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Investigating Metabolic Plant Response toward Deoxynivalenol Accumulation in Four Winter Cereals.

ABSTRACT: Deoxynivalenol (DON) is a phytotoxic agent supporting the spread of fungal diseases in cereals worldwide, i.e., fusarium head blight. It is known that DON accumulation may elicit changes in plant secondary metabolites in response to pathogen attack. This study maps the changes in selected secondary metabolite classes upon DON contamination occurring in fifteen Triticum spp. genotypes, among them emmer, spelt, and soft wheat, and 2 tritordeum varieties, cultivated in two different sites and over two harvest years. The main phenolic classes (i.e., alkylresorcinols, soluble, and cell-wall bound phenolic acids) were targeted analyzed, while changes in the lipidome signature were collected through untargeted HRMS experiments. The results, obtained across multiple Triticum species and in open fields, confirmed the modulation of first-line biological pathways already described in previous studies involving single cereal species or a limited germplasm, thus reinforcing the involvement of nonspecific chemical defenses in the plant response to pathogen attack.

SUBMITTER: Righetti L

PROVIDER: S-EPMC10870777 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Investigating Metabolic Plant Response toward Deoxynivalenol Accumulation in Four Winter Cereals.

Righetti Laura L Vanara Francesca F Bruni Renato R Sardella Claudia C Blandino Massimo M Dall'Asta Chiara C

Journal of agricultural and food chemistry 20240205 6

Deoxynivalenol (DON) is a phytotoxic agent supporting the spread of fungal diseases in cereals worldwide, i.e., fusarium head blight. It is known that DON accumulation may elicit changes in plant secondary metabolites in response to pathogen attack. This study maps the changes in selected secondary metabolite classes upon DON contamination occurring in fifteen <i>Triticum</i> spp. genotypes, among them emmer, spelt, and soft wheat, and 2 tritordeum varieties, cultivated in two different sites an ...[more]

PMID: 38315448

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Project description:Wheat is one of the most important cereals, whose growth and development is strongly limited by drought. This study investigated the physiological and metabolic response of six winter wheat cultivars to drought with the emphasis on the induction of dominant metabolites affected by the treatment and genotypes or both. The plants were exposed to a moderate (non-lethal) drought stress, which was induced by withholding watering for six days under controlled greenhouse conditions. A decline in CO2 assimilation (Pn) and transpiration rate, stomata closure, a decrease in relative water content (RWC) and increase of malondialdehyde content were observed in drought-treated plants of all cultivars. These changes were most pronounced in Ellvis, while Soissons was able to retain the higher RWC and Pn. Among the studied metabolites, sugars (sucrose, glucose, fructose, several disaccharides), organic acids (malic acid, oxalic acids), amino acids (proline, threonine, gamma-aminobutyric acid (GABA), glutamine) and sugar alcohols such as myo-inositol accumulated to higher levels in the plants exposed to drought stress in comparison with the control. The accumulation of several metabolites in response to drought differed between the genotypes. Drought induced the production of sucrose, malic acid and oxalic acid, unknown organic acid 1, unknown disaccharide 1, 2 and 3, GABA, L-threonine, glutamic acid in four (Soissons, Žitarka, Antonija or Toborzó) out of six genotypes. In addition, Soissons, which was the most drought tolerant genotype, accumulated the highest amount of unknown disaccharide 5, galactonic and phosphoric acids. The two most drought sensitive cultivars, Srpanjka and Ellvis, demonstrated different metabolic adjustment in response to the stress treatment. Srpanjka responded to drought by increasing the amount of glucose and fructose originated from hydrolyses of sucrose and accumulating unidentified sugar alcohols 1 and 2. In Ellvis, drought caused inhibition of photosynthetic carbon metabolism, as evidence by the decreased Pn, gs, RWC and accumulation levels of sugar metabolites (sucrose, glucose and fructose). The results revealed the differences in metabolic response to drought among the genotypes, which drew attention on metabolites related with general response and on those metabolites which are part of specific response that may play an important role in drought tolerance.

Project description: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.

Dataset Information

Investigating Metabolic Plant Response toward Deoxynivalenol Accumulation in Four Winter Cereals.

Publications

Investigating Metabolic Plant Response toward Deoxynivalenol Accumulation in Four Winter Cereals.

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