QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review

During the past decade, numerous studies have been published on molecular mapping of Fusarium head blight (FHB) resistance in wheat. We summarize the relevant findings from 52 quantitative trait loci (QTL) mapping studies, nine research articles on marker-assisted selection and seven on marker-assisted germplasm evaluation. QTL for FHB resistance were found on all wheat chromosomes except chromosome 7D. Some QTL were found in several independent mapping studies indicating that such QTL are stable and therefore useful in breeding programmes. We summarize and update current knowledge on the genetics of FHB resistance in wheat resulting from QTL mapping investigations and review and suggest FHB breeding strategies based on the available information and DNA markers.     

Mapping of QTL for resistance against Fusarium head blight in the winter wheat population Pelikan//Bussard/Ning8026

We report on the identification of FHB ( Fusarium head blight) resistance quantitative trait loci (QTL) of the donor 'G93010' (Bussard/Ning8026) in the background of elite breeding material adapted to the central European climate. With a multiple interval mapping method, two major resistance QTL were identified. Qfhs.lfl-7BS/5BL and Qfhs.lfl-6BS reduced FHB severity individually by 30% and 24%. The combination of both QTL decreased disease severity most effectively by about one half. Qfhs.lfl-6BS is most likely identical to Fhb2 , thus, the effectiveness of Fhb2 in central European breeding material has been validated. Qfhs.lfl-7BS/5BL overlapped with QTL for plant height and heading date. Nevertheless, the selection of lines combining a good FHB resistance level with an acceptable plant height was possible. As the donors of the QTL have probably not yet been utilized in European breeding material, we identified well-adapted lines of the mapping population as valuable donors for marker-assisted breeding programmes.     

Influence of the D genome in conferring resistance to fusarium head blight in spring wheat

Reciprocal crosses were made between resistant hexaploid spring wheat cultivars/lines Sumai 3, Ning8331, and 93FHB21, and susceptible tetraploids Stewart 63 and DT486 to generate 35 chromosome pentaploids. Four heads from each of five F₁ pentaploid plants from each cross were screened with Fusarium graminearum for fusarium head blight (FHB) reaction. No pentaploid was as resistant to FHB as the resistant parents. Pentaploids derived from several crosses were more resistant than the susceptible parents, a few were more susceptible, and all plants from crosses with 93FHB21 failed to survive. Most viable seeds were obtained from the cross Sumai 3 × DT486. From this cross four of the five F₁ pentaploid parents were fertile and 354F₂ seeds derived from these four pentaploids were sown and evaluated for their FHB reaction. The majority of F₂ plants from pentaploids 1 and 3had the visual appearance and level of resistance of Sumai 3, whereas progeny from pentaploids 4 and 5 were more varied morphologically and generally more susceptible. Forty-three of the screened F₂ plants were tested for the presence of specific D chromosomes by wheat microsatellite analysis. There was no relationship between presence/absence of D chromosomes and FHB reaction. Twenty-four lines had all D chromosomes present of which 10 were intermediate-susceptible and 14 were resistant to FHB. Three lines, one resistant and two intermediate, had no D chromosomes. The remainder had between 1 and 6 of the D chromosomes present and ranged from resistant to susceptible in FHB reaction. It appears that FHB resistance is not conferred by the D genome of Sumai 3. This revised version was published online in July 2006 with corrections to the Cover Date.     

奶牛次级性状的微卫星标记与QTL定位研究进展

本文对奶牛繁殖性状（产犊容易度、排卵数）、体型性状（乳房性状、肢蹄性状、体型性状）、健康性状（体细胞和乳房炎抗性）和生产效率性状（生产寿命、泌乳速度等）等四类次级性状QTL定位的研究进展进行了综述。     

Molecular mapping of quantitative trait loci for field resistance to Fusarium head blight in a European winter wheat population

Fusarium head blight (FHB), one of the most destructive diseases of wheat in many parts of the world, can reduce the grain quality due to mycotoxin contamination up to rejection for usage as food or feed. Objective of this study was to map quantitative trait loci (QTL) associated with FHB resistance in the winter wheat population ‘G16‐92’ (resistant)/‘Hussar’. In all, 136 recombinant inbred lines were evaluated in field trials in 2001 and 2002 after spray inoculation with a Fusarium culmorum suspension. The area under disease progress curve was calculated based on the visually scored FHB symptoms. For means across all environments two FHB resistance QTL located on chromosomes 1A, and 2BL were identified. The individual QTL explained 9.7% and 14.1% of the phenotypic variance and together 26.7% of the genetic variance. The resistance QTL on 1A coincided with a QTL for plant height in contrast to the resistance QTL on 2BL that appeared to be independently inherited from morphological characteristics like plant height and ear compactness. Therefore, especially the QTL on 2BL could be of great interest for breeding towards FHB resistance.     

Diallel analysis of Fusarium head blight resistance in genetically diverse winter wheat germplasm

New sources of partial resistance to Fusarium head blight (FHB) in wheat have been identified over the past decade; however, little is known of their breeding value. A 20 parent partial diallel that included resistant genotypes from the U.S., Europe, China and South America was used to evaluate the potential of these sources of resistance as parents in wheat breeding programs. Eight plants replication⁻¹ of each of 190 crosses and 20 parents were point-inoculated with Fusarium graminearum under greenhouse conditions in two replicated experiments. Both general (GCA) and specific combining ability (SCA) were significant. Most of the variance for FHB severity was associated with additive genes; however, estimates for SCA ranged from highly negative to highly positive in both resistant × resistant and resistant × susceptible crosses which suggest that improving FHB resistance through gene pyramiding strategies based on additive genetic variation may be complicated by interaction effects that condition FHB resistance.     

The potential of genomic‐assisted breeding to improve Fusarium head blight resistance in winter durum wheat

Durum wheat is the most important tetraploid wheat mainly used for semolina and pasta production, but is notorious for its high susceptibility to Fusarium head blight (FHB). Our objectives were to identify and characterize quantitative trait loci (QTL) in winter durum and to evaluate the potential of genomic approaches for the improvement of FHB resistance. Here, we employed an international panel of 170 winter and 14 spring durum lines, phenotyped for Fusarium culmorum resistance at five environments. Heading date, plant height and mean FHB severity showed significant genotypic variation with high heritabilities and FHB resistance was negatively correlated with both heading date and plant height. The dwarfing gene Rht‐B1 significantly affected FHB resistance and the genome‐wide association scan identified eight additional QTL affecting FHB resistance, explaining between 1% and 14% of the genotypic variation. A genome‐wide prediction approach yielded only a slightly improved predictive ability compared to marker‐assisted selection based on the four strongest QTL. In conclusion, FHB resistance in durum wheat is a highly quantitative trait and in breeding programmes may best be tackled by classical high‐throughput recurrent phenotypic selection that can be assisted by genomic prediction if marker profiles are available.     

Selection for Fusarium head blight resistance in early generations reduces the deoxynivalenol (DON) content in grain of winter and spring wheat

Fusarium head blight (FHB) results in yield losses and contamination of kernels by mycotoxins, particularly deoxynivalenol (DON). For minimizing DON content in grain, indirect selection methods would increase gains from selection compared to the costly and time‐consuming DON analysis. The aim of this study was to examine whether an early selection for fewer FHB symptoms would lead to a reduced DON content in grain after inoculation with Fusarium culmorum. Starting with a double‐cross derived population of about 1,100 genotypes, 30 F_1:3 genotypes were selected for FHB rating in a two‐step selection in spring wheat with the non‐adapted resistance sources CM82036 and ‘Frontana’. In winter wheat, 30 F_1:2 genotypes were selected out of a double‐cross derived population of about 600 F₁ plants from crosses with German resistance sources (‘Dream’, G16‐92). Selected genotypes were grouped in three categories according to their FHB rating (low, moderate and high) and analysed afterwards for grain DON content. The three groups differed in their DON content illustrating that indirect selection should already be feasible in the earliest generations. Because of the wide genotypic ranges for DON contents within one grouping, a final DON analysis for selected materials is advisable to achieve full selection gain.     

Variation for resistance to Fusarium head blight in spring barley

Fusarium head blight (FHB) is a fungal disease of barley and other cereals, causing substantial yield and quality losses, mainly due to the contamination of the harvest with mycotoxins. We aimed to evaluate genetic variation for resistance to FHB and its association with other plant characters in diverse barley germplasm in order to identify useful lines for resistance breeding. The 143 barley lines consisted of 88 current European spring barley lines and cultivars, 33 accessions from the genebank at IPK Gatersleben, and 22 lines obtained from North American institutions. We conducted artificially inoculated field experiments with Fusarium graminearum Schwabe during two seasons. FHB severity was evaluated by repeated assessment of visual symptoms. On a set of 49 lines several trichothecene mycotoxins were analyzed. Variation for FHB severity was quantitative. The lines with lowest FHB severity were 'CIho 4196' and 'PI 566203'. Also within the European spring barley collection variation for FHB severity was highly significant. There was a significant negative correlation between plant height and FHB severity (r=– 0.55). FHB severity assessed in the field and the amount of deoxynivalenol in the harvested grains were positively correlated (r= 0.87). Several lines with a useful level of FHB resistance were found or confirmed and are recommended as crossing partners.     

Types and components of resistance to Fusarium head blight of wheat

Resistance of wheat to Fusarium head blight caused by Fusarium graminearum and F. culmorum was identified in natural epidemics in 1985 and 1987 as well after artificial inoculations (1983–1988 and 1984–1987). Out of 25 genotypes tested, five were identified with no significant difference in head blight scores, but differing significantly in yield after artificial inoculation, i.e. tolerance differences were detected at different resistance levels. Some genotypes that were similar in yield or head blight scores differed in seed infection severity. Genotypes with awns were more susceptible to head blight when tested under natural epidemic condition in the field; but this trait did not influence head blight severity in artificial inoculations. Dwarf genotypes were more severely infected by head blight than tall genotypes under natural conditions, but genotypes of different plant height classes were similarly susceptible after artificial inoculations. In the early generations of a breeding programme resistance measured by visual evaluation of artificial inoculation is the most important way to screen. If selection of dwarf and awned genotypes cannot be avoided, the higher susceptibility caused by awns and dwarfness under natural epidemic conditions can be decreased by a higher level of physiological resistance, as variability in physiological resistance is available. In later generations, traits like percentage of seed infection or tolerance can be identified by additionally measuring yield reduction. Stability of disease reaction appears to be connected with resistance level, the most resistant genotypes are the most stable, and the most susceptible ones tend to have more unstable reactions in different epidemic conditions.     

Diallel analysis of resistance to head blight caused by Fusarium culmorum in winter wheat

Summary Ten homozygous winter wheat genotypes representing different levels of resistance to Fusarium head blight were crossed in all possible combinations excluding reciprocals. Parents, F₁ and F₂ were inoculated with one pathogenic strain of Fusarium culmorum. Data for head blight, observed 21 days after first inoculation (OBS-2), and for the area under the disease progress curve, based on observations 14, 21 and 28 days after first inoculation (AUDPC), were analyzed. The contrast between parents and F₁ crosses indicated dommance effects of the resistance genes. Diallel analysis according to Griffing's Method 4, Model 1 showed significant general combining ability (GCA) effects for both F₁ and F₂; specific combining ability effects were not significant. With the exception of one genotype for which general performance for Fusarium resistance was not in agreement with its GCA, the resistance to F. culmorum was uniformly transmitted to all offspring, and the parents can be described in terms of GCA. It is suggested that in the progenies with one of the awned lines as parent, one resistance gene was linked with the gene coding for presence of awns, located on chromosome 4B. A single observation date, taken at the right time, was as effective in assessing resistance as the AUDPC.     

The inheritance of resistance to head blight caused by Fusarium culmorum in winter wheat

Summary Crosses were made among ten winter wheat genotypes representing different levels of resistance to Fusarium head blight to obtain F₁ and F₂ generations. Parents, F₁ and F₂ were inoculated with one strain of Fusarium culmorum. Data on incidence of head blight 21 days after first inoculation were analyzed. Broad-sense heritabilities averaged 0.39 and ranged from 0.05 to 0.89 in the individual F₂ families. The joint-scaling test indicated that the inheritance of Fusarium head blight resistance was adequately described by the additive-dominance model, with additive gene action being the most important factor of resistance. With respect to the non-additive effects, dominance of resistance predominated over recessiveness. The number of segregating genes governing resistance in the studied populations was estimated to vary between one and six. It was demonstrated that resistance genes differed between parents and affected resistance differently.     

Characterization of Chinese wheat germplasm for resistance to Fusarium head blight at CIMMYT, Mexico

Fusarium head blight (FHB) poses a challenge for wheat breeders worldwide; there are limited sources of resistance and the genetic basis for resistance is not well understood. In the mid-1980s, a shuttle breeding and germplasm exchange program launched between CIMMYT-Mexico and China, enabled the incorporation of FHB resistance from Chinese bread wheat germplasm into CIMMYT wheat. Most of the Chinese wheat materials conserved in the CIMMYT germplasm bank had not been fully characterized for FHB reaction under Mexican environments, until 2009, when 491 Chinese bread wheat lines were evaluated in a FHB screening nursery in Mexico, and 304 (61.9 %) showed FHB indices below 10 %. Subsequent testing occurred in 2010 for plant height (PH), days to heading (DH), and leaf rust response. In 2012, 140 elite lines with good agronomic types were further evaluated for field FHB reaction and deoxynivalenol (DON) accumulation. Most of the tested lines showed good resistance: 116 (82.9 %) entries displayed FHB indices lower than 10 %, while 89 (63.6 %) had DON contents lower than 1.0 ppm. Significant negative correlations were observed between FHB traits (FHB index, DON content, and Fusarium damaged kernels) and PH, DH, and anther extrusion. A subset of 102 elite entries was selected for haplotyping using markers linked to 10 well known FHB quantitative trait loci (QTL). 57 % of the lines possessed the same 2DL QTL marker alleles as Wuhan 1 or CJ 9306, and 26.5 % had the same 3BS QTL allele as Sumai 3. The remaining known QTL were of low frequency. These materials, especially those with none of the above tested resistance QTL (26.5 %), could be used in breeding programs as new resistance sources possessing novel genes for FHB resistance and DON tolerance.     

Simultaneous selection for yield-related traits and susceptibility to Fusarium head blight in spring wheat RIL population

Fusarium head blight (FHB), caused by the fungal plant pathogen Fusarium, is a fungal disease that occurs in wheat and can cause significant yield and grain quality losses. The present paper examines variation in the resistance of spring wheat lines derived from a cross between Zebra and Saar cultivars. Experiments covering 198 lines and parental cultivars were conducted in three years, in which inoculation with Fusarium culmorum was applied. Resistance levels were estimated by scoring disease symptoms on kernels. In spite of a similar reaction of parents to F. culmorum infection, significant differentiation between lines was found in all the analyzed traits. Seven molecular markers selected as linked to FHB resistance QTLs gave polymorphic products for Zebra and Saar: Xgwm566, Xgwm46, Xgwm389, Xgwm533, Xgwm156, Xwmc238, and Xgwm341. Markers Xgwm389 and Xgwm533 were associated with the rate of Fusarium-damaged kernels (FDK) as well as with kernel weight per spike and thousand kernel weight in control plants. Zebra allele of marker Xwmc238 increased kernel weight per spike and thousand kernel weight both in control and infected plants, whereas Zebra allele of marker Xgwm566 reduced the percentage of FDK and simultaneously reduced the thousand kernel weight in control and infected plants.     

Response to selection in F2 generations of winter wheat for resistance to head blight caused by Fusarium culmorum

Summary In a field trial, F₃ winter wheat lines from plants selected for Fusarium head blight resistance in F₂ generations of a set of crosses, composing a 10×10 half diallel, were tested with their parental lines for resistance to Fusarium culmorum. Selection responses averaged 3.7% on the head blight percentage scale and ranged from –22.0% to 27.1%. Realized heritabilities averaged 0.23 and ranged from 0 to 0.96. Significant transgression for resistance was observed which was suggested to be genetically fixed. It was estimated that resistant parents differed in one or two resistance genes. The possibility of accumulation of resistance genes was shown. The level of head blight resistance of the parental line appeared to be a good indicator of the potential resistance level of its crosses.     

Means and variances for Fusarium head blight resistance of F2-derived bulks from winter triticale and winter wheat crosses

Fusarium head blight (FHB), caused by Fusarium graminearum and Fusarium culmorum, is a devastating disease in cereals. This study was undertaken to estimate progeny means and variances in each of five winter triticale and winter wheat crosses using unselected F₂−derived lines in F₄ or F₅ generation bulked at harvest of the previous generation. Fifty (triticale) and 95 (wheat) progeny per cross were inoculated in two (triticale) or three (wheat) field environments. FHB rating was assessed on a whole-plot basis. Mean disease severities of the parents ranged from 2.3 to 6.4 in triticale and from 3.1 to 6.5 in wheat on a 1-to-9 scale (1 = symptomless, 9 = 100% infected). The midparent values generally resembled the means of their derived progeny. Significant (P < 0.01) genotypic variance was detected within each cross, but genotype × environment interaction and error variances were also high for both crops. Medium to high entry-mean heritabilities (0.6–0.8) underline the feasibility of selecting F₂-derived bulks on a plot basis in several environments. Phenotypic correlation of FHB resistance between generation F_2:4 and F_2:5 was r = 0.87 (P < 0.01) tested across 150 wheat bulks at two locations. Our estimates of selection gain are encouraging for breeders to improve FHB resistance in triticale and wheat by recurrent selection within adapted materials.     

Genetic variation for resistance to Fusarium head blight in bread wheat

Summary During a four year period, a total of 258 winter and spring wheat genotypes were evaluated for resistance to head blight after inoculation with Fusarium culmorum strain IPO 39-01. It was concluded that genetic variation for resistance is very large. Spring wheat genotypes which had been reported to be resistant to head blight caused by Fusarium graminearum were also resistant to F. culmorum. The resistant germplasm was divided into three gene pools: winter wheats from Eastern Europe, spring wheats from China/Japan and spring wheats from Brazil. In 32 winter wheat genotypes in 1987, and 54 winter wheat genotypes in 1989, the percentage yield reduction depended on the square root of percentage head blight with an average regression coefficient of 6.6. Heritability estimates indicated that for selection for Fusarium head blight resistance, visually assessed head blight was a better selection criterion than yield reduction.     

Molecular markers: actual and potential contributions to wheat genome characterization and breeding

The demands for increasing global crop production have prompted the development of new approaches relying on molecular marker technologies to investigate and improve the plant genome. The merits of molecular markers make them valuable tools in a range of research areas. This review describes novel approaches based on modern molecular marker technologies for characterization and utilization of genetic variation for wheat improvement. Large-scale genome characterization by DNA-fingerprinting has revealed no declining trends in the molecular genetic diversity in wheat as a consequence of modern intensive breeding thus opposing the genetic ‘erosion’ hypothesis. A great number of important major genes and quantitative trait loci have been mapped with molecular markers. Marker-assisted selection based on a tight linkage between a marker allele and a gene(s) governing a qualitative or quantitative trait is gaining considerable importance as it facilitates and accelerates cultivar improvement through precise transfer of chromosome regions carrying the gene of interest. The implementations of molecular markers in wheat genotyping, mapping and breeding complemented by specific approaches associated with the complex polyploid nature of common wheat are analyzed and presented.     

Phenotypic selection for high resistance to Fusarium head blight after introgression of quantitative trait loci (QTL) from exotic spring wheat and verification by simple sequence repeat markers a posteriori

Fusarium head blight (FHB) has become an important disease of wheat. We introgressed three resistance quantitative trait loci (QTL) alleles on chromosomes 3B, 5A (from CM82036) and 3A (from ‘Frontana’) into European elite spring wheat and performed phenotypic selection among double‐cross (DC) derived progeny in generations DCF₂ and DCF₃. After recombination and selfing, we analysed 135 phenotypically selected progeny by simple sequence repeat (SSR) markers linked to the QTL. In a second experiment, we forwarded the best 20 progeny for a further two generations by pedigree selection. Progeny were inoculated at two to four locations with Fusarium culmorum and the percentage of infected spikelets per plot was estimated. Both experiments show that phenotypic selection was highly effective. One‐hundred out of 135 phenotypically selected DCF_1:3 progeny had the combination of donor‐QTL alleles (3B + 5A + 3A, 3B + 5A) with the highest effects on FHB resistance. In the subsequent generations, sufficient genotypic variance was detected. The best F_5:7 bulks had similar resistance to the donor CM82036. The FHB rating was reduced in total by 45% points compared to the parental mean. QTL with high effects can be detected solely by phenotypic selection after targeted introgression.