Breeding for Fusarium head blight resistance in wheat—Progress and challenges

Fusarium head blight is among the most extensively studied fungal diseases of wheat and other small grain cereals due to its impact on yield and quality, but particularly due to its potential to produce mycotoxins, which are harmful to humans and animals. Since our last comprehensive review on QTL mapping and marker-assisted selection for FHB resistance in wheat in 2009, numerous studies have been conducted to identify, validate or fine-map resistance QTL. The main aim of this review is to update and summarize findings on FHB resistance breeding of wheat published during the last decade. Furthermore, we compiled a user-friendly table listing FHB resistance QTL data providing a valuable resource for further FHB resistance research. The role of morphological and phenological traits on FHB resistance and possible consequences for resistance breeding are discussed. This review concentrates current knowledge on breeding for FHB resistance and suggests strategies to enhance resistance by deploying molecular breeding methods, including marker-assisted and genomic selection.     

Different quantitative trait loci for <Emphasis Type="Italic">Fusarium</Emphasis> resistance in wheat seedlings and adult stage in the Wuhan/Nyubai wheat population

Fusarium head blight (FHB), caused primarily by Fusarium graminearum (Schwabe), is an important wheat disease. In addition to head blight, F. graminearum also causes Fusarium seedling blight (FSB) and produces the mycotoxin deoxynivalenol (DON) in the grain. The objectives of this study were: (1) to compare the relationship between resistance of wheat lines to F. graminearum in the seedlings and spikes and (2) to determine whether the quantitative trait loci (QTL) for FSB were the same as QTLs for FHB resistance and DON level reported for the same population previously (Somers et al. 2003). There was no relationship between FSB infection and FHB index or DON content across the population. A single QTL on chromosome 5B that controlled FSB resistance was identified in the population; the marker WMC75 explained 13.8% of the phenotypic variation for FSB. This value implies that there may be other QTL with minor effects present, but they were not detected in the analysis. Such a QTL on chromosome 5B was not reported previously among the QTLs associated with FHB resistance and DON level in this population. However, because of recombination, some lines in the present study have Fusarium resistance for both seedling and head blight simultaneously. For example, DH line HC 450 had the highest level of resistance to FSB and FHB and was among the ten lines with lowest DON content. This line is a good candidate to be used as a parent for future crosses in breeding for Fusarium seedling resistance, together with breeding for head blight resistance. This approach may be effective in increasing overall plant resistance to Fusarium.     

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.     

抗赤霉病小麦新品种扬麦18的选育研究

小麦赤霉病是世界范围灾害性小麦病害。为了培育和推广抗赤霉病小麦品种,解决赤霉病对长江中下游地区小麦生产的危害。通过高产育种和抗赤霉病育种技术路线有机结合,运用“综合性状协调点”的观点,培育出了综合性状优良,多年表现既高产稳产又抗赤霉病（MR-R）小麦品种扬麦18,在生产上大面积推广应用。该品种的育成与推广应用初步实现了小麦抗赤霉病育种目标。     

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.     

Confirmation of the relationship between plant height and Fusarium head blight resistance in wheat (<Emphasis Type="Italic">Triticum aestivum</Emphasis> L.) by QTL meta-analysis

Fusarium head blight (FHB) is a serious wheat disease all over the world. In this study, the relationships between plant height (PH) and FHB were investigated across the whole wheat genome by QTL meta-analysis from fifty-six experiments. Coincident meta-QTL (MQTL) for PH and FHB were found on chromosomes 2D, 3A, 4B, 4D and 7A. Rht-B1, Rht-D1, Rht8, MQTLs P7 and P26 were consistent with FHB MQTLs. The meta-analysis results confirmed the negative associations of Rht-B1, Rht-D1, and Rht8 with FHB resistance. The associations of PH and FHB resistance on chromosomes 3A and 7A have not been reported and need further investigation. These regions should be given attention in breeding programs. MQTLs derived from several resistance sources were also observed. Some FHB MQTLs for different types of resistance overlapped. These findings could be useful for improving wheat varieties with resistance to FHB.     

Effect of the Rht-D1 dwarfing locus on Fusarium head blight rating in three segregating populations of winter wheat

Fusarium head blight (FHB) is one of the major fungal diseases in wheat throughout the world. To control FHB severity, breeding genetically resistant varieties is thought to be the most promising strategy. In wheat breeding programmes, short cultivars predominantly carrying the Norin 10 derived semi-dwarfing allele Rht-D1b ( Rht2 ) are preferred worldwide because of higher achievable grain yields and lower risk of lodging. This study was conducted to determine the influence of different alleles at the Rht-D1 locus on FHB reaction. Three winter wheat populations were produced by crossing rather susceptible varieties 'Biscay', 'Pirat' and 'Rubens' carrying mutant-type allele Rht-D1b with the more resistant varieties 'Apache', 'Romanus' and 'History' containing the Rht-D1a wild-type allele ( rht2 ). The 190, 216 and 103 progeny of the F₄-derived populations were assayed for the presence of Rht-D1a or Rht-D1b , plant height, and mean FHB rating after spray inoculation at flowering time with a highly aggressive isolate of Fusarium culmorum . Comparably, high mean FHB severities ranging from 28% to 49% for all population × environment combinations were achieved, with significant genotypic variation for FHB rating and plant height within all populations. Both traits were negatively correlated with r ranging from −0.48 to −0.61 in the complete populations. However, within the subpopulations homozygous for one or other height allele these correlations decreased considerably. The Rht-D1b semi-dwarfing allele resulted in 7–18% shorter plants, depending on the population, but a considerably increased FHB reaction of 22–53%. Nevertheless, significant genotypic variance for FHB resistance remained in all tested Rht-D1b subpopulations indicating that selection for moderately FHB resistant genotypes within agronomically beneficial Rht-D1b genotypes is still feasible.     

Combining ability of resistance to head blight caused by Fusarium culmorum (W.G. Smith) in the F1 of a seven parent diallel of winter wheat (Triticum aestivum L.)

Fusarium head blight (FHB, scab) caused by Fusarium spp. is a widespread disease of cereals causing relevant yield and quality losses and contaminating cereal products with mycotoxins. Breeding resistant cultivars is the method of choice for controlling the disease. Resistance to FHB is a quantitative trait and is most likely governed by several genes. We present the results of an F₁ diallel analysis of FHB resistance involving six resistant and one susceptible European winter wheat genotypes of diverse origin in order to identify promising combinations for the selection of improved cultivars. Parents and F₁s including reciprocals were evaluated for FHB resistance in an artificially inoculated field trial. Two traits were assessed: visual disease symptoms on the heads and the percentage of Fusarium damaged kernels in a harvested sample. General combining ability (GCA) and specific combining ability (SCA) effects were statistically significant for visual symptoms and kernel damage, whereas reciprocal effects were small or not significant. Heterosis for resistance was common, indicating that the parental genotypes possess different resistance genes. Selection of transgressive segregates should be feasible from such heterotic combinations. This revised version was published online in August 2006 with corrections to the Cover Date.     

Utilization of alien genes to enhance Fusarium head blight resistance in wheat – A review

Fusarium head blight (FHB) is a destructive disease of wheat worldwide. Sources of resistance to FHB are limited in wheat. Search for novel sources of effective resistance to this disease has been an urgent need in wheat breeding. Fusarium head blight resistance has been identified in relatives of wheat. Alien chromatin carrying FHB resistance genes has been incorporated into wheat through chromosome addition, substitution, and translocation. Relatives of wheat demonstrate a great potential to enhance resistance of wheat to FHB.     

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.     

Resistance to Fusarium head blight and deoxynivalenol accumulation in wheat

Fusarium head blight (FHB), caused by Fusarium graminearum Schwabe (telomorph =Gibberella zeae (Schw.)), is an important wheat disease world‐wide. Production of deoxynivalenol (DON) by F. graminearum in infected wheat grain is detrimental to livestock and is also a safety concern in human foods. An international collection of 116 wheat lines was evaluated for FHB resistance and concentration of DON in grain. Plants were inoculated with mixed isolates of F. graminearum in the greenhouse by injecting conidia into a single spikelet of each spike and in the field by scattering F. graminearum‐infected wheat kernels on the soil surface. FHB symptoms were evaluated by visual inspection in both the greenhouse and field, and DON was analysed by HPLC. Significant differences in FHB ratings and DON levels were observed among cultivars. In the greenhouse test, visual symptoms varied from no spread of FHB from the inoculated spikelet to spread throughout the spike, and DON levels ranged from trace levels to 283 mg/kg. In the field test, DON ranged from 2.8 to 52 mg/kg. The greenhouse test identified 16 wheat lines from various origins that accumulated less than 2 mg/kg DON. These lines may be useful as sources for breeding wheat cultivars with lower DON levels. Correlation coefficients were significant between FHB symptom ratings, seed quality traits, and DON levels. Thus, the percentage of scabbed spikelets and kernels can be generally used to predict DON levels in harvested wheat grain. In breeding programmes, selection for plants having few scabbed spikelets and scabbed kernels is most likely to result in low DON levels.     

Differential influence of QTL linked to Fusarium head blight,Fusarium-damaged kernel,deoxynivalenol contents and associated morphological traits in a Frontana-derived wheat population

The genetic background of Fusarium head blight (FHB) resistance in the moderately resistant wheat variety Frontana was investigated in the GK Mini Manó/Frontana DH population (n = 168). The plant material was evaluated across seven epidemic environments for FHB, Fusarium-damaged kernel (FDK) and deoxynivalenol (DON) contents caused by two Fusarium species (F. culmorum and F. graminearum). The effects of phenotypic traits such as plant height and heading date were also considered in the experiments. In the population, 527 polymorph markers (DArT, SSR) within a distance of 1,381 cM distance were mapped. The quantitative trait locus/loci (QTL) on chromosomes 4A and 4B demonstrated a significant linkage only with FHB, while QTL on chromosomes 3A, 4B, 7A and 7B were linked to DON accumulation alone. Regions determining all the investigated Fusarium resistance traits were identified on chromosomes 1B, 2D, 3B, 5A, 5B and 6B. The markers in these regions are of the greatest significance from the aspect of resistance breeding. Our results indicate that the genetic background of resistance against FHB, FDK and DON accumulation can differ, and all these traits should be taken under consideration during resistance tests. Moreover, this is the first report on the mapping of Frontana-derived QTL that influence DON accumulation, which is important since the level of DON contamination determines the actions of the food and feed industries. Selection should therefore also focus on this trait by using molecular markers linked to DON content.     

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.     

Alleles on the two dwarfing loci on 4B and 4D are main drivers of FHB‐related traits in the Canadian winter wheat population “Vienna” × “25R47”

Fusarium head blight (FHB), leaf rust and stem rust are among the most destructive wheat diseases. High‐yielding, native disease resistance sources are available in North America. The objective of this study was to map loci associated with FHB traits, leaf rust, stem rust and plant height in a “Vienna”/”25R47” population. DArT markers were used to generate a genetic map, and quantitative trait loci (QTL) analysis was performed by evaluating 113 doubled haploid lines across three environments in Ontario, Canada. FHB resistance QTL were identified on chromosomes 4D, 4B, 2D and 7A, while a QTL for leaf and stem rust resistance was identified on chromosome 1B. The dwarfing alleles of both Rht‐B1 and Rht‐D1 were associated with increased FHB index and DON content.     

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.     

Genome-wide association mapping and genomic prediction of Fusarium head blight resistance,heading stage and plant height in winter rye (Secale cereale)

Rye is a multi-purpose cereal crop grown in Central and Eastern Europe as well as in Western Canada. Fusarium head blight (FHB) is one of the diseases that have a severe negative impact on rye, but knowledge about FHB resistance at the genomic level is totally missing in rye. The objective of this study was to elucidate the genetic architecture of FHB resistance in winter rye using genome-wide association (GWA) mapping complemented by genomic prediction (GP) in comparison with marker-assisted selection (MAS). Additionally, plant height and heading stage were analysed. A panel of 465 S₁-inbred lines of winter rye was phenotyped in three environments (location–year combinations) for FHB resistance by inoculation with Fusarium culmorum and genotyped with a 15k SNP array. Significant genotypic variation and high heritabilities were found for FHB resistance, heading stage and plant height. FHB did not correlate with heading stage, but was moderately correlated with plant height (r = −.52, p < .001) caused by some susceptible short inbred lines. The GWA scan identified 15 QTL for FHB resistance that jointly explained 74% of the genotypic variance. In addition, we detected 11 QTL for heading stage and 8 QTL for plant height, explaining 26% and 14% of the genotypic variance, respectively. A genome-wide prediction approach resulted in 44% higher prediction abilities than marker-assisted selection for FHB resistance. In conclusion, genomic approaches appear promising to improve and accelerate breeding for complex traits in winter rye.     

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.     

Quantitative trait loci for resistance to Fusarium head blight in recombinant inbred wheat lines from the cross Huapei 57-2 / Patterson

Fusarium head blight (FHB), primarily caused by Fusarium graminearum in North America, often results in significant losses in yield and grain quality of wheat (Triticum aestivum L.). Evaluation of FHB resistance is laborious and can be affected by environmental conditions. The development of DNA markers associated with FHB quantitative trait loci (QTL) and their use in breeding programs could greatly enhance selection. The objective of this study was to identify the location and effect of QTLs for FHB resistance using simple sequence repeat (SSR) markers. A population of wheat recombinant inbred lines derived from the cross ‘Huapei57-2’/‘Patterson’ was characterized for type II resistance in one field experiment and two tests under controlled conditions in the greenhouse. Bulked segregant analysis followed by QTL mapping was used to identify the major segregating QTLs. Results indicate that ‘Huapei 57-2’ may have the same resistance allele as ‘Sumai3’ at a QTL located on the short arm of chromosome 3B. Other QTLs of lower effect size were identified on the long arm of 3Band on chromosomes 3A and 5B. Our findings along with results from other studies demonstrate that the effect of the QTL on3BS is large and consistent across a wide range of genetic backgrounds and environments. Pyramiding this QTL with other FHB QTLs using marker-assisted selection should be effective in improving FHB resistance in a wheat breeding program. This revised version was published online in August 2006 with corrections to the Cover Date.     

Combined inoculation of wheat pathogens Zymoseptoria tritici and Fusarium culmorum as a tool for increasing selection intensity in resistance breeding

Resistances to Septoria tritici blotch (STB) and Fusarium head blight (FHB) are important goals in European wheat breeding. We tested 25 winter wheat cultivars differing in their resistance to both diseases by inoculating Zymoseptoria tritici or Fusarium culmorum either separately on different plots or combined on the same plot. Experiments were carried out across three location × year combinations in four variants: non‐inoculated, STB inoculated, FHB inoculated and STB+FHB inoculated at the respective optimal plant stages. On the individually inoculated plots, mean STB severities ranged from 12% to 70% and mean FHB severities from 0.3% to 67% across wheat cultivars. The resistances to STB and FHB were not correlated. Mean disease severities of the respective inoculation variants, STB vs. STB+FHB and FHB vs. STB+FHB, were not significantly different (P > 0.1), and correlations between both inoculation variants were extremely high (r = 0.98) for STB. In conclusion, breeding populations have to be selected for both resistances separately, but phenotyping can be performed on the same plot without ranking differences of the respective resistance.     

Genetic variation and associations involving Fusarium head blight and deoxynivalenol accumulation in cultivated oat (Avena sativa L.)

Resistance in oats (Avena sativa L.) to Fusarium graminearum was phenotyped in 424 spring oat lines from North America and Scandinavia and genotyped with 2974 SNP markers. Fusarium head blight (FHB), deoxynivalenol (DON) content, days to flowering (DTF) and days to yellow maturity (DTM) were scored in field trials in 2011–12. Trials with phenotypic ranges from 1 to 30 ppm, and sufficient accuracy were obtained by an augmented design and spawn inoculation. Discriminant analysis–PCA identified the different gene pools, with overlaps corresponding to known pedigrees and germplasm exchanges. Structure was negligible and GWAS (genomewide association study) was done using mixed linear models in TASSEL or partial least‐squares regression (PLSR). PLSR allows simultaneous analyses of several phenotypes (environments and/or traits) and is a promising tool for GWAS in plants and should be tested in species with sequenced genomes. FHB was associated with phenology QTLs, due to very susceptible early lines from the Midwest. Lines with consistently low DON (and early heading) were identified. Six QTLs for DON were not associated with earliness, including three QTLs reported previously.