeding of the 12th International Wheat Genetics Symposium, Yokohama, Japan, pp 8–13
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia XC (2014) Catalogue of gene symbols for wheat: 2013-2014 supplement. https://wheat.pw.usda.gov/GG3/wgc. Accessed 24 April 2024
McIntosh RA, Dubcovsky J, Rogers WJ, Xia XC, Raupp WJ (2020) Catalogue of gene symbols for wheat: 2020 supplement. https://wheat.pw.usda.gov/GG3/wgc. Accessed 24 April 2024
Miedaner T (2016) Breeding strategies for improving plant resistance to diseases. In: Al-Khayri JM, Jain SM, Johnson DV (eds) Advances in plant breeding strategies: agronomic, abiotic and biotic stress traits. Springer, Berlin, pp 561–599. https://doi.org/10.1007/978-3-319-22518-0
Miedaner T, Juroszek P (2021) Climate change will influence disease resistance breeding in wheat in Northwestern Europe. Theor Appl Genet 134:1771–1785. https://doi.org/10.1007/s00122-021-03807-0
Miedaner T, Akel W, Flath K, Jacobi A, Taylor M, Longin F, Würschum T (2020) Molecular tracking of multiple disease resistance in a winter wheat diversity panel. Theor Appl Genet 133:419–431. https://doi.org/10.1007/s00122-019-03472-4
Milus EA, Lee KD, Brown-Guedira G (2015) Characterization of stripe rust resistance in wheat lines with resistance gene Yr17 and implications for evaluating resistance and virulence. Phytopathology 105:1123–1130. https://doi.org/10.1094/PHYTO-11-14-0304-R
Möhring J, Piepho HP (2009) Comparison of weighting in two-stage analysis of plant breeding trials. Crop Sci 49:1977–1988. https://doi.org/10.2135/cropsci2009.02.0083
Mundt CC (2018) Pyramiding for resistance durability: theory and practice. Phytopathology 108:792–802. https://doi.org/10.1094/PHYTO-12-17-0426-RVW
Olivera P, Newcomb M, Szabo LJ et al (2015) Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in southern Ethiopia in 2013–14. Phytopathology 105:917–928. https://doi.org/10.1094/PHYTO-11-14-0302-FI
Olivera PD, Villegas D, Cantero-Martínez C, Szabo LJ, Rouse MN, Luster DG, Bartaula R, Lopes MS, Jin Y (2022) A unique race of the wheat stem rust pathogen with virulence on Sr31 identified in Spain and reaction of wheat and durum cultivars to this race. Plant Pathol 71:873–889. https://doi.org/10.1111/ppa.13530
Olivera Firpo PD, Newcomb M, Flath K, Sommerfeldt-Impe N, Szabo LJ, Carter M, Luster DG, Jin Y (2017) Characterization of Puccinia graminis f. sp. tritici isolates derived from an unusual wheat stem rust outbreak in Germany in 2013. Plant Pathol 66:1258–1266. https://doi.org/10.1111/ppa.12674
Pal N, Jan I, Saini DK, Kumar K, Kumar A, Sharma PK, Kumar S, Balyan HS, Gupta PK (2022) Meta-QTLs for multiple disease resistance involving three rusts in common wheat (Triticum aestivum L.). Theor Appl Genet 135:2385–2405. https://doi.org/10.1007/s00122-022-04119-7
Pathan AK, Park RF (2007) Evaluation of seedling and adult plant resistance to stem rust in European wheat cultivars. Euphytica 155:87–105. https://doi.org/10.1007/s10681-006-9308-z
Patpour M, Hovmøller MS, Rodriguez-Algaba J et al (2022) Wheat stem rust back in Europe: diversity, prevalence and impact on host resistance. Front Plant Sci 13:882440. https://doi.org/10.3389/fpls.2022.882440
Patpour M, Baidya S, Basnet R, Justesen AF, Hodson D, Thapa D, Hovmøller MS (2024) First report of Ug99 Wheat Stem Rust caused by Puccinia graminis f. sp. tritici in South Asia. Plant Dis 1:1–2. https://doi.org/10.1094/PDIS-03-24-0644-PDN. (in print)
Piepho HP, Möhring J (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177:1881–1888. https://doi.org/10.1534/genetics.107.074229
Porceddu E, Ceoloni C, Lafiandra D et al (1988) Genetic resources and plant breeding: problems and prospects. In: Miller TE, Koebner RMD (eds) Proceedings of the 7th International wheat genetics symposium, Cambridge, 13–19 July 1988, vol 1, Institute of Plant Science Research, Cambridge Laboratory, pp 7–22
Qiu Y, Mei J (2019) RSpectra: solvers for large-scale eigenvalue and SVD problems. R package version 0.14-0. https://CRAN.R-project.org/package=RSpectra. Accessed 12 Feb 2024
Ren TH, Yang ZJ, Yan BJ, Zhang HQ, Fu SL, Ren ZL (2009) Development and characterization of a new 1BL.1RS translocation line with resistance to stripe rust and powdery mildew of wheat. Euphytica 169:207–213. https://doi.org/10.1007/s10681-009-9924-5
Roelfs AP, Martens JW (1988) An international system of nomenclature for Puccinia graminis f. sp. tritici. Phytopathology 78(5):526–533
Rollar S, Geyer M, Hartl L, Mohler V, Ordon F, Serfling A (2021) Quantitative trait loci mapping of adult plant and seedling resistance to stripe rust (Puccinia striiformis Westend.) in a multiparent advanced generation intercross wheat population. Front Plant Sci 12:684671. https://doi.org/10.3389/fpls.2021.684671
Saunders DGO, Pretorius ZA, Hovmøller MS (2019) Tackling the re-emergence of wheat stem rust in Western Europe. Commun Biol 2:51. https://doi.org/10.1038/s42003-019-0294-9
Schlegel R, Korzun V (1997) About the origin of 1RS.1BL wheat-rye chromosome translocations from Germany. Plant Breed 116:537–540. https://doi.org/10.1111/j.1439-0523.1997.tb02186.x
Seah S, Bariana H, Jahier J, Sivasithamparam K, Lagudah ES (2001) The introgressed segment carrying rust resistance genes Yr17, Lr37 and Sr38 in wheat can be assayed by a cloned disease resistance gene-like sequence. Theor Appl Genet 102:600–605. https://doi.org/10.1007/s001220051686
Serfling A, Kopahnke D, Habekuss A, Novakazi F, Ordon F (2016) Wheat diseases: an overview. In: Langridge P (ed) Achieving sustainable cultivation of wheat, vol 1. breeding, quality traits, pests and diseases. Burleigh Dodds Science Publishing, Cambridge, pp 263–294. https://doi.org/10.19103/as.2016.0004.19
Shahinnia F, Geyer M, Schürmann F et al (2022) Genome-wide association study and genomic prediction of resistance to stripe rust in current Central and Northern European winter wheat germplasm. Theor Appl Genet 135:3583–3595. https://doi.org/10.1007/s00122-022-04202-z
Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA, Bhavani S, Rouse MN, Pretorius ZA, Szabo LJ, Huerta-Espino J, Basnet BR, Lan C, Hovmøller MS (2015) Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathology 105:872–884. https://doi.org/10.1094/PHYTO-01-15-0030-FI
Singh H, Kaur J, Bala R, Srivastava P, Sharma A, Grover G et al (2022) Residual effect of defeated stripe rust resistance genes/QTLs in bread wheat against prevalent pathotypes of Puccinia striiformis f. sp. tritici. PLoS ONE 17(4):e0266482. https://doi.org/10.1371/journal.pone.0266482
Tong J, Zhao C, Liu D, Jambuthenne DT, Sun M, Dinglasan E et al (2024) Genome-wide atlas of rust resistance loci in wheat. Theor Appl Genet 137:179. https://doi.org/10.1007/s00122-024-04689-8
Tsushima A, Lewis CM, Flath K, Kildea S, Saunders DG (2022) Wheat stem rust recorded for the first time in decades in Ireland. Plant Pathol 71:890–900. https://doi.org/10.1111/ppa.13532
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423. https://doi.org/10.3168/jds.2007-0980
Walkowiak S, Gao L, Monat C et al (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature 588:277–283. https://doi.org/10.1038/s41586-020-2961-x
Wang Y, Yu C, Cheng Y, Yao F, Long L, Wu Y, Li J, Li H, Wang J, Jiang Q, Li W, Pu Z, Qi P, Ma J, Deng M, Wei Y, Chen X, Chen G, Kang H, Jiang Y, Zheng Y (2021) Genome-wide association mapping reveals potential novel loci controlling stripe rust resistance in a Chinese wheat landrace diversity panel from the southern autumn-sown spring wheat zone. BMC Genomics 22:34. https://doi.org/10.1186/s12864-020-07331-1
Xu S (2003) Theoretical basis of the Beavis effect. Genetics 165:2259–2268. https://doi.org/10.1093/genetics/165.4.2259
Xue S, Zhang Z, Lin F, Kong Z, Cao Y, Li C, Yi H, Mei M, Zhu H, Wu J, Xu H, Zhao D, Tian D, Zhang C, Ma Z (2008) A high-density intervarietal map of the wheat genome enriched with markers derived from expressed sequence tags. Theor Appl Genet 117:181–189. https://doi.org/10.1007/s00122-008-076
Zelba O, Hanzalová A, Dumalasová V, Viehmannová I (2022) Analyzing wheat cultivars grown in Czech Republic for eight stem rust resistance genes. Europ J Pl Path 162:221–230. https://doi.org/10.1007/s10658-021-02397-3
Zhang D, Bowden RL, Yu J, Carver BF, Bai G (2014) Association analysis of stem rust resistance in US winter wheat. PLoS ONE 9(7):e103747. https://doi.org/10.1371/journal.pone.0103747
Acknowledgements
The authors thank the technical teams at the different locations for valuable help. Also, we are grateful to the reviewers for their highly valuable suggestions and improvements to the manuscript.
Funding
Open Access funding enabled and organized by Projekt DEAL. This study was funded by a grant of the German ‘Bundesministerium für Ernährung und Landwirtschaft (BMEL)’ based on a resolution of the German ‘Bundestag’ to Thomas Miedaner and Kerstin Flath. The ‘Bundesanstalt für Landwirtschaft und Ernährung (BLE)’ holds the project sponsorship within the program for “Promotion of Innovation” (Innovationsprogramm, GetreideProtekt, grant no. FKZ281B202016). Open Access funding enabled and organized by Projekt DEAL.
Author information
Authors and Affiliations
Contributions
Study conception and design were performed by Thomas Miedaner and Kerstin Flath. Material preparation and data collection were performed by Johannes Schacht, Philipp Boeven, Wessam Akel, and Hubert Kempf for their respective wheat populations and locations, data collection at Berlin-Dahlem by Kerstin Flath and Anne-Kristin Schmitt. PCR-marker analyses were done by Philipp Schulz. All statistical analyses were performed by Wera Eckhoff and Paul Gruner. The manuscript was written by Thomas Miedaner with input from all authors, Paul Gruner and Kerstin Flath contributed to the final draft. All authors approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Thomas Miedaner is on the editorial board of TAG. All other authors declare no conflict of interest.
Ethical approval
The authors declare that the experiments do not involve humans or animals and comply with the current laws in Germany.
Additional information
Communicated by Urmil Bansal.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Miedaner, T., Eckhoff, W., Flath, K. et al. Mapping rust resistance in European winter wheat: many QTLs for yellow rust resistance, but only a few well characterized genes for stem rust resistance. Theor Appl Genet 137, 215 (2024). https://doi.org/10.1007/s00122-024-04731-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-024-04731-9