Deoxynivalenol (DON) is a toxicologically relevant trichothecene mycotoxin frequently found in cereal products. It is a virulence factor produced by the plant pathogen Fusarium graminearum during cereal crop infections. Investigating plant defense mechanisms is crucial for understanding plant resistance to F. graminearum and identifying new biocatalysts for DON detoxification. Previous studies identified DON-thiol adducts in cereal samples, indicating partial DON detoxification by glutathione transferases (GSTs). DON possesses two electrophilic centers for thiol conjugation, resulting in either epoxide opening at C13 or Michael addition at C10. At present, information on plant GSTs that catalyze these reactions is limited. In this study, Fusarium-inducible wheat GSTs were identified by analyzing the transcriptome of Fusarium-infected wheat heads. Twelve highly induced genes of the tau and phi GST classes were heterologously expressed and purified, biochemically characterized with model substrates, and assayed for activity with DON. Use of LC-MS showed that four of the selected tau class GSTs conjugated DON to GSH by epoxide opening (DON-13-GSH) and/or the reversible Michael addition reaction (DON-10-GSH). The crystal structure of a wheat GST (herein designated "TaGST-10") in complex with DON-13-GSH was solved at a resolution of 2.3 Å and provided insights into the binding of DON at the active site of tau class GSTs. Our results corroborate the hypothesis that enzyme-catalyzed, GSH-mediated DON detoxification may be involved in plant response to Fusarium infection.

AbstractFusarium head blight (FHB), mainly caused by Fusarium graminearum and Fusarium culmorum, is a major wheat disease. Significant efforts have been made to improve resistance to FHB in bread wheat (Triticum aestivum), but more work is needed for durum wheat (Triticum turgidum spp. durum). Bread wheat has ample genetic variation for resistance breeding, which can be readily exploited, while durum wheat is characterized by higher disease susceptibility and fewer valuable resistance sources. The Wheat Initiative – Expert Working Group on Durum Wheat Genomics and Breeding has promoted a scientific discussion to define the key actions that should be prioritized for achieving resistance in durum wheat comparable to that found in bread wheat. Here, a detailed state of the art and novel tools to improve FHB resistance in durum are presented, together with a perspective on the next steps forward. A meta‐analysis grouping all quantitative trait loci (QTL) associated with FHB resistance in both bread and durum wheat has been conducted to identify hotspot regions that do not overlap with Rht alleles, which are known to negatively correlate with FHB resistance. A detailed list of QTL related to FHB resistance and deoxynivalenol contamination and durum lines carrying different sources of FHB resistance are provided as a strategic resource. QTL, closely linked markers and durum wheat lines carrying the useful alleles, can be selected to design an effective breeding program. Finally, we highlight the priority actions that should be implemented to achieve satisfactory resistance to FHB in durum wheat.

Fusarium head blight (FHB) is a disease that affects all cereals worldwide. This includes emmer wheat (Triticum turgidum ssp. dicoccum), the ancestor of durum and bread wheat. We screened 143 cultivated emmer genotypes from a breeding program and gene bank collections for FHB severity at 2 locations over 2 years. Due to the high negative correlation between FHB severity and heading date (HD) (r = -0.65, p < 0.001), plot-level FHB scores were corrected for HD before further analysis (FHBcorr). Genetic variation for FHB severity was high, ranging from 2.15 to 8.33 on a 1-9 scale. Twelve genotypes carried the semi-dwarfing Rht-B1b marker allele, which reduced plant height by 32 cm but increased FHB severity by 20%. Genome-wide association study detected seven quantitative trait nucleotides (QTNs) for FHBcorr and three QTNs for plant height. The most important QTN for both traits was located on chromosome 4B, explaining 50.9% and 15.8% of the phenotypic variation in plant height and FHBcorr, respectively, and was localized near the semi-dwarfing Rht-B1 locus. Three other large-effect loci for FHBcorr were found on chromosomes 5B and 7B. In total, 72.6% of phenotypic variation was explained by all markers. The use of Rht-B1b in emmer breeding has a high effect on plant height but would entail the introgression of potent FHB-resistance from either native or exotic sources.

Plant BreedingVolume 143, Issue 1 p. 1-1 EDITORIAL Special Issue on Breeding and breeding research for resistance to Fusarium diseases in cereals David A. van Sanford, David A. van Sanford University of Kentucky, Lexington, Kentucky, USASearch for more papers by this authorHermann Buerstmayr, Hermann Buerstmayr University of Natural Resources and Life Sciences, Tulln, AustriaSearch for more papers by this authorZhengqiang Ma, Zhengqiang Ma Nanjing Agricultural University, Nanjing, ChinaSearch for more papers by this authorThomas Miedaner, Thomas Miedaner State Plant Breeding Institute, University of Hohenheim, Stuttgart, GermanySearch for more papers by this authorBarbara Steiner, Barbara Steiner University of Natural Resources and Life Sciences, Tulln, AustriaSearch for more papers by this author David A. van Sanford, David A. van Sanford University of Kentucky, Lexington, Kentucky, USASearch for more papers by this authorHermann Buerstmayr, Hermann Buerstmayr University of Natural Resources and Life Sciences, Tulln, AustriaSearch for more papers by this authorZhengqiang Ma, Zhengqiang Ma Nanjing Agricultural University, Nanjing, ChinaSearch for more papers by this authorThomas Miedaner, Thomas Miedaner State Plant Breeding Institute, University of Hohenheim, Stuttgart, GermanySearch for more papers by this authorBarbara Steiner, Barbara Steiner University of Natural Resources and Life Sciences, Tulln, AustriaSearch for more papers by this author First published: 09 January 2024 https://doi.org/10.1111/pbr.13158Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat No abstract is available for this article. Volume143, Issue1Special Issue:Breeding and breeding research for resistance to Fusarium diseases in cereals. Hybrid rice breeding, dedicated to Prof. Longping Yuan (1930–2021).February 2024Pages 1-1 RelatedInformation

Fusarium head blight (FHB) is one of the most devastating diseases of wheat and can lead to significant yield losses as well as a contamination of the crop with mycotoxins that are a major concern in cereal-based food and feed products. The aims of this study were thus to investigate the relationship between resistance against multiple Fusarium species and to assess the potential of an indirect phenotypic and genomic selection for the resistance against the accumulation of several mycotoxins in wheat. Strong phenotypic and genetic correlations between the mycotoxin contents, FHB severity and FHB-associated traits were observed, irrespective of if traits were assessed in trials inoculated with a DON or HT-2/T-2 producing Fusarium species. A multi-stage phenotypic or genomic selection with low anther retention being used for an indirect selection among early generation selection candidates, followed by an evaluation of the pre-selected set in disease nurseries, and lastly by assessing the mycotoxin content of the most promising genotypes is suggested as a suitable strategy to breed for wheat cultivars with reduced risk of mycotoxin accumulation.

FHB resistance of durum wheat was improved by introgression of Fhb1 and resistance genes from emmer wheat and by selection against adverse alleles of elite durum wheat. Durum wheat is particularly susceptible to Fusarium head blight (FHB) and breeding for resistance is impeded by the low genetic variation within the elite gene pool. To extend the genetic basis for FHB resistance in durum wheat, we analyzed 603 durum wheat lines from crosses of elite durum wheat with resistance donors carrying resistance alleles derived from Triticum aestivum, T. dicoccum and T. dicoccoides. The lines were phenotyped for FHB resistance, anthesis date, and plant height in artificially inoculated disease nurseries over 5 years. A broad variation was found for all traits, while anthesis date and plant height strongly influenced FHB severities. To correct for spurious associations, we adjusted FHB scorings for temperature fluctuations during the anthesis period and included plant height as a covariate in the analysis. This resulted in the detection of seven quantitative trait loci (QTL) affecting FHB severities. The hexaploid wheat-derived Fhb1 QTL was most significant on reducing FHB severities, highlighting its successful introgression into several durum wheat backgrounds. For two QTL on chromosomes 1B and 2B, the resistance alleles originated from the T. dicoccum line Td161 and T. dicoccoides accessions Mt. Hermon#22 and Mt. Gerizim#36, respectively. The other four QTL featured unfavorable alleles derived from elite durum wheat that increased FHB severities, with a particularly negative effect on chromosome 6A that simultaneously affected plant height and anthesis date. Therefore, in addition to pyramiding resistance genes, selecting against adverse alleles present in elite durum wheat could be a promising avenue in breeding FHB-resistant durum wheat.

SummaryAegilops tauschii is the diploid progenitor of the wheat D subgenome and a valuable resource for wheat breeding, yet, genetic analysis of resistance against Fusarium head blight (FHB) and the major Fusarium mycotoxin deoxynivalenol (DON) is lacking. We treated a panel of 147 Ae. tauschii accessions with either Fusarium graminearum spores or DON solution and recorded the associated disease spread or toxin‐induced bleaching. A k‐mer‐based association mapping pipeline dissected the genetic basis of resistance and identified candidate genes. After DON infiltration nine accessions revealed severe bleaching symptoms concomitant with lower conversion rates of DON into the non‐toxic DON‐3‐O‐glucoside. We identified the gene AET5Gv20385300 on chromosome 5D encoding a uridine diphosphate (UDP)‐glucosyltransferase (UGT) as the causal variant and the mutant allele resulting in a truncated protein was only found in the nine susceptible accessions. This UGT is also polymorphic in hexaploid wheat and when expressed in Saccharomyces cerevisiae only the full‐length gene conferred resistance against DON. Analysing the D subgenome helped to elucidate the genetic control of FHB resistance and identified a UGT involved in DON detoxification in Ae. tauschii and hexaploid wheat. This resistance mechanism is highly conserved since the UGT is orthologous to the barley UGT HvUGT13248 indicating descent from a common ancestor of wheat and barley.

Durum wheat is more susceptible to Fusarium head blight (FHB) than other types or classes of wheat. The disease is one of the most devastating in wheat; it reduces yield and end-use quality and contaminates the grain with fungal mycotoxins such as deoxynivalenol (DON). A panel of 265 Canadian and European durum wheat cultivars, as well as breeding and experimental lines, were tested in artificially inoculated field environments (2019–2022, inclusive) and two greenhouse trials (2019 and 2020). The trials were assessed for FHB severity and incidence, visual rating index, Fusarium-damaged kernels, DON accumulation, anthesis or heading date, maturity date, and plant height. In addition, yellow pigment and protein content were analyzed for the 2020 field season. To capture loci underlying FHB resistance and related traits, GWAS was performed using single-locus and several multi-locus models, employing 13,504 SNPs. Thirty-one QTL significantly associated with one or more FHB-related traits were identified, of which nine were consistent across environments and associated with multiple FHB-related traits. Although many of the QTL were identified in regions previously reported to affect FHB, the QTL QFhb-3B.2, associated with FHB severity, incidence, and DON accumulation, appears to be novel. We developed KASP markers for six FHB-associated QTL that were consistently detected across multiple environments and validated them on the Global Durum Panel (GDP). Analysis of allelic diversity and the frequencies of these revealed that the lines in the GDP harbor between zero and six resistance alleles. This study provides a comprehensive assessment of the genetic basis of FHB resistance and DON accumulation in durum wheat. Accessions with multiple favorable alleles were identified and will be useful genetic resources to improve FHB resistance in durum breeding programs through marker-assisted recurrent selection and gene stacking.

Research needs a balance of risk-taking in "breakthrough projects" and gradual progress. For building a sustainable knowledge base, it is indispensable to provide support for both.

Research needs a balance of risk‐taking in “breakthrough projects” and gradual progress. For building a sustainable knowledge base, it is indispensable to provide support for both.

Aegilops tauschii , the diploid wild progenitor of the D subgenome of bread wheat, is a reservoir of genetic diversity for improving bread wheat performance and environmental resilience. Here we sequenced 242 Ae. tauschii accessions and compared them to the wheat D subgenome to characterize genomic diversity. We found that a rare lineage of Ae. tauschii geographically restricted to present-day Georgia contributed to the wheat D subgenome in the independent hybridizations that gave rise to modern bread wheat. Through k -mer-based association mapping, we identified discrete genomic regions with candidate genes for disease and pest resistance and demonstrated their functional transfer into wheat by transgenesis and wide crossing, including the generation of a library of hexaploids incorporating diverse Ae. tauschii genomes. Exploiting the genomic diversity of the Ae. tauschii ancestral diploid genome permits rapid trait discovery and functional genetic validation in a hexaploid background amenable to breeding.

Background Fusarium head blight (FHB) is a devastating disease of wheat worldwide. Resistance to FHB is quantitatively controlled by the combined effects of many small to medium effect QTL. Flowering traits, especially the extent of extruded anthers, are strongly associated with FHB resistance. Results To characterize the genetic basis of FHB resistance, we generated and analyzed phenotypic and gene expression data on the response to Fusarium graminearum (Fg) infection in 96 European winter wheat genotypes, including several lines containing introgressions from the highly resistant Asian cultivar Sumai3. The 96 lines represented a broad range in FHB resistance and were assigned to sub-groups based on their phenotypic FHB severity score. Comparative analyses were conducted to connect sub-group-specific expression profiles in response to Fg infection with FHB resistance level. Collectively, over 12,300 wheat genes were Fusarium responsive. The core set of genes induced in response to Fg was common across different resistance groups, indicating that the activation of basal defense response mechanisms was largely independent of the resistance level of the wheat line. Fg-induced genes tended to have higher expression levels in more susceptible genotypes. Compared to the more susceptible non-Sumai3 lines, the Sumai3-derivatives demonstrated higher constitutive expression of genes associated with cell wall and plant-type secondary cell wall biogenesis and higher constitutive and Fg-induced expression of genes involved in terpene metabolism. Gene expression analysis of the FHB QTL Qfhs.ifa-5A identified a constitutively expressed gene encoding a stress response NST1-like protein (TraesCS5A01G211300LC) as a candidate gene for FHB resistance. NST1 genes are key regulators of secondary cell wall biosynthesis in anther endothecium cells. Whether the stress response NST1-like gene affects anther extrusion, thereby affecting FHB resistance, needs further investigation. Conclusion Induced and preexisting cell wall components and terpene metabolites contribute to resistance and limit fungal colonization early on. In contrast, excessive gene expression directs plant defense response towards programmed cell death which favors necrotrophic growth of the Fg pathogen and could thus lead to increased fungal colonization.

Aegilops tauschii, the diploid wild progenitor of the D-subgenome of bread wheat, constitutes a reservoir of genetic diversity for improving bread wheat performance and environmental resilience. To better define and understand this diversity, we sequenced 242 Ae. tauschii accessions and compared them to the wheat D-subgenome. We characterized a rare, geographically-restricted lineage of Ae. tauschii and discovered that it contributed to the wheat D-subgenome, thereby elucidating the origin of bread wheat from at least two independent hybridizations. We then used k -mer-based association mapping to identify discrete genomic regions with candidate genes for disease and pest resistance and demonstrated their functional transfer into wheat by transgenesis and wide crossing, including the generation of a library of ‘synthetic’ hexaploids incorporating diverse Ae. tauschii genomes. This pipeline permits rapid trait discovery in the diploid ancestor through to functional genetic validation in a hexaploid background amenable to breeding.

Genomic selection with genome-wide distributed molecular markers has evolved into a well-implemented tool in many breeding programs during the last decade. The resistance against Fusarium head blight (FHB) in wheat is probably one of the most thoroughly studied systems within this framework. Aside from the genome, other biological strata like the transcriptome have likewise shown some potential in predictive breeding strategies but have not yet been investigated for the FHB-wheat pathosystem. The aims of this study were thus to compare the potential of genomic with transcriptomic prediction, and to assess the merit of blending incomplete transcriptomic with complete genomic data by the single-step method. A substantial advantage of gene expression data over molecular markers has been observed for the prediction of FHB resistance in the studied diversity panel of breeding lines and released cultivars. An increase in prediction ability was likewise found for the single-step predictions, although this can mostly be attributed to an increased accuracy among the RNA-sequenced genotypes. The usage of transcriptomics can thus be seen as a complement to already established predictive breeding pipelines with pedigree and genomic data, particularly when more cost-efficient multiplexing techniques for RNA-sequencing will become more accessible in the future.

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.

Fusarium head blight (FHB) is a devastating disease for cereals. FHB is managed by fungicides at anthesis, but their efficacy is variable. Conventional fungicides accumulate in the soil and are dangerous for animal and human health. This study assayed the antifungal ability of chitosan hydrochloride against Fusarium graminearum. Chitosan reduced F. graminearum growth and downregulated the transcript of the major genes involved in the cell growth, respiration, virulence, and trichothecenes biosynthesis. Chitosan promoted the germination rate, the root and coleoptile development, and the nitrogen balance index in two durum wheat genotypes, Marco Aurelio (FHB-susceptible) and DBC480 (FHB-resistant). Chitosan reduced FHB severity when applied on spikes or on the flag leaves. FHB severity in DBC480 was of 6% at 21 dpi after chitosan treatments compared to F. graminearum inoculated control (20%). The elicitor-like property of chitosan was confirmed by the up-regulation of TaPAL, TaPR1 and TaPR2 (around 3-fold). Chitosan decreased the fungal spread and mycotoxins accumulation. This study demonstrated that the non-toxic chitosan is a powerful molecule with the potential to replace the conventional fungicides. The combination of a moderately resistant genotype (DBC480) with a sustainable compound (chitosan) will open new frontiers for the reduction of conventional compounds in agriculture.

Trichothecenes are sesquiterpenoid mycotoxins produced by fungi from the order Hypocreales, including members of the Fusarium genus that infect cereal grain crops. Different trichothecene-producing Fusarium species and strains have different trichothecene chemotypes belonging to the Type A and B class. These fungi cause a disease of small grain cereals, called Fusarium head blight, and their toxins contaminate host tissues. As potent inhibitors of eukaryotic protein synthesis, trichothecenes pose a health risk to human and animal consumers of infected cereal grains. In 2009, Foroud and Eudes published a review of trichothecenes in cereal grains for human consumption. As an update to this review, the work herein provides a comprehensive and multi-disciplinary review of the Fusarium trichothecenes covering topics in chemistry and biochemistry, pathogen biology, trichothecene toxicity, molecular mechanisms of resistance or detoxification, genetics of resistance and breeding strategies to reduce their contamination of wheat and barley.

The major Fusarium mycotoxin deoxynivalenol (DON) is a virulence factor in wheat and has also been shown to induce defense responses in host plant tissue. In this study, global and tracer labeling with 13C were combined to annotate the overall metabolome of wheat spikes and to evaluate the response of phenylalanine-related pathways upon treatment with DON. At anthesis, spikes of resistant and susceptible cultivars as well as two related near isogenic wheat lines (NILs) differing in the presence/absence of the major resistance QTL Fhb1 were treated with 1 mg DON or water (control), and samples were collected at 0, 12, 24, 48, and 96 h after treatment (hat). A total of 172 Phe-derived wheat constituents were detected with our untargeted approach employing 13C-labeled phenylalanine and subsequently annotated as flavonoids, lignans, coumarins, benzoic acid derivatives, hydroxycinnamic acid amides (HCAAs), as well as peptides. Ninety-six hours after the DON treatment, up to 30% of the metabolites biosynthesized from Phe showed significantly increased levels compared to the control samples. Major metabolic changes included the formation of precursors of compounds implicated in cell wall reinforcement and presumed antifungal compounds. In addition, also dipeptides, which presumably are products of proteolytic degradation of truncated proteins generated in the presence of the toxin, were significantly more abundant upon DON treatment. An in-depth comparison of the two NILs with correlation clustering of time course profiles revealed some 70 DON-responsive Phe derivatives. While several flavonoids had constitutively different abundance levels between the two NILs differing in resistance, other Phe-derived metabolites such as HCAAs and hydroxycinnamoyl quinates were affected differently in the two NILs after treatment with DON. Our results suggest a strong activation of the general phenylpropanoid pathway and that coumaroyl-CoA is mainly diverted towards HCAAs in the presence of Fhb1, whereas the metabolic route to monolignol(-conjugates), lignans, and lignin seems to be favored in the absence of the Fhb1 resistance quantitative trait loci.

Key messageGenomic selection had a higher selection response for FHB resistance than phenotypic selection, while association mapping identified major QTL on chromosome 3B unaffected by plant height and flowering date.AbstractFusarium head blight (FHB) is one of the most destructive diseases of durum wheat. Hence, minimizing losses in yield, quality and avoiding contamination with mycotoxins are of pivotal importance, as durum wheat is mostly used for human consumption. While growing resistant varieties is the most promising approach for controlling this fungal disease, FHB resistance breeding in durum wheat is hampered by the limited variation in the elite gene pool and difficulties in efficiently combining the numerous small-effect resistance quantitative trait loci (QTL) in the same line. We evaluated an international collection of 228 genotyped durum wheat cultivars for FHB resistance over 3years to investigate the genetic architecture and potential of genomic-assisted breeding for FHB resistance in durum wheat. Plant height was strongly positively correlated with FHB resistance and led to co-localization of plant height and resistance QTL. Nevertheless, a major QTL on chromosome 3B independent of plant height was identified in the same chromosomal interval as reported for the prominent hexaploid resistance QTL Fhb1, though haplotype analysis highlighted the distinctiveness of both QTL. Comparison between phenotypic and genomic selection for FHB resistance revealed a superior prediction ability of the former. However, simulated selection experiments resulted in higher selection responses when using genomic breeding values for early generation selection. An earlier identification of the most promising lines and crossing parents was feasible with a genomic selection index, which suggested a much faster short-term population improvement than previously possible in durum wheat, complementing long-term strategies with exotic resistance donors.

Fusarium head blight (FHB) is a major fungal disease affecting wheat production worldwide. Since the early 1990s, FHB, caused primarily by Fusarium graminearum, has become one of the most significant diseases faced by wheat producers in Canada and the United States. The increasing FHB problem is likely due to the increased adoption of conservation tillage practices, expansion of maize production, use of susceptible wheat varieties in rotation, and climate variability. Durum wheat (Triticum turgidum sp. durum) is notorious for its extreme susceptibility to FHB and breeding for resistance is complicated because sources of FHB resistance are rare in the primary gene pool of tetraploid wheat. Losses due to this disease include yield, test weight, seed quality, food and feed quality, and when severe, market access. More importantly, it is the contamination with mycotoxins, such as deoxynivalenol, in Fusarium-infected durum kernels that causes the most serious economic as well as food and feed safety concerns. Several studies and thorough reviews have been published on germplasm development and breeding for FHB resistance and the genetics and genomics of FHB resistance in bread or common wheat (T. aestivum); however, similar reviews have not been conducted in durum wheat. Thus, the aim of this review is to summarize and discuss the recent research efforts to mitigate FHB in durum wheat, including quantitative trait locus mapping, genome-wide association studies, genomic prediction, mutagenesis and characterization of genes and pathways involved in FHB resistance. It also highlights future directions, FHB-resistant germplasm, and the potential role of morphological traits to enhance FHB resistance in durum wheat.