The genetics of Ug99 stem rust resistance in spring wheat variety ‘Linkert‘

Abstract

Wheat stem rust caused by Puccinia graminis f. sp. tritici (Pgt) threatens wheat production worldwide. The objective of this study was to characterize wheat stem rust resistance in ‘Linkert’, a variety with adult plant resistance effective to emerging wheat stem rust pathogen strain Ug99. Two doubled haploid (DH) populations and one recombinant inbred line (RIL) population were developed with ‘Linkert’ as a stem rust resistant parent. Hard red spring wheat variety ‘Forefront’ and genetic stock ‘LMPG’ were used as stem rust susceptible parents of the DH populations. Breeding line ‘MN07098-6’ was used as a susceptible parent of the RIL population. Both DH and RIL populations with their parents were evaluated both at the seedling stage and in the field against Pgt races. Genotyping data of the DH populations were generated using the wheat iSelect 90k SNP assay. The RIL population was genotyped by genotyping-by-sequencing. We found QTL consistently associated with wheat stem rust resistance on chromosome 2BS for the Linkert/Forefront DH population and the Linkert/MN07098-6 RIL population both in Ethiopia and Kenya. Additional reliable QTL were detected on chromosomes 5BL (125.91 cM) and 4AL (Sr7a) for the Linkert/LMPG population in Ethiopia and Kenya. Different QTL identified in the populations reflect the importance of examining the genetics of resistance in populations derived from adapted germplasm (Forefront and MN07098-6) in addition to a genetic stock (LMPG). The associated markers in this study could be used to track and select for the identified QTL in wheat breeding programs.

Introduction

Stem rust of wheat (Triticum aestivum L.), caused by Puccinia graminis f. sp. tritici (Pgt) Erikss. & Henning, is a destructive disease of wheat worldwide (Singh et al., 2011; Savary et al., 2019). The emergence of a race of Pgt known as Ug99 that defeats the widely deployed stem rust resistance gene, Sr31, poses a threat to wheat production (Singh et al., 2015). The use of genetic resistance is a preferred strategy for mitigating losses from crop diseases including stem rust of wheat.

Breeding for disease resistance is one of the primary objectives of wheat improvement programs in the United States and worldwide. Since the early 20^th century, there have been international collaborations on genetic resistance breeding for controlling stem rust disease in wheat (Triticum spp.) (Carleton, 1905; Waldron, 1935; Stakman, 1955; Evans, 1980). Consequently, to date 64 stem rust resistance (Sr) genes have been characterized and mapped to chromosome locations in wheat (McIntosh et al., 2020). Out of these, 16 wheat Sr genes have been cloned by either map-based cloning (Sr13, Sr21, Sr33, Sr35, Sr50, Sr55, Sr57, Sr60, and Sr62) or target sequence capture approaches (Sr22, Sr26, Sr27, Sr43, Sr45, Sr46, and Sr61) (Arora et al., 2019; Periyannan et al., 2013; Zhang et al., 2017; Chen et al., 2018; Saintenac et al., 2013; Mago et al., 2015; Moore et al., 2015; Krattinger et al., 2009; Steuernagel et al., 2016; Chen et al., 2020; Zhang et al., 2021; Yu et al., 2022). Since the discovery of Ug99, there has been an intensive search for resistance genes both in domesticated wheat and its wild relatives, and 36 numerically designated stem rust resistance genes that are effective to the Ug99 race group have been characterized (Rouse et al., 2014a; Singh et al., 2015): Sr2, Sr12, Sr13, Sr14, Sr15, Sr21, Sr22, Sr25, Sr26, Sr27, Sr28, Sr29, Sr32, Sr33, Sr35, Sr37, Sr39, Sr40, Sr42, Sr43, Sr44, Sr45, Sr46, Sr47, Sr48, Sr50, Sr51, Sr52, Sr53, Sr55, Sr56, Sr57, Sr59, Sr61, Sr62, and Sr63. However, only few are available in conventional North American spring wheat germplasm including Sr2, Sr12, Sr13, Sr25, Sr55, and Sr57 (Rouse et al., 2014b; Bajgain et al., 2015a; Edae et al., 2018). In addition, many QTL have also been reported using bi-parental populations (Hiebert et al., 2010; Haile et al., 2012; Njau et al., 2013; Zurn et al., 2014; Kumsa et al., 2015; Bajgain et al., 2015b), and association mapping (Yu et al., 2011; Letta et al., 2013; Zhang et al., 2014; Bajgain et al., 2015a; Edae et al., 2018). Despite the availability of numerous genes and QTL, stem rust still remains a threat to wheat production worldwide due to continuous emergence of new Pgt races in different parts of the world and the lack of resistance deployed in conventional wheat varieties effective to the emerging races (Olivera et al., 2015; Newcomb et al., 2016; Olivera et al., 2019, 2022). This implies the importance of persistently carrying out resistance breeding in wheat through the identification and characterization of new resistance genes from both domestic germplasm and its wild relatives.

The development of new sequencing technologies has facilitated the discovery of a large number of SNP markers for many crop species such as hexaploid wheat (Chapman et al., 2015), barley (Mascher et al., 2013), rice (Spindel et al., 2013) and maize (Romay et al., 2013). Genomic/genomic resources such as wheat reference sequences The International Wheat Genome Sequencing Consortium (IWGSC), 2018), wheat 90K iselect SNP chips (Wang et al., 2014) and genotype-by-sequencing (GBS), a reduced representation genotyping platform (Poland et al., 2012), have been used effectively to discover genes/QTL for several traits including disease resistance in wheat.

Genetic resistance to rust pathogens can be generally grouped into two categories: resistance that is effective at all plant growth stages and resistance that is effective at the adult plant stage. All-stage resistance genes often confer major-effects and account for thirty of the thirty-six Ug99-effective genes. Adult plant resistance genes often confer relatively minor effects and include Sr2, Lr67/Sr55/Yr46/Pm46, Sr56, Lr34/Sr57Yr18/Pm38, Lr46/Sr58/Yr29/Pm39, and Sr63 (Mago et al., 2002; Singh et al., 2015). These six designated adult plant resistance genes have not been reported to exhibit race-specificity supporting an expectation (Singh et al., 2011, 2014) that effective adult plant resistance genes are non-race-specific. Though few examples of race-specific adult plant resistance genes have been reported for stripe rust (Yr11, 12, 13, and 14; Milus et al., 2015) and leaf rust (Lr12; Singh and Bowden, 2010), the generally non-race-specific characteristic of adult plant resistance genes justifies an emphasis on adult plant resistance for achieving durable resistance to stem rust in wheat.

Though an abundance of genetic sources of resistance exist to emerging stem rust races, few conventional wheat varieties possess effective resistance. Singh et al., 2015 reported that only 16% of U.S. hard red spring wheat varieties and breeding lines showed resistance to the Ug99 race group. This susceptibility is significant as the U.S. hard red spring wheat growing region is historically vulnerable to major epidemics of wheat stem rust when virulent races are present, resulting in over 50% statewide yield losses in Minnesota and North Dakota during epidemic years. One exception to this widespread vulnerability is hard red spring wheat variety ‘Linkert’, released in 2013 by the University of Minnesota (Anderson et al., 2018). Linkert exhibited consistent adult plant resistance to Ug99 in Kenya (Anderson et al., 2018). Linkert became a successful variety that was grown on 833,900 acres in Minnesota and North Dakota in 2018 and was the most widely grown wheat variety in Minnesota from 2016 to 2020. The objective of this study was to characterize the genetics of stem rust resistance in ‘Linkert’ with particular attention to the adult plant resistance exhibited to Ug99.

Materials and methods

Mapping populations

Two doubled haploid (DH) mapping populations were developed by crossing Linkert with both hard red spring wheat variety ‘Forefront’ (Glover et al., 2013) and genetic stock LMPG-6 (‘Little Club’//3 3 ‘Prelude’/8 3 Marquis’/3/’Gabo’), a highly rust susceptible, day length insensitive line that was developed for the purpose of producing near-isogenic lines for Sr genes (Knott, 2000). ‘Linkert’ is a hard red spring wheat developed and released by the Minnesota Agricultural Experiment Station (MAES) in 2013. Linkert is one of the highest quality hard red winter wheats with yield comparable to other high protein varieties and better disease resistance. Doubled haploid progeny were produced at a service facility at Washington State University through a modified maize pollination method (Niu et al., 2014). A recombinant inbred line (RIL) population was derived through single seed descent to the F₆ generation after crossing Linkert and University of Minnesota breeding line ‘MN07098-6’. A total of 107, 190, and 172 lines were derived from the Linkert/Forefront (LK/FF), Linkert/LMPG-6 (LK/LM), and Linkert/MN07098-6 (09X149) populations, respectively.

Disease evaluations

The lines in the DH populations with their parents were evaluated in the field for three years (2016-2018) in Kenya for response to the Ug99 race group (Pgt races including TTKSK, TTKTT), and in Ethiopia for response to Pgt races TKTTF, TTKSK, TRTTF and JRCQC (Kosgey et al., 2021). The RIL population (F_6:8 generation) was evaluated in Kenya and Ethiopia for two years (2016 and 2017). The DH populations were also evaluated at Rosemont, MN for three years (2015-2017) with four domestic Pgt races evaluated in single race nurseries inoculated with races QTHJC, QFCSC, TPMKC and RCRSC, according to previously described methods (Edae et al., 2018). Mixtures of spores of Pgt races for field evaluations were inoculated both in Ethiopia and Kenya (Kosgey et al., 2021). Stem rust severity was visually scored in the experimental plots based on the modified Cobb scale of 0-100, where 0 = immunity (no uredinia or any other sign of infection) and 100% = completely susceptible (Peterson et al., 1948). Infection response was rated as resistant (R), small uredinia surrounded by necrosis; moderately resistant (MR), medium-sized uredinia surrounded by necrosis or chlorosis; moderately susceptible (MS), medium-sized uredinia without necrosis; susceptible (S), large uredinia without necrosis; or MRMS, an infection response that included both the MR and MS categories (Roelfs et al., 1992). Coefficient of infection (COI) values were generated by multiplying the stem rust severity value for each line by a constant value for each infection response: 0 = 0, R = 0.2, RMR = 0.3, MR = 0.4, M = 0.6, MS = 0.8, S = 1.0 (Knott, 1989). Average coefficient of infection for the two replicates were determined and used for analyses. Raw mean coefficients of infection values across the two randomized replicates in each environment were used for QTL analyses.

At the seedling stage, the DH populations and parents were evaluated with Pgt races QTHJC (isolate 0069MN399), QFCSC (isolate 95MN1080), TPMKC (isolate 74MN1409), RCRSC (isolate 00MN99C), TRTTF (06YEM34-1), and TKTTF (isolate 13ETH18-1) according to previously described methods (Hundie et al., 2019). All four parents were susceptible as seedlings to race TTKSK (04KEN156/04; Ug99 race group).

DNA extraction and genotyping

Tissues were harvested from approximately two weeks old seedlings of the populations and parents and grown in a greenhouse before placing into 96-well plates. The harvested leaves were dried in a lyophilizer and ground for 2 min using a Genogrinder (SPEX Sample Prep). DNA extraction was carried out following an SDS method: 300 µl extraction buffer (200 mM Tris-HCL pH 8.0, 250 mM NaCl, 25 mM EDTA, 0.5% SDS, ddH20) was added to each well followed by gently shaking the 96-well plates before adding 300 µl of chloroform:isoamyl alcohol (24:1) to each well. The suspension was mixed for 3 minutes on a plate shaker followed by centrifuging for 20 min at 2500 rpm, and the supernatant (200-300 µl) was transferred to separate tubes.

After decanting the supernatant, 300 µl of 70% ethanol was added to each tube, the tubes were centrifuged for 20 min at 2,500 rpm, the ethanol was poured out, and the DNA pellets were air-dried. When the pellets were completely dry, 100 µl of 1xTE was added to each tube to resuspend the pellet. DNA was quantified using a NanoDrop 1000 spectrophotometer (Thermo Fisher, Waltham, MA, United States).

Genotyping data of the DH populations were generated using the iSelect 90k SNP assay developed for wheat (Wang et al., 2014). SNPs with minor allele frequency (MAF) less than 25% were removed, all monomorphic markers and markers with missing data points for one or both parental genotypes were also removed. No heterozygote genotypes were retained in the data set. Missing data points were represented by “-”. SNPs with > 10% missing data points were removed, and none of the lines were removed as missing data for all individuals for a given SNP was < 1%. SNPs with segregation distortion p-values of less than 0.5 were removed before creating linkage maps for both DH populations. For the LK/FF population, one SNP was removed due to high missing values in the segregation distortion filtered data set. However, for the LK/LM population, all SNPs had missing values < 6.4% and none of the SNPs were removed. SNPs with lod error (Lincoln and Lander, 1992) values greater than four were removed for the final linkage map construction. After applying the filtering criteria described above, a total of 1,091 and 1,552 high quality SNPs were used for QTL mapping for LK/FF and LK/LM populations, respectively. These SNP markers were used to make linkage groups using JoinMap 4.0 (Upadhyaya, 2006). The Kosambi mapping function was used to estimate the map distance.

Genomic DNA from the Linkert/MN07098-6 population was extracted using the BioSprint 96 DNA Plant Kit (QIAGEN, Valencia, CA) and genotyped using the genotype-by-sequencing approach (Poland et al., 2012). Reads were filtered for phred quality score (Q) of ≥ 30 and de-multiplexed using ‘sabre’ (https://github.com/najoshi/sabre, accessed 05-12-2022). Filtered reads were aligned to the Triticum aestivum v1.0 reference sequence (The International Wheat Genome Sequencing Consortium (IWGSC), 2018) using default parameters in the Burrows-Wheeler Aligner 0.7.5 (Li, 2013). Discovery of genome-wide markers (SNPs) was done using default parameters in SAMtools 1.6 and BCFtools 1.6 (Li et al., 2009; Li, 2011). SNPs with heterozygote level and missing data points greater than 10% and 25%, respectively, were removed. A filtered data set comprised of 1,674 SNPs was used for QTL mapping.

Quantitative trait loci (QTL) analysis was conducted in R package RQTL (Broman et al., 2003) with composite interval mapping (CIM) method using both seedling infection type data and field response data from the populations. Before QTL mapping, categorical field infection responses and seedling infection types were converted to a linear 0-9 scale (Zhang et al., 2014; Gao et al., 2016).

Results

Phenotypic evaluation

Linkert was susceptible at the seedling stage to virulent Pgt races such as TTKSK, TTKTT, and TTRTF, but was resistant to the Ethiopian TKTTF isolate. Forefront was also susceptible to both TTKSK and TTKTT (Table 1). Disease severity values ranged from 1- 47%, 4 - 44% and 4 - 25%, 65 - 70% for Linkert, Forefront, LMPG-6 and MN07098-6, respectively, for response to Pgt races in East Africa (Table 1). Although LMPG-6 had lower average severity percentage than Linkert and Forefront, the average coefficient of infection was similar for all the three parents (16.26- 17.24). For North American Pgt races, Linkert was resistant to all Pgt races (QFCSC, RCRSC, QTHJC and TPMKC) tested at the seedling stage whereas LMPG-6 was susceptible to all races. However, Forefront was resistant to QFCSC and RCRSC but susceptible to QTHJC and TPMKC races at the seedling stage (Table 2). There was strong phenotypic correlation between Ethiopia and Kenya field data based on severity and infection response except for the data from Kenya in 2016 and Ethiopia in 2017. Both severity and infection response data recorded in 2016 in Kenya were poorly correlated with other years in Kenya and Ethiopia (Figure 1; Supplementary Table 1).

Figure 1

Seedling infection type (IT) values in linear scale less than six were considered as resistant whereas IT values greater than six were considered as susceptible. All individuals of the Linkert/Forefront population were resistant to Pgt races QFCSC and RCRSC. For all races tested in this study the percentage of resistant lines was greater than 50% except for response to race TPMKC which resulted in resistance in only 35.7% of the Linkert/Forefront and 29.4% of the Linkert/LMPG individuals (Table 3).

Genetic linkage maps

For Linkert/Forefront population, a total of 1,088 SNPs from 90k SNP chip mapped to 25 linkage groups, and these 25 linkage groups corresponded to 19 wheat chromosomes. Apart from two wheat chromosomes, 6D and 7D, all wheat chromosomes were represented in the map of Linkert/Forefront population (Figure 2). For both populations, chromosome 7B comprised the highest number of SNPs whereas chromosomes 3D (5 SNPs) and 4D (11 SNPs) had the lowest number of SNPs for LK/FF and LK/LM populations, respectively (Supplementary Tables 2A, B). For the Linkert/LMPG-6 (LK/LM) population a total of 1,552 SNPs from 90k SNP chip mapped to 25 linkage groups. However, the 25 linkage groups were assigned to 17 wheat chromosomes. Five chromosomes (3D, 5D, 6D and 7D) all were from D genome were missing from the linkage (Figure 3; Supplemental Table 2B). Since SNP identification was carried out using wheat genome reference sequence for the validation population, Linkert/MN07098-6, linkage map creation was not attempted because we were able to generate this population specific physical map for the 1,674 GBS SNPs (Figure 3). Unlike 90K SNP chip, all 21 wheat chromosomes were recovered for the GBS platform and chromosome 6B had the highest number of SNPs (2540) whereas only three SNPs passed the filtering criteria for chromosome 4D (Supplementary Table 2C). Relatively GBS SNPs were only evenly distributed on chromosome 6B but for the remaining chromosomes SNPs that met the filtering criteria (see Materials and Methods section) were mainly on the terminal ends of chromosomes. However, unlike GBS, large gap size on linkage maps were not observed for the 90K SNP chip most of the cases.

Figure 2

Figure 3

QTL analyses

In this study, after considering QTL within five centimorgans as redundant QTL, a total of 55 significant QTL distributed on 18 chromosomes were detected for all populations evaluated both under field and seedling stages for resistance to stem rust (Tables 4–7). QTL were detected on all chromosomes except 5D and 7D. Although the phenotypic variance explained was less than 20% in most cases, the QTL detected on chromosomes 1BL and 4DS in the LK/LM population evaluated in the field for race QFCSC and the QTL on chromosome 4AL for race TKTTF at the seedling stage explained substantial amounts of phenotypic variation (38.4-69.0%). In this study, all-stage QTL were detected only on chromosomes 1B (52.0 cM) and 4AL for race RCRSC detected in the Linkert/Forefront and Linkert/LMPG-6 populations, respectively (Tables 4, 5). The remaining detected QTL were expressed only either at seedling or adult plant stages.

A majority of the QTL were population, environment, and race-specific. However, one QTL (marker: CAP12_c2189_159) on chromosome 2BS (1.9 cM) was detected across two populations in multiple environments (Tables 4, 7). It was also detected for field response to race QTHJC and seedling response to race TPMKC (Tables 5, 6). A population-specific stable QTL was detected on chromosome 5BL (125.9 cM) in the LK/LM population across environments in Ethiopia and Kenya (Table 4). It also provided field resistance against races RCRSC and TPMKC (Table 5). The gene Sr7a was detected on 4AL (marker: CAP12QT_c2972_140) in the LK/LM population in Ethiopia and in Rosemont for response to RCRSC in 2016, and seedling response to race TKTTF. In Linkert/MN07098-6, a QTL on chromosome 2BS (30.1 Mbp) was consistently detected and explained up to 19.3% of the phenotypic variation (Table 7). At chromosome level, Linkert/MN07098-6 had a total 11 chromosomes on which QTL were detected and some of the QTL had similar chromosome regions (e.g., 2BS) as detected in other populations.

Discussion

The objective of this study was to characterize the genetics of stem rust resistance in the hard red spring wheat variety Linkert by testing progenies developed by crossing with three stem rust susceptible lines, cultivar Forefront, breeding line MN07098-6, and genetic stock LMPG-6, with different Pgt races in the field and at the seedling stage in a greenhouse.

A reliable stem rust QTL was identified on chromosome 2BS in the Linkert/Forefront and Linkert/MN07098-6 populations. Interestingly, in addition to conferring adult plant resistance to the Ug99 race group in African field environments, it was detected at the seedling stage for response to race TPMKC. In addition to relatively consistent expression under different environments, the phenotypic variation explained by the QTL was also substantial (9.02-19.32%). Seven Sr genes have been reported on 2BS, and out of these Sr36, Sr39, and Sr40 (Wu et al., 2009; Niu et al., 2011; Rouse et al., 2012) are effective against the Ug99 race TTKSK. However, the QTL detected in this study is only effective to the Ug99 race group at the adult growth stage, excluding the previously described major effect all-stage resistance genes on chromosome arm 2BS. The coincidence of this QTL with seedling response to race TPMKC warrants further study. Kosgey et al. (2021) also detected a QTL (QSr.cdl-2BS.2) on 2BS using field-tested recombinant inbred lines derived from a cross made between CI 14275 (resistant parent) and LMPG-6 (susceptible parent), and the KASP marker that was developed from SNP Excalibur_c7963_1722_C1 was also associated with reduced stem rust severity. Thus, the resistance in Linkert and CI 14275 is most likely similar. Previous QTL mapping studies have also shown that there were at least eight QTL regions on the short arm of chromosome 2B (from 0-160 mbp range) detected in both GWAS and bi-parental populations (Crossa et al., 2007; Bajgain et al., 2015a; Bajgain et al., 2015b; Bajgain et al., 2016; Edae et al., 2018), and the associated SNPs were IWB2369 (pos: 48.5 cM; 31.50 mbp), IWB69830 (pos: 46.76 cM; 31.30 mbp), IWB24614 (104. 80 mbp), IWB32327 (104.80 mbp), IWB23439 (48.04 cM; 55.04 mbp), and BS00073426-51 (160.00 mbp). Gene Sr23 mapped on distal end of 2BS and was described as completely linked with Lr16 (McIntosh and Luig, 1973b) and expressed under conditions of high temperature and high light intensity (Luig, 1983). All cultivars that possess Lr16 also were reported to possess Sr23 (Kassa et al., 2017). Cultivars such as Exchange, Selkirk, Warden and Etoile de choisy are sources of Sr23. A recent report also indicated that Lr16 is present in North American cultivars such as ‘AC Domain’, ‘AC Karma’, ‘AC Majestic’, ‘AC Splendor’, ‘Columbus’, and ‘Grandin’ (Kassa et al., 2017). Although major gene Lr16/Sr23 was mapped on chromosome 2BS, it is unlikely that the QTL detected in the current study is Lr16/Sr23 because the QTL is mapped 21 cM away from that of the Lr16/Lr23 position.

The Linkert/LMPG-6 population possessed a relatively consistent QTL on chromosome 4AL (SNP: CAP12_c2972_140) that provided resistance against different Pgt races both at seedling and adult stages implying it can provide all-stage resistance against stem rust races RCRSC and TKTTF. Edae et al., 2018 reported a strong association signal in the region of major gene Sr7a for resistance against race RCRSC. Similarly, in this study the QTL on chromosome 4AL was detected at adult and seedling stages for Pgt race RCRSC, indicating Linkert possesses gene Sr7a, as previously postulated (Anderson et al., 2018).

The QTL detected on chromosome 5BL in Linkert/LMPG-6 was relatively stable. This region of 122-128 cM on the long arm of chromosome 5B harbored a QTL that provided field resistance against virulent races in East Africa (Ethiopia and Kenya) and North American Pgt races (RCRSC and TPMKC). This QTL was detected in the Linkert/LMPG-6 population but not in the Linkert/Forefront or Linkert/MN07098-6 populations. Stem rust resistance gene Sr56 that confers adult plant resistance (APR) was mapped on chromosome 5BL (McIntosh et al., 2012). Several QTL have been reported using both bi-parental populations and GWAS including adult plant resistance gene Sr56 (Crossa et al., 2007; Bansal et al., 2008; Bhavani et al., 2011). In previous studies the 5BL QTL representing Sr56 explained 10-13% phenotypic variation and contributed an important component of the “Sr2 complex” (Bhavani et al., 2011). The QTL detected in the current study explained up to 13% of phenotypic variation, and the QTL, QSr.Sun-5BL, reported by Bansal et al., 2008 also explained 11 to 12% of the phenotypic variation in adult plant stem rust response and was responsible for a 12-15% reduction in stem rust severity. Since Sr56 was first reported from European ‘Arina’ winter wheat, a pedigree link between Sr56 and Linkert is not known. Further studies are warranted to determine if the 5BL QTL is Sr56. It is possible that both Forefront and MN07098-6 also possess the resistance allele of the 5BL QTL, which would explain why it was not detected in the corresponding populations.

Besides stem rust QTL on 2BS, 5BL, and 4AL, numerous environment and population-specific QTL were found that corresponded with previously reported QTL. Three QTL were detected on chromosome 7A. Two of them provided resistance against Pgt race TPMKC (pos: 157.0 cM and 27.0 cM). Several QTL have been reported on 7AL (Bajgain et al., 2015a; Edae et al., 2018) for stem rust resistance, and the major genes Sr15 and Sr22 are located on 7AL (Sears and Briggle, 1969; The and McIntosh, 1975). Similarly, QTL were detected on chromosome 7B for stem rust resistance. Two QTL that provided field resistance against races QTHJC (pos: 126.0 cM) and QFCSC (pos: 144.0 cM) were detected on 7BL. Edae et al., 2018 also reported QTL for Pgt race QFCSC on 7BL (pos: 109.0 cM) using association mapping.

The seedling and single-race field experiments in Rosemount, MN facilitated a precise evaluation of resistance QTL to the four races evaluated. As expected, all-stage resistance gene Sr7a was consistently detected in both seedling and field studies in response to avirulent race RCRSC. However, the other QTL were detected only in seedling or field environments. This seems to contrast with the expectation that QTL detected at the seedling stage would be effective in the field consistent with “all-stage” resistance. This may be explained by the relatively low effectiveness of the seedling QTL detected other than Sr7a. Not detecting these weakly effective QTL in the field may be the result of (1) true ineffectiveness of these QTL in the field or (2) the masking of weakly effective all-stage QTL by the presence of adult plant resistance loci. Our results are similar with the findings of an association mapping study conducted by Edae et al., 2018 where conventional North American spring wheat lines possesses largely seedling- or field-effective QTL. Only the most strongly effective QTL were detected in both seedling and field studies.

In conclusion, despite the large number of environment and race-specific QTL identified in the current study, we found Linkert derived QTL that were consistently associated with adult plant resistance to Ug99 stem rust on chromosome 2BS in the Linkert/Forefront and Linkert/MN07098-6 populations. Additional QTL were detected consistently on chromosomes 5BL (125.9 cM) and 4AL (Sr7a) with the Linkert/LMPG population. Combined with the detection of the QTL on 2BS in previous studies, the identification of the 2BS QTL in the two populations derived from conventional germplasm demonstrates the importance of this QTL in contributing towards stem rust adult plant resistance in United States hard red spring wheat.

References

• 1

  AndersonJ. A.WiersmaJ. J.LinkertG. L.ReynoldsS. K.KolmerJ. A.JinY.et al. (2018). Registration of 'Linkert' spring wheat with good straw strength and adult plant resistance to the Ug99 family of stem rust race. J. Plant Registration12, 208–214.

  • Google Scholar
  • View reference in article

• 2

  AroraA.SteuernagelB.GauravK.ChandramohanS.LongY.MatnyO.et al. (2019). Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat. Biotechnol.37, 139–143. doi: 10.1038/s41587-018-0007-9

  • CrossRef
  • Google Scholar
  • View reference in article

• 3

  BajgainP.RouseM. N.BhavaniS.AndersonJ. A. (2015b). QTL mapping of adult plant resistance to Ug99 stem rust in the spring wheat population RB07/MN06113-8. Mol. Breed.35, 170. doi: 10.1007/s11032-015-0362-x

  • CrossRef
  • Google Scholar
  • View reference in article

• 4

  BajgainP.RouseM. N.BulliP.BhavaniS.GordonT.WanyeraR.et al. (2015a). Association mapping of North American spring wheat breeding germplasm reveals loci conferring resistance to Ug99 and other African stem rust races. BMC Plant Biol.15, 249. doi: 10.1186/s12870-015-0628-9

  • CrossRef
  • Google Scholar

• 5

  BajgainP.RouseM. N.TsiloT. J.MachariaG. K.BhavaniS.JinY.et al. (2016). Nested association mapping of stem rust resistance in wheat using genotyping by sequencing. PloS One11, e0155760. doi: 10.1371/journal.pone.0155760

  • CrossRef
  • Google Scholar
  • View reference in article

• 6

  BabikerE. M.Gordonv.BonmanJ. M. (2017). Genetic Loci conditioning adult plant resistance to the Ug99 race group and seedling resistance to races TRTTF abd TTTTF of the stem rust pathogen in wheat landrace Cltr 15026. Plant Dis.101, 496–501.

  • Google Scholar
  • View reference in article

• 7

  BansalU. K.BossoliniE.MiahH.KellerB.ParkR. F.BarianaH. S. (2008). Genetic mapping of seedling and adult plant stem rust resistance in two European winter wheat cultivars. Euphytica164, 821–828. doi: 10.1007/s10681-008-9736-z

  • CrossRef
  • Google Scholar
  • View reference in article

• 8

  BhavaniS.SinghR. P.ArgillierO.Huerta-EspinoJ.SinghS.NjauP.et al. (2011). “Mapping durable adult plant stem rust resistance to the race Ug99 group in six CIMMYT wheats,” in 2011 BGRI technical workshopBorlaug Global Rust Initiative, St. Paul, MN, pp 43–pp 53.

  • Google Scholar
  • View reference in article

• 9

  BromanK. W.WuH.SenŚ.ChurchillG. A. (2003). R/qtl: QTL mapping in experimental crosses. Bioinformatics19, 889–890. doi: 10.1093/bioinformatics/btg112

  • CrossRef
  • Google Scholar
  • View reference in article

• 10

  CarletonM. A. (1905). Lessons from the grain-rust epidemic of 1904. Farmers’ Bulletin No. 219, 1–24.

  • Google Scholar
  • View reference in article

• 11

  ChaoS.RouseM. N.AcevedoM.Szabo-HeverA.BockelmanH.BonmanM. J.et al. (2017). Evaluation of genetic diversity and host resistance to stem rust in USDA NSGC durum wheat accessions. Plant Genome10, (2). doi: 10.3835/plantgenome2016.07.0071

  • CrossRef
  • Google Scholar
  • View reference in article

• 12

  ChapmanJ.MascherM.BuluçA.BarryK.GeorganasE.SessionA.et al. (2015). A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biol.16, 26. doi: 10.1186/s13059-015-0582-8

  • CrossRef
  • Google Scholar

• 13

  ChenS.RouseM. N.ZhangW.ZhangX.GuoY.BriggsJ.et al. (2020). Wheat gene Sr60 encodes a protein with two putative kinase domains that confers resistance to stem rust. New Phytol225, 948-959. doi: 10.1111/nph.16169

  • CrossRef
  • Google Scholar
  • View reference in article

• 14

  ChenS.ZhangW.BolusS.RouseM. N.DubcovskyJ. (2018). Identification and characterization of wheat stem rust resistance gene Sr21 effective against the Ug99 race group at high temperature. PloS Genet.14, e1007287. doi: 10.1371/journal.pgen.1007287

  • CrossRef
  • Google Scholar
  • View reference in article

• 15

  CrossaJ.BurguenoJ.DreisigackerS.VargasM.Herrera-FoesseS. A.LillemoM.et al. (2007). Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics177, 1889–1913. doi: 10.1534/genetics.107.078659

  • CrossRef
  • Google Scholar
  • View reference in article

• 16

  EdaeA. E.PumphreyM. O.RouseM. N. (2018). A genome wide association study of resistance to North American stem rust races in a hexaploid spring wheat (Triticum aestivum L.) breeding germplasm. Front. Plant Sci.9. doi: 10.3389/fpls.2018.00052

  • CrossRef
  • Google Scholar

• 17

  EvansL. T. (1980). Responses to challenge: William Farrer and the making of wheat. J. Aust. Inst. Agric. Sci.46, 3–13.

  • Google Scholar
  • View reference in article

• 18

  GaoL.TurnerM. K.ChaoS.KolmerJ.AndersonJ. A. (2016). Genome wide association study of seedling and adult plant leaf rust resistance in elite spring wheat breeding lines. PloS One11, e0148671. doi: 10.1371/journal.pone.0148671

  • CrossRef
  • Google Scholar
  • View reference in article

• 19

  GloverK. D.RuddJ. C.DevkotaR. N.HallR. G.JinY.OsborneL. E.et al. (2013). Registration of “Forefront” wheat. J. Plant Registrat.7, 184–190. doi: 10.3198/jpr2012.07.0007crc

  • CrossRef
  • Google Scholar
  • View reference in article

• 20

  HaileJ. K.NachitM. M.HammerK.BadeboA.RoderM. S. (2012). QTL mapping of resistance to race Ug99 of Puccinia graminis f. sp. Tritici in durum wheat (Triticum durum Desf.). Mol. Breed.30, 1479–1493. doi: 10.1007/s11032-012-9734-7

  • CrossRef
  • Google Scholar
  • View reference in article

• 21

  HiebertC. W.FetchT. G.ZegeyeT. (2010). Genetics and mapping of stem rust resistance to Ug99 in the wheat cultivar Webster. Theor. Appl. Genet.121, 65–69. doi: 10.1007/s00122-010-1291-z

  • CrossRef
  • Google Scholar
  • View reference in article

• 22

  HundieB.GirmaB.TadesseZ.EdaeE.OliveraP.HailuA. E.et al. (2019). Characterization of ethiopian wheat germplasm for resistance to four puccinia graminis f. sp. tritici races facilitated by single-race nurseries. Plant Dis.103, 2359–2366. doi: 10.1094/PDIS-07-18-1243-RE

  • CrossRef
  • Google Scholar

• 23

  JulianaP.PolandJ.Huerta-EspinoJ.ShresthaS.CrossaJ.Crespo-HerreraL.et al. (2019). Improving grain yield, stress resilience and quality of bread wheat using large-scale genomics. Nat. Genet.51, 1530–1539. doi: 10.1038/s41588-019-0496-6

  • CrossRef
  • Google Scholar

• 24

  KrattingerS.LagudahE.SpielmeyerW.SinghR.Huerta-EspinoJ.McfaddenH.et al. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science323 (5919), 1360–1363.

  • Google Scholar
  • View reference in article

• 25

  KassaM.YouF.HiebertC.PozniakC.FobertP.SharpeA.et al. (2017). Highly predictive SNP markers for efficient selection of the wheat leaf rust resistance gene Lr16. BMC Plant Biol.17, 45. doi: 10.1186/s12870-017-0993-7

  • CrossRef
  • Google Scholar
  • View reference in article

• 26

  KnottD. R. (2000). Inheritance of resistance to stem rust in ‘Triumph 64’ Winter wheat. Crop Sci.40, 1237–1124. doi: 10.2135/cropsci2000.4051237x

  • CrossRef
  • Google Scholar
  • View reference in article

• 27

  KnottD. R. (1989). The wheat rust: Breeding for resistance (Berlin: Spring-Verlag).

  • Google Scholar
  • View reference in article

• 28

  KosgeyZ. C.EdaeE. A.Dill-MackyR.JinY.BulbulaW. D.GemechuA.et al. (2021). Mapping and validation of stem rust resistance loci in spring wheat line CI 14275. Front. Plant Sci.11, 609659. doi: 10.3389/fpls.2020.609659

  • CrossRef
  • Google Scholar
  • View reference in article

• 29

  KumsaT. T.BaenzigerP. S.RouseM. N.GuttieriM.DweikatI.Brown-GuediraG.et al. (2015). Characterization of stem rust resistance in wheat cultivar Gage. Crop Sci.55, 229–239. doi: 10.2135/cropsci2014.05.0348

  • CrossRef
  • Google Scholar
  • View reference in article

• 30

  LincolnS. E.LanderE. S. (1992). Systematic detection of errors in genetic linkage data. Genomics14, 604–610. doi: 10.1016/S0888-7543(05)80158-2

  • CrossRef
  • Google Scholar
  • View reference in article

• 31

  LettaT.MaccaferriM.BadeboA.AmmarK.RicciA.CrossaJ.et al. (2013). Searching for novel sources of field resistance to Ug99 and Ethiopian stem rust races in durum wheat via association mapping. Theor. Appl. Genet.126, 1237–1256. doi: 10.1007/s00122-013-2050-8

  • CrossRef
  • Google Scholar
  • View reference in article

• 32

  LiH. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics27, 2987–2993. doi: 10.1093/bioinformatics/btr509

  • CrossRef
  • Google Scholar
  • View reference in article

• 33

  LiH. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM (Cambridge, MA 02142: Oxford University Press), 1–3. Available at: https://arxiv.org/abs/1303.3997.

  • Google Scholar
  • View reference in article

• 34

  LiH.HandsakerB.WysokerA.FennellT.RuanJ.HomerN.et al. (2009). 1000 Genome Project Data Processing Subgroup. The sequence alignment/map format and SAMtools. Bioinf. (Oxford England)25, 2078–2079. doi: 10.1093/bioinformatics/btp352

  • CrossRef
  • Google Scholar
  • View reference in article

• 35

  LuigN. H. (1983). A survey of virulence genes in wheat stem rust, Puccinia graminis f. sp. tritici. Fortschr. der Pflanzenzuechtung 11. 198PP.

  • Google Scholar
  • View reference in article

• 36

  MagoR.SpielmeyerW.LawrenceG.LagudahE.EllisJ.PryorA. (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. doi: 10.1007/s00122-002-0879-3

  • CrossRef
  • Google Scholar

• 37

  MagoR.ZhangP.VautrinS.ŠimkováH.BansalU.LuoM. C.et al. (2015). The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat. Plants1, 15186. doi: 10.1038/nplants.2015.186

  • CrossRef
  • Google Scholar
  • View reference in article

• 38

  MascherM.MuehlbauerG. D.RokhsarD.ChapmanJ.SchmutzJ.BarryK.et al. (2013). Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ). Plant J.76, 718–727. doi: 10.1111/tpj.12319

  • CrossRef
  • Google Scholar

• 39

  MegerssaS.AmmarK.AcevedoM.Brown-GuediraG.WarrdB.et al. (2020). Multiple-race stem rust resistance loci identified in durum wheat using genome-wide association mapping. Front. Plant Sc.11. doi: 10.3389/fpls/.2020.598509

  • CrossRef
  • Google Scholar
  • View reference in article

• 40

  McIntoshR. A.DubcovskyJ.RogersW. J.MorrisC. F.AppelsR.XiaX. C. (2012). Catalogue of gene symbols for wheat: supplement. Ann. Wheat Newsl58, 259.

  • Google Scholar
  • View reference in article

• 41

  McIntoshR. A.DubcovskyJ.RogersW. J.XiaX. C.RauppW.J. (2020). Catalogue of gene symbols for wheat: supplement. Ann. Wheat Newsl66, 109-128.

  • Google Scholar
  • View reference in article

• 42

  McIntoshR. A.LuigN. H. (1973). Linkage of genes for reaction to Puccinia graminis f. sp. tritici and P. recondita in Selkirk wheat and related cultivars. Aust. J. Biol. Sci.26, 1145–1152. doi: 10.1071/BI9731145

  • CrossRef
  • Google Scholar
  • View reference in article

• 43

  MilusE.MoonD.LeeK. D.MatonE. (2015). Race-specific adult plant resistance in winter wheat to stripe rust and characterization of pathogen virulence patterns. Phytopathology105, 1114–1122. doi: 10.1094/PHYTO-11-14-0305-R

  • CrossRef
  • Google Scholar
  • View reference in article

• 44

  MooreJ. W.Herrera-FoesselS.LanC.SchnippenkoetterW.AyliffeM.Huerta-EspinoJ.et al. (2015). A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet.47, 1494–1498.

  • Google Scholar
  • View reference in article

• 45

  NewcombM.OliveraP. D.RouseM. N.SzaboL. J.JohnsonJ.GaleS.et al. (2016). Kenyan isolates of Puccinia graminis f. sp. tritici from 2008 to 2014: Virulence to SrTmp in the Ug99 race group and implications for breeding programs. Phytopathology106 (7), 729–736 8.

  • Google Scholar
  • View reference in article

• 46

  NiuZ.JiangA.Abu HammadW.OladzadabbasabadiA.XuS. S.MergoumM.et al. (2014). Review of doubled haploid production in durum and common wheat through wheat × maize hybridization. Plant Breed.133, 313–320. doi: 10.1111/pbr.12162

  • CrossRef
  • Google Scholar
  • View reference in article

• 47

  NiuZ.KloindworthD. I.FriesenT. I.ChaoS.JinY.CaiX.et al. (2011). Target introgression of a wheat stem rust resistance gene by DNA marker-assisted chromosome engineering. Genetics187, 1011–1021. doi: 10.1534/genetics.110.123588

  • CrossRef
  • Google Scholar
  • View reference in article

• 48

  NjauP. N.BhavaniS.Huerta-EspinoJ.KellerB.SinghR. P. (2013). Identification of QTL associated with durable adult plant resistance to stem rust race Ug99 in wheat cultivar ‘Pavon 76’. Euphytica190, 33–44. doi: 10.1007/s10681-012-0763-4

  • CrossRef
  • Google Scholar

• 49

  OliveraP.NewcombM.SzaboL. J.RouseM.JohnsonJ.GaleS.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. Phytopathology105 (7),917–928.

  • Google Scholar
  • View reference in article

• 50

  OliveraP. D.SikharulidzeZ.DumbadzeR.SzaboL. J.NewcombM.NatsarishviliK.et al. (2019). Presence of a Sexual Population of Puccinia graminis f. Sp. Tritici in Georgia Provides a Hotspot for Genotypic and Phenotypic Diversity. Phytopathology109 (12), 2152–2160.

  • Google Scholar
  • View reference in article

• 51

  OliveraP. D.VillegasD.Cantero-MartínezC.SzaboL. J.RouseM. N.LusterD. G.et al. (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 pathology71 (4),873–889 17. doi: 10.1111/ppa.13530

  • CrossRef
  • Google Scholar
  • View reference in article

• 52

  PeriyannanS.MooreJ.AyliffeM.BansalU.WangX.HuangL.et al. (2013). The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science80). 341, 786–788. doi: 10.1126/science.1239028

  • CrossRef
  • Google Scholar
  • View reference in article

• 53

  PetersonR. F.CambellA. B.HannahA. E. (1948). A diagrammatic scale for estimating rust intensity of leaves and stem of cereals. Can. J. Res. Sect. C.26, 496–500. doi: 10.1139/cjr48c-033

  • CrossRef
  • Google Scholar
  • View reference in article

• 54

  PolandJ. A.BrownP. J.SorrellsM. E.JanninkJ. L. (2012). Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PloS One7, e32253. doi: 10.1371/journal.pone.0032253

  • CrossRef
  • Google Scholar
  • View reference in article

• 55

  RoelfsA. P.SinghR. P.SaariE. E. (1992). Rust disease of wheat: Concepts and Methods of Disease Management (Mexico: CIMMYT).

  • Google Scholar
  • View reference in article

• 56

  RomayM.MillardM.GlaubitzJ.PeifferJ.SwartsK.CasstevensT. M.et al. (2013). Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol.14, R55. doi: 10.1186/gb-2013-14-6-r55

  • CrossRef
  • Google Scholar
  • View reference in article

• 57

  RouseM. N.NavaI. C.ChaoS.AndersonJ. A.JinY. (2012). Identification of markers linked to the race Ug99 effective stem rust resistance gene Sr28 in wheat (Triticum aestivum L.). Theor. Appl. Genet.125, 877–885. doi: 10.1007/s00122-012-1879-6

  • CrossRef
  • Google Scholar
  • View reference in article

• 58

  RouseM. N.NirmalaJ.JinY.ChaoS.FetchT. G.PretoriusZ. A.et al. (2014a). Characterization of Sr9h, a wheat stem rust resistance allele effective to Ug99. Theor. Appl. Genet.127, 1681–1688. doi: 10.1007/s00122-014-2330-y

  • CrossRef
  • Google Scholar
  • View reference in article

• 59

  RouseM. N.TalbertL. E.SinghD.ShermanJ. D. (2014b). Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.). Theor. Appl. Genet.127, 1549–1559.

  • Google Scholar
  • View reference in article

• 60

  SaintenacN.ZhangW.SalcedoA.RouseM. N.TrickH. N.AkhunovE.et al. (2013). Identification of wheat gene Sr35 that Confers resistance to Ug99 stem rust race group. Science341 (16), 783–786.

  • Google Scholar
  • View reference in article

• 61

  SavaryS.WillocquetL.Pethybridge S. J.EskerP.McRobertsmN.NelsonA. (2019). The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol.3, 430–439. doi: 10.1038/s41559-018-0793-y

  • CrossRef
  • Google Scholar
  • View reference in article

• 62

  SearsE. R.BriggleL. W. (1969). Mapping gene Pm1 for resistance to Erysiphe graminis f. sp. tritici on chromosome 7A of wheat. Crop Sci.9, 96. doi: 10.2135/cropsci1969.0011183X000900010033x

  • CrossRef
  • Google Scholar
  • View reference in article

• 63

  ShewabezE.BekeleE.AlemuA.MugnaiL.TadesseW. (2022). Genetic characterization and genome-wide association mapping for stem rust resistance in spring bread wheat. BMC Genomic Data23, 11. doi: 10.1186/s12863-022-01030-4

  • CrossRef
  • Google Scholar
  • View reference in article

• 64

  SinghS.BowdenR. L. (2010). Molecular mapping of adult-plant race-specific leaf rust resistance gene Lr12 in bread wheat. Mol. Breed28, 137-142. doi: 10.1007/s11032-010-9467-4

  • CrossRef
  • Google Scholar

• 65

  SinghR.Herrera-FoesselS.Huerta-EspinoJ.SinghS.BhavaniS.LanC.et al. (2014). Progress towards genetics and breeding for minor genes-based resistance to Ug99 and other rusts in CIMMYT high-yielding spring wheat. J. Integr. Agric.13, 255–261. doi: 10.1016/S2095-3119(13)60649-8

  • CrossRef
  • Google Scholar

• 66

  SinghR. P.HodsonD. P.JinY.LagudahE. S.AyliffeM. A.BhavaniS.et al. (2015). Emergence and spread of new races of wheat stem rust fungus: Continued threat to food security and prospects of genetic control. Phytopathology105, 872–884. doi: 10.1094/PHYTO-01-15-0030-FI

  • CrossRef
  • Google Scholar

• 67

  SinghR. P.Huerta-EspinoJ.BhavaniS.Herrerra-FoesselS.SinghD.SinghP.et al. (2011). Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica179, 175–186. doi: 10.1007/s10681-010-0322-9

  • CrossRef
  • Google Scholar
  • View reference in article

• 68

  SpindelJ.WrightM.ChenC.CobbJ.GageJ.HarringtonS.et al. (2013). Bridging the genotyping gap: using genotyping by sequencing (GBS) to add high-density SNP markers and new value to traditional bi-parental mapping and breeding populations. Theor. Appl. Genet.126, 2699–2716. doi: 10.1007/s00122-013-2166-x

  • CrossRef
  • Google Scholar
  • View reference in article

• 69

  StakmanE. C. (1955). Progress and problems in plant pathology. Ann. Appl. Biol.42, 22–33. doi: 10.1111/j.1744-7348.1955.tb02407.x

  • CrossRef
  • Google Scholar
  • View reference in article

• 70

  SteuernagelB.PeriyannanS. K.Hernández-PinzónI. H.WitekK.RouseM. N.YuG.et al. (2016). Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat. Biotechnol.34, 652–655. doi: 10.1038/nbt.3543

  • CrossRef
  • Google Scholar
  • View reference in article

• 71

  TheT. T.McIntoshR. A. (1975). Cytogenetical studies in wheat VIII. Telocentric mapping and linkage studies involving Sr22 and other genes in chromosome 7AL. Aust. J. Biol. Sci.28, 531–538. doi: 10.1071/BI9750531

  • CrossRef
  • Google Scholar
  • View reference in article

• 72

  The International Wheat Genome Sequencing Consortium (IWGSC) (2018). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science361, eaar7191. doi: 10.1126/science.aar7191

  • CrossRef
  • Google Scholar
  • View reference in article

• 73

  UpadhyayaN. M.MagoR.PanwarV.Hewitt T.LuoM.Chen J.et al. (2006). JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Ed. KyazmaB. V. (Wageningen, Netherlands).

  • Google Scholar
  • View reference in article

• 74

  WaldronL. R. (1935). Stem rust epidemics and wheat breeding (North Dakota Agricultural College: Agricultural Experiment Station).

  • Google Scholar
  • View reference in article

• 75

  WangS.WongD.ForrestK.AllenA.ChaoS.HuangB. E. (2014). Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol. J.12, 787–796. doi: 10.1111/pbi.12183

  • CrossRef
  • Google Scholar
  • View reference in article

• 76

  WuS.PumpharyM.BaiG. (2009). Molecular mapping of stem-rust resistance gene Sr40 in wheat. Crop Sci.49, 1681–1686.

  • Google Scholar
  • View reference in article

• 77

  YuL. X.Lorenz.A.RutkoskiJ.SinghR. P.BhavaniS.HuertaEspinoJ.et al. (2011). Association mapping and gene-gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor. Appl. Genet.123, 1257–1268. doi: 10.1007/s00122-011-1664-y

  • CrossRef
  • Google Scholar
  • View reference in article

• 78

  YuG.MatnyO.ChampouretN.SteuernagelB.Moscou.M. J.Hernández-PinzónI.et al. (2022). Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62. Nat. Commun.13, 1607. doi: 10.1038/s41467-022-29132-8

  • CrossRef
  • Google Scholar
  • View reference in article

• 79

  YuG.MatnyO.GourdoupisS.NayapuramN.AljedaaniF. R.WangY. L.et al. (2023). The wheat stem rust resistance gene Sr43 encodes an unusual protein kinase. Nat. Genet.55, 921–926. doi: 10.1038/s41588-023-01402-1

  • CrossRef
  • Google Scholar
  • View reference in article

• 80

  ZhangD.BowdenR. L.JinY.CarverB. F.BaiG. (2014). Association analysis of stem rust resistance in U.S. winter wheat. PloS One9, e103747. doi: 10.1371/journal.pone.0103747

  • CrossRef
  • Google Scholar
  • View reference in article

• 81

  ZhangW.ChenaS.AbateaZ.NirmalaJ.RousebM.DubcovskyJ. (2017). Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proc. Natl. Acad. Sci. U.S.A.114, E9483–E9492. doi: 10.1073/pnas.1706277114

  • CrossRef
  • Google Scholar
  • View reference in article

• 82

  ZhangJ.HewittT. C.BoshoffW. H. P.DundasI.UpadhyayaN.LiJ.et al. (2021). A recombined Sr26 and Sr61 disease resistance gene stack in wheat encodes unrelated NLR genes. Nat. Commun.12, 3378. doi: 10.1038/s41467-021-23738-0

  • CrossRef
  • Google Scholar
  • View reference in article

• 83

  ZurnJ. D.NewcombM.RouseM. N.JinY.ChaoS.SthapitJ.et al. (2014). High-density mapping of a resistance gene to Ug99 from the Iranian landrace PI 626573. Mol. Breed.34, 871–881. doi: 10.1007/s11032-014-0081-8

  • CrossRef
  • Google Scholar
  • View reference in article