Determining the order of resistance genes against Stagonospora nodorum blotch, Fusarium head blight and stem rust on wheat chromosome arm 3BS
© Thapa et al. 2016
Received: 24 November 2015
Accepted: 14 January 2016
Published: 2 February 2016
Stagonospora nodorum blotch (SNB), Fusarium head blight (FHB) and stem rust (SR), caused by the fungi Parastagonospora (synonym Stagonospora) nodorum, Fusarium graminearum and Puccinia graminis, respectively, significantly reduce yield and quality of wheat. Three resistance factors, QSng.sfr-3BS, Fhb1 and Sr2, conferring resistance, respectively, to SNB, FHB and SR, each from a unique donor line, were mapped previously to the short arm of wheat chromosome 3B. Based on published reports, our hypothesis was that Sr2 is the most distal, Fhb1 the most proximal and QSng.sfr-3BS is in between Sr2 and Fhb1 on wheat chromosome arm 3BS.
To test this hypothesis, 1600 F2 plants from crosses between parental lines Arina, Alsen and Ocoroni86, conferring resistance genes QSng.sfr-3BS, Fhb1 and Sr2, respectively, were genotyped and phenotyped for SNB along with the parental lines. Five closely linked single-nucleotide polymorphism (SNP) markers were used to make the genetic map and determine the gene order.
The results indicate that QSng.sfr-3BS is located between the other two resistance genes on chromosome 3BS. Knowing the positional order of these resistance genes will aid in developing a wheat line with all three genes in coupling, which has the potential to provide broad-spectrum resistance preventing grain yield and quality losses.
Fusarium head blight (FHB), stem rust (SR), and Stagonospora nodorum blotch (SNB), incited by the fungi Fusarium graminearum, Puccinia graminis f. sp. tritici, and Parastagonospora (synonyms Phaeosphaeria, Stagonospora) nodorum, respectively, cause yield losses up to 50 % or more in wheat (Triticum aestivum) when favorable environmental conditions enable severe epidemics [1–4]. FHB reduces test weight and lowers the market grade of wheat grain. Symptoms of FHB include bleaching and premature death of cereal spikelets; signs on glumes include white or pink fungal growth that becomes visible under humid conditions . The causal fungus produces various toxins including deoxynivalenol (DON), commonly called vomitoxin, because it induces symptoms of nausea and vomiting in mammals [6, 7]. Grain that is heavily contaminated with DON cannot be sold for food or feed, leading to a complete loss of the crop after harvest. The primary inoculum for the disease comes from airborne sexual (ascospores) or asexual (macroconidia) spores produced on debris from previous crops including stalks and stubble of maize, wheat and other cereals . In addition, insects such as mites and thrips  and wind and rain splash  can transport inoculum from infected crop residue to the anthers extruded from wheat flowers; anthers are the most susceptible tissue and the primary site of most initial infections . Outbreaks of FHB have increased during the past 20 years making it currently one of the most challenging fungal diseases of wheat .
FHB resistance is polygenic , and symptom expression is highly influenced by the environment. Two major types of resistance, I and II, have been identified that can be effective against FHB in wheat . Type I resistance reduces initial infection and is assessed as disease incidence. Type II resistance reduces fungal spread within wheat spikes and is assessed as the number of infected spikelets within a spike after inoculation into a single floret. Fhb1 (also referred to as QFhs.ndsu-3BS) is a major gene for resistance against FHB that is located in the distal region of wheat chromosome arm 3BS . Alsen, a spring wheat cultivar released recently by North Dakota State University, is a source of type II resistance provided by Fhb1 . Molecular marker UMN10 is closely linked to Fhb1 and can be used for marker-assisted selection (MAS) for FHB resistance .
Stem rust is another important fungal disease wherever wheat is grown. Signs of SR appear first on the stem as diamond-shaped pustules, which develop into larger lesions on the plant epidermis . Each pustule contains urediniospores that give infected plants a rust-red color. When plants mature, black teliospores are produced in the pustules, hence the name black stem rust. Many epidemics of SR during the past 80 years have reduced wheat yields by 50 % in the Great Plains of the United States [1–3]. SR is managed typically with host resistance, but the pathogen has shown a remarkable ability to overcome introduced resistance genes. The resulting “boom and bust” cycles have led to periodic epidemics when resistance breaks down , emphasizing the need for a focus on SR resistance in wheat breeding programs. Interest in SR has increased since 1998 with the discovery of race TTKSK (also known as Ug99) in eastern Africa . This race is concerning because it overcomes Sr31, a resistance gene introduced into wheat from rye . This gene previously provided resistance to 90 % of the world’s wheat crop. Race TTKSK is currently spreading across Africa, Asia and the Middle East and poses a major threat to global wheat production .
SR resistance gene Sr2 provides broad-spectrum protection against this disease . This gene was transferred from tetraploid emmer wheat (Triticum dicoccum) into the susceptible bread wheat cultivar ‘Marquis’ during the 1920s . Sr2 has a recessive inheritance and provides adult-plant resistance [21, 22] against all known pathotypes of stem rust including race TTKSK (Ug99) . However, it only confers partial resistance and does not provide sufficient protection under heavy disease pressure . Selection for Sr2 in the field is difficult for plant breeders due to its recessive inheritance and relatively weak phenotype . However, pseudo black chaff, a physiological trait that causes pigmentation of stems and/or glumes, is genetically linked and can provide a surrogate for direct selection on Sr2 .
SNB is another major yield-reducing foliar and glume disease of wheat. SNB has increased in importance worldwide following the introduction and widespread production of dwarf and semi-dwarf wheat lines , and by growing wheat lines that are susceptible to toxins produced by the SNB pathogen [27, 28]. In addition, recent adoption of cultural practices such as minimum-tillage agriculture [29–31] and increased use of high-nitrogen fertilizers have increased the impact of this disease. The diagnostic symptoms of the leaf-blotch phase of the disease are chlorotic lesions on the lower leaves that initially are red-brown in color with a yellow halo and eventually develop into tan, lens-shaped lesions containing dark specks of pycnidia producing the asexual pycnidiospores . The glume-blotch phase of the disease occurs later when heads and grains are infected by conidia released from pycnidia and spread by rain-splash dispersal .
Several quantitative trait loci (QTL) for resistance to SNB have been identified that provide partial resistance against the disease in wheat [33–38]. SNB resistance gene QSng.sfr-3BS is present in parental line Arina and has been mapped to wheat chromosome arm 3BS . Arina is a Swiss winter wheat cultivar with excellent resistance to SNB that has been planted to more than 40 % of the Swiss wheat acreage since 1985 . However, the map location of QSng.sfr-3BS relative to those for Fhb1 and Sr2 is not known definitively and all three genes currently are in different genetic backgrounds, complicating their use in wheat-improvement programs.
The objective of this analysis was to determine the order of resistance genes Fhb1, Sr2 and QSng.sfr-3BS to test the hypothesis that QSng.sfr-3BS occurs between the other two genes on wheat chromosome arm 3BS, with the long-term goal to obtain all three genes in coupling. The first objective was achieved by crossing three parental lines with resistance to Fhb1, Sr2 or QSng.sfr-3BS to combine the resistance genes into a single background. A segregating F2 population of 1600 plants was genotyped with SNP markers to validate the presence of the resistance genes and to determine their order. The entire F2 progeny set also was phenotyped for resistance to SNB to test the associations between disease resistance and molecular markers.
Analysis of previously published linkage maps
Resistance genes and/or QTL for various qualitative and quantitative traits located in the 3BS region of the wheat genome were identified through literature searches. Linkage arrangements and map locations were obtained from previously published sources [23, 40–45] and a probable genetic linkage map was constructed using MergeMap , a free software tool for combining data from multiple sources into a single linkage map based on genetic distances from shared markers.
Mapping population development
Summary information of the three wheat cultivars contributing genes for resistance against Stagonospora nodorum blotch, Fusarium head blight and stem rust and summary of simple-sequence repeat markers linked to each resistance gene used for genotyping parental wheat lines during the initial analysis of 400 F2 progeny (Xgwm389) and for all progeny sets (Xumn10)
Approximately 400 F2 seeds in a plastic tray and 20 seeds of winter wheat cultivar Arina in a 15.24-cm pot were planted, dormancy was broken, seedlings were vernalized and transplanted during the spring of 2012 as described above. The F2 seeds were vernalized for only 2 weeks and then the seedlings were transplanted into 10-cm-diameter pots and placed in a greenhouse. Day length, temperature and fertilization were as described above. The pot with the Arina seeds was kept at 2.8 °C for 65 days for vernalization as required to stimulate flowering of winter wheat. All 400 F2 plants were genotyped with molecular markers linked to Fhb1 and Sr2 (Table 1) to identify those progeny that were likely to be homozygous for both resistance genes. Two plants were identified as double homozygotes and were crossed to the SNB-resistant winter wheat cultivar Arina containing QSng.sfr-3BS.
The F1 seeds from this cross were planted, dormancy was broken, seedlings were vernalized for 65 days and transplanted during summer of 2012 as described above. Day length, temperature and fertilization with Miracle-Gro were as described above. The F1 plants were allowed to self pollinate and spikes were covered with glycine bags during flowering to avoid cross contamination.
The resulting F2 population, its parents and Chinese Spring as a susceptible control were evaluated for SNB resistance in a greenhouse at Purdue University during January of 2013. Seeds of the F2 lines (N = 1600) and parents (N = 20/parent) were planted in 67-cm long × 34-cm wide × 6-cm deep Styrofoam seedling transplant trays with 128 cells. One seed was planted per cell to allow the plants to be genotyped before transplanting. Following vernalization at 3 °C for 75 days, seedlings were transplanted into 10-cm-diameter plastic pots, one seedling per pot during March of 2013. Day length was 11 h for 14 days (22 °C day, 20 °C night), which was increased to 14 h for 7 days (28 °C day, 24 °C night), and then to 16 h (28 °C day, 24 °C night) until maturity. Plants were watered as needed and fertilized with Miracle-Gro twice before transplanting and once with 12-12-12 fertilizer after transplanting.
Disease screening for SNB resistance in a greenhouse
List of Kompetitive Allele-Specific PCR (KASPar) single-nucleotide polymorphism (SNP) markers and their sequences used to genotype 1600 F2 progeny derived from a cross of Arina (Qsng-sfr-3BS) by two F2 progeny from a cross between Alsen and Ocoroni86 that were homozygous for the molecular markers linked to the Fhb1 (Alsen) and Sr2 (Ocoroni86) resistance genes
Linkage and QTL analyses
The genetic linkage map was constructed using the genotypic data of the F2 progeny derived from the cross involving all three resistance genes with the software package JoinMap 3.0 . The Kosambi mapping function was used to calculate the map distances . The orders of the resistance genes within the linkage group were determined via the maximum likelihood (ML) mapping algorithm with an LOD of 10. The genetic map for QTL analysis was constructed using five SNP markers. The phenotypic data for SNB along with genotypic data collected from the F2 progeny after the second cross were utilized for QTL analysis. The QTL for SNB resistance was identified via interval mapping in Windows QTL Cartographer version 2.5 .
Linkage predictions from previously published maps
To combine the three genes from different parents into a single segregating population, crosses were made initially to identify plants having the Fhb1 and Sr2 genes present in the two spring wheat parents linked in coupling. Among 400 F2 seedlings tested from the cross Alsen (Fhb1) × Ocoroni86 (Sr2), two were homozygous for the molecular marker Xumn10 that is closely linked to Fhb1 and markers Xgwm389 and Xglk683 that flank the Sr2 resistance gene. The linkage distance between loci Xumn10 and Xgwm389 was 16.6 cM. Since the marker analyses indicated that these plants should be homozygous for both resistance genes, they were crossed with Arina (QSng.sfr-3BS) to develop a population in which all three resistance genes and the linked molecular markers would segregate. A population of F1 seeds was created from Arina crossed with each double homozygote and maintained separately. The population with the highest number of F2 seeds (approximately 1600) was used to determine the gene order and to make the genetic linkage map.
Genetic linkage map
In total, 119 simple-sequence repeat (SSR) and SNP loci were screened to identify polymorphic markers in the distal region of chromosome arm 3BS. However, it was difficult to identify markers with different alleles from all three parents. The SSR markers Xumn10 and Xgwm389 (Table 1) have been reported as closely linked to Fhb1 and Sr2, respectively, and were used to track the genes of interest after every cross and every generation except for the F2 from the second cross, where KASpar markers amenable to high-throughput genotyping were used.
QTL analysis for Stagonospora nodorum blotch resistance
Markers linked to the quantitative trait locus associated with Stagonospora nodorum blotch resistance detected by single-marker analysis of 1600 F2 progeny derived from a cross of Arina (QSng.sfr-3BS) by an F2 progeny from a cross between Alsen and Ocoroni86 that was homozygous for the molecular markers linked to the Fhb1 (Alsen) and Sr2 (Ocoroni86) resistance genes
QTL analysis performed for Stagonospora nodorum blotch resistance by interval mapping of F2 progeny derived from a cross of Arina (QSng.sfr-3BS) by an F2 progeny from a cross between Alsen and Ocoroni86 that was homozygous for the molecular markers linked to the Fhb1 (Alsen) and Sr2 (Ocoroni86) resistance genes
The main objectives of this analysis were to determine the order of resistance genes Fhb1, Sr2 and QSng.sfr-3BS on wheat chromosome arm 3BS and to move all three genes into a common genetic background. Analyses using shared markers on previously published linkage maps with MergeMap suggested that the SR resistance gene (Sr2) is the most distal, the FHB resistance gene (Fhb1) is the most proximal and the P. nodorum resistance gene (QSng.sfr-3BS) is between Sr2 and Fhb1 on the short arm of chromosome 3B of wheat. This hypothesis was supported by analysis of the 1600 F2 progeny that segregated for markers linked to all three resistance genes. Comparison of our linkage map and a recently published map of the Fhb1-Sr2 region of chromosome 3BS based on a Ning7840/Clark BC7F7 population  supported this map order (Fig. 4). The Bernardo et al. map in 2012  has loci Xsnp3BS-2, Xsnp3BS-3, Xumn10, and Xsnp3BS-9 in common with ours and all were in the same order with similar distances in both maps.
The long-term goal of this research is to combine all three genes in coupling to develop a linkage block on 3BS with resistance to different fungal pathogens. This is of particular interest because Fhb1 is the most commonly deployed gene for resistance against F. graminearum, Sr2 is effective against SR race TTKSK (Ug99), and SNB is common in most wheat-growing areas worldwide. The gene order was not known when the project was initiated, and the most successful cross among the original three parents was between the spring wheat cultivars Alsen and Ocoroni86, having the most distal (Fhb1) and most proximal (Sr2) genes, respectively. From a population of 400 F2 individuals, we were able to recover two plants homozygous for marker alleles associated with both resistance genes, indicating that recombination had occurred in both gametes for each plant. The relative ease with which plants homozygous for Fhb1 and Sr2 were recovered allowed for rapid generation of a population segregating for all three loci. However, this then required development of a very large population when generating the final genetic linkage map utilizing genotypic data from F2 progeny from a cross with Fhb1 and Sr2 in coupling and QSng.sfr-3BS in repulsion.
Previously identified molecular markers that are tightly linked to Sr2 and Fhb1 segregating in the large F2 population were used as proxies for these resistance genes, and phenotyping was done with SNB only to avoid any confounding effects that might have arisen if all three diseases had been tested on the same plants. The histogram of SNB phenotypes was skewed towards susceptibility, which might reflect the assay conditions as well as inheritance of disease resistance. To ensure adequate infection, spikes were inoculated with freshly prepared inoculum and the spikes were covered for 3 days. These highly permissive conditions may have increased the severity of the disease and caused heterozygotes to have a susceptible phenotype. Unfortunately, the SNP locus (g1130) that was most closely linked to QSng.sfr-3BS behaved as a dominant marker in the cross so it was not possible to distinguish the large number of heterozygotes from either homozygote. This precluded an analysis to test how well the marker predicted the phenotype by itself.
It was difficult to determine the exact position of the QSng.sfr-3BS gene in the QTL analysis due to the small number of segregating loci, which spanned a narrow genetic window of only 10 cM. Single-marker analysis showed that all five SNP markers were highly significant, indicating the presence of a SNB resistance QTL in this region of 3BS. A highly significant QTL peak (Fig. 5) was identified approximately 1 cM proximal to the predictive SNP marker g01130 for SNB. This locus was most closely associated with QSng.sfr-3BS, which was also supported by Shatalina et al. in 2013 . Markers Xsnp3BS-2 for Sr2 and Xumn10 for Fhb1 were placed on either side of locus g01130. Therefore, it seems most likely that the first peak on the interval mapping analysis corresponds with QSng.sfr-3BS, approximately 1 cM proximal to g01130 and about 4 cM distal to the marker for Fhb1. Inclusion of additional markers proximal to Xsnp3BS-9 that are not associated with the resistance phenotype would anchor the QTL analysis and provide better definition to the peak; the wide peak with all markers significantly associated with resistance in Fig. 5 is most likely an artifact of an overly narrow genetic window. As expected for these distances, recombinant plants that appeared to have both Sr2 and QSng.sfr-3BS were recovered at a lower frequency than those with Fhb1 and QSng.sfr-3BS in coupling. In total, five recombinant plants with QSng.sfr-3BS in coupling with either Fhb1 or Sr2 were identified in the F2 population. Those recombinant progeny with two resistance genes in coupling can be used in further crosses to obtain recombinants having all three resistance genes in a single linkage block.
The low level of phenotypic variation explained by marker locus g01130 as shown in Tables 3 and 4 could be due to the low number of polymorphic markers and quality of phenotypic data collected. As the study was conducted on an F2 population, phenotypic data were taken from single plants. Lack of replication increases error variance , which might have decreased the overall phenotypic variation (Tables 3 and 4). This could be addressed by increasing the marker density to increase the power to detect linked QTL , and by phenotyping F2:3 populations so that multiple plants can be phenotyped per entry. In addition, a recent study by Shatalina et al. in 2013  suggested the presence of two genetically distinct SNB resistance loci in the QSng.sfr-3BS target interval. Marker loci sun2 and g01130 were tightly linked and were located between these two loci in the telomeric region of chromosome 3BS [55, 58]. After comparing our genetic map and two of the genetic maps from Shatalina et al. in 2013 [55, 58], SNB resistance locus QSng.sfr-3BS from our study was located distal to marker locus sun2, consistent with gene A in Shatalina et al. in 2013 . These results indicate a high genetic complexity to the SNB resistance controlled by QSng.sfr-3BS. Presence of two linked resistance loci also could be the reason behind the wide, highly significant QTL (Fig. 5). This hypothesis could be tested by adding more markers and by scoring F3 families for resistance phenotype.
Knowing the positional order of these resistance genes will enable the development of a wheat line with all three genes in coupling to provide durable and broad-spectrum resistance against multiple major diseases of wheat. The tight linkage between Sr2, QSng.sfr-3BS, and Fhb1 shown from this study suggests that, once obtained, it should be relatively easy to maintain this linkage block in a breeding program. Previously published linkage maps have reported that leaf rust resistance gene Sv2 is in the same general region and likely occurs between Fhb1 and QSng.sfr-3BS (Fig. 2). Yellow rust (stripe rust) resistance gene Yrns-B1 was reported on chromosome arm 3BS , proximal to the other genes (Fig. 2). Therefore, it may be possible in the future to combine Sv2 and Yrns-B1 with the other three genes in coupling for a linkage block with resistance against five important fungal pathogens of wheat.
RT, KAW, HWO and SBG designed the experiment. RT, KAW and SBG collected phenotypic data. RT, GB and MM collected genotypic data. RT, GB and MM analyzed the data and interpreted the results. RT, GB, HWO and SBG wrote the manuscript. All authors read and approved the final manuscript.
We thank Ian Thompson for his assistance in developing the P. nodorum cultures and for helping with some of the inoculations. We thank Aaron D. Lubelski for his assistance with phenotyping and computerized graphics. This project was supported by a research grant from the Agriculture and Food Research Initiative (No. 2010-85117-20607) from the USDA National Institute of Food and Agriculture and by USDA CRIS project 3602-22000-015-00D.
Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the U.S. Department of Agriculture.
The authors declare that they have no competing interests.
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