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Candidate Genes for Aggressiveness in a Natural Fusarium culmorum Population Greatly Differ between Wheat and Rye Head Blight.

ABSTRACT: Fusarium culmorum is one of the species causing Fusarium head blight (FHB) in cereals in Europe. We aimed to investigate the association between the nucleotide diversity of ten F. culmorum candidate genes and field ratings of aggressiveness in winter rye. A total of 100 F. culmorum isolates collected from natural infections were phenotyped for FHB at two locations and two years. Variance components for aggressiveness showed significant isolate and isolate-by-environment variance, as expected for quantitative host-pathogen interactions. Further analysis of the isolate-by-environment interaction revealed the dominant role of the isolate-by-year over isolate-by-location interaction. One single-nucleotide polymorphism (SNP) in the cutinase (CUT) gene was found to be significantly (p < 0.001) associated with aggressiveness and explained 16.05% of the genotypic variance of this trait in rye. The SNP was located 60 base pairs before the start codon, which suggests a role in transcriptional regulation. Compared to a previous study in winter wheat with the same nucleotide sequences, a larger variation of pathogen aggressiveness on rye was found and a different candidate gene was associated with pathogen aggressiveness. This is the first report on the association of field aggressiveness and a host-specific candidate gene codifying for a protein that belongs to the secretome in F. culmorum.

SUBMITTER: Castiblanco V

PROVIDER: S-EPMC5872317 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Candidate Genes for Aggressiveness in a Natural Fusarium culmorum Population Greatly Differ between Wheat and Rye Head Blight.

Castiblanco Valheria V Castillo Hilda Elena HE Miedaner Thomas T

Journal of fungi (Basel, Switzerland) 20180116 1

Fusarium culmorum is one of the species causing Fusarium head blight (FHB) in cereals in Europe. We aimed to investigate the association between the nucleotide diversity of ten F. culmorum candidate genes and field ratings of aggressiveness in winter rye. A total of 100 F. culmorum isolates collected from natural infections were phenotyped for FHB at two locations and two years. Variance components for aggressiveness showed significant isolate and isolate-by-environment vari ...[more]

PMID: 29371506

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Project description:BackgroundFusarium culmorum is an important pathogen causing head blight of cereals in Europe. This disease is of worldwide importance leading to reduced yield, grain quality, and contamination by mycotoxins. These mycotoxins are harmful for livestock and humans; therefore, many countries have strict regulatory limits for raw materials and processed food. Extensive genetic diversity is described among field populations of F. culmorum isolates for aggressiveness and production of the trichothecene mycotoxin deoxynivalenol (DON). However, the causes for this quantitative variation are not clear, yet. We analyzed 92 isolates sampled from different field populations in Germany, Russia, and Syria together with an international collection for aggressiveness and DON production in replicated field experiments at two locations in two years with two hosts, wheat and rye. The 30x coverage whole-genome resequencing of all isolates resulted in the identification of 130,389 high quality single nucleotide polymorphisms (SNPs) that were used for the first genome-wide association study in this phytopathogenic fungus.ResultsIn wheat, 20 and 27 SNPs were detected for aggressiveness and DON content, respectively, of which 10 overlapped. Additionally, two different SNPs were significantly associated with aggressiveness in rye that were among those SNPs being associated with DON production in wheat. Most of the SNPs explained only a small proportion of genotypic variance (pG), however, four SNPs were associated with major quantitative trait loci (QTLs) with pG ranging from 12 to 48%. The QTL with the highest pG was involved in DON production and associated with a SNP most probably located within the Tri4 gene.ConclusionsThe diversity of 92 isolates of F. culmorum were captured using a heuristic approach. Key phenotypic traits, SNPs, and candidate genes underlying aggressiveness and DON production were identified. Clearly, many QTLs are responsible for aggressiveness and DON content in wheat, both traits following a quantitative inheritance. Several SNPs involved in DON metabolism, among them the Tri4 gene of the trichothecene pathway, were inferred as important source of variation in fungal aggressiveness. Using this information underlying the phenotypic variation will be of paramount importance in evaluating strategies for successful resistance breeding.

Project description:BackgroundFusarium head blight (FHB) caused by Fusarium graminearum not only causes severe losses in yield, but also reduces quality of wheat grain by accumulating mycotoxins. Breeding for host plant resistance is considered as the best strategy to manage FHB. Resistance in wheat to FHB is quantitative in nature, involving cumulative effects of many genes governing resistance. The poor understanding of genetics and lack of precise phenotyping has hindered the development of FHB resistant cultivars. Though more than 100 QTLs imparting FHB resistance have been reported, none discovered the specific genes localized within the QTL region, nor the underlying mechanisms of resistance.FindingsIn our study recombinant inbred lines (RILs) carrying resistant (R-RIL) and susceptible (S-RIL) alleles of QTL-Fhb2 were subjected to metabolome and transcriptome profiling to discover the candidate genes. Metabolome profiling detected a higher abundance of metabolites belonging to phenylpropanoid, lignin, glycerophospholipid, flavonoid, fatty acid, and terpenoid biosynthetic pathways in R-RIL than in S-RIL. Transcriptome analysis revealed up-regulation of several receptor kinases, transcription factors, signaling, mycotoxin detoxification and resistance related genes. The dissection of QTL-Fhb2 using flanking marker sequences, integrating metabolomic and transcriptomic datasets, identified 4-Coumarate: CoA ligase (4CL), callose synthase (CS), basic Helix Loop Helix (bHLH041) transcription factor, glutathione S-transferase (GST), ABC transporter-4 (ABC4) and cinnamyl alcohol dehydrogenase (CAD) as putative resistance genes localized within the QTL-Fhb2 region.ConclusionSome of the identified genes within the QTL region are associated with structural resistance through cell wall reinforcement, reducing the spread of pathogen through rachis within a spike and few other genes that detoxify DON, the virulence factor, thus eventually reducing disease severity. In conclusion, we report that the wheat resistance QTL-Fhb2 is associated with high rachis resistance through additive resistance effects of genes, based on cell wall enforcement and detoxification of DON. Following further functional characterization and validation, these resistance genes can be used to replace the genes in susceptible commercial cultivars, if nonfunctional, based on genome editing to improve FHB resistance.

Project description:Fusarium head blight (FHB), caused mainly by Fusarium graminearum, is the foremost destructive disease of cereals worldwide. Effector-like molecules produced by F. graminearum play key roles in the infection process and are assumed to be one of the essential components of the pathogen's aggressiveness. However, their nature and role in the disease are still largely misunderstood. As a mean to provide relevant information about the molecular determinism of F. graminearum aggressiveness, we surveyed three F. graminearum strains on three wheat cultivars contrasted by their susceptibility to FHB. F. graminearum strains revealed large differences in aggressiveness which were mostly unchanged when facing hosts of contrasted susceptibility, suggesting that their behavior rely on intrinsic determinants. Surveying the fungal mass progress and the mycotoxin production rate in the spikes did not evidence any simple relationship with aggressiveness differences, while clues were found through a qualitative and quantitative characterization of the three strain proteomes established in planta especially with regards to early synthesized putative effectors. Independently of the wheat cultivar, the three F. graminearum strains produced systematically the same protein set during the infection but substantial differences in their abundance enabled the categorization of fungal aggressiveness. Overall, our findings show that the contrasts in F. graminearum aggressiveness were not based on the existence of strain-specific molecules but rather on the ability of the strain to ensure their sufficient accumulation. Protein abundance variance was mostly driven by the strain genetics and part was also influenced by the host cultivar but strain by cultivar interactions were marginally detected, depicting that strain-specific protein accumulations did not depend on the host cultivar. All these data provide new knowledge on fungal aggressiveness determinants and provide a resourceful repertoire of candidate effector proteins to guide further research.

Project description:IntroductionFusarium avenaceum causing Fusarium seedling blight (FSB) and Fusarium head blight (FHB) on barley is associated with economic losses of crop yield and quality, and the accumulation of mycotoxins including the enniatins (ENNs) A, A1, B and B1. Although F. avenaceum is the main producer of ENNs, studies on the ability of isolates to cause severe Fusarium diseases or produce mycotoxins in barley are limited.MethodsIn this work, we investigated the aggressiveness of nine isolates of F. avenaceum to two cultivars of malting barley, Moonshine and Quench, and defined their ENN mycotoxin profiles in in vitro and in planta experiments. We assessed and compared the severity of FSB and FHB caused by these isolates to disease severity by F. graminearum, F. tricinctum and F. poae. Quantitative real-time polymerase chain reaction and Liquid Chromatography Tandem Mass Spectrometry assays were used to quantify pathogen DNA and mycotoxin accumulation, respectively, in barley heads.ResultsIsolates of F. avenaceum were equally aggressive to barley stems and heads and caused the most severe FSB symptoms resulting in up to 55% reductions of stem and root length. Fusarium graminearum caused the most severe FHB disease, followed by the isolates of F. avenaceum with the most aggressive F. avenaceum isolates capable of causing similar bleaching of barley heads as F. avenaceum. Fusarium avenaceum isolates produced ENN B as the predominant mycotoxin, followed by ENN B1 and A1 in vitro. However, only the most aggressive isolates produced ENN A1 in planta and none produced ENN A or beauvericin (BEA) either in planta or in vitro.DiscussionThe capacity of F. avenaceum isolates to produce ENNs was related to the accumulation of pathogen DNA in barley heads, whilst FHB severity was related to the synthesis and accumulation of ENN A1 in planta. Cv. Moonshine was significantly more resistant than Quench to FSB or FHB, caused by any Fusarium isolate, and to the accumulation of pathogen DNA, ENNs or BEA. In conclusion, aggressive F. avenaceum isolates are potent ENN producers causing severe FSB and FHB with ENN A1 requiring further investigation as potential virulence factor for F. avenaceum in cereals.

Dataset Information

Candidate Genes for Aggressiveness in a Natural Fusarium culmorum Population Greatly Differ between Wheat and Rye Head Blight.

Publications

Candidate Genes for Aggressiveness in a Natural Fusarium culmorum Population Greatly Differ between Wheat and Rye Head Blight.

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