Antioxidant Secondary Metabolites in Cereals: Potential Involvement in Resistance to Fusarium and Mycotoxin Accumulation

Abstract

Gibberella and Fusarium Ear Rot and Fusarium Head Blight are major diseases affecting European cereals. These diseases are mainly caused by fungi of the Fusarium genus, primarily Fusarium graminearum and Fusarium verticillioides. These Fusarium species pose a serious threat to food safety because of their ability to produce a wide range of mycotoxins, including type B trichothecenes and fumonisins. Many factors such as environmental, agronomic or genetic ones may contribute to high levels of accumulation of mycotoxins in the grain and there is an urgent need to implement efficient and sustainable management strategies to reduce mycotoxin contamination. Actually, fungicides are not fully efficient to control the mycotoxin risk. In addition, because of harmful effects on human health and environment, their use should be seriously restricted in the near future. To durably solve the problem of mycotoxin accumulation, the breeding of tolerant genotypes is one of the most promising strategies for cereals. A deeper understanding of the molecular mechanisms of plant resistance to both Fusarium and mycotoxin contamination will shed light on plant-pathogen interactions and provide relevant information for improving breeding programs. Resistance to Fusarium depends on the plant ability in preventing initial infection and containing the development of the toxigenic fungi while resistance to mycotoxin contamination is also related to the capacity of plant tissues in reducing mycotoxin accumulation. This capacity can result from two mechanisms: metabolic transformation of the toxin into less toxic compounds and inhibition of toxin biosynthesis. This last mechanism involves host metabolites able to interfere with mycotoxin biosynthesis. This review aims at gathering the latest scientific advances that support the contribution of grain antioxidant secondary metabolites to the mechanisms of plant resistance to Fusarium and mycotoxin accumulation.

Keywords: Fusarium; antioxidants; cereals; mycotoxins; resistance.

Figure 1

Main antioxidant secondary metabolites quantified in maize at (A) maturity and at (B) early stage when mycotoxin biosynthesis is initiated (milk-dough stage). This model is based on maize results obtained by Atanasova-Penichon et al. (2012), Atanasova-Penichon and Richard-Forget (2014) and Picot et al. (2013).

Figure 2

(A) Relative quantification of fungal DNA in maize kernels, expressed as a log10 (F. graminearum DNA/maize DNA) ratio of a susceptible variety (blue triangles, right Y-axis), and level of trichothecenes accumulated in maize kernels (red squares, left Y-axis) after silk inoculation with F. graminearum. Vertical bars show standard error of the mean. Top X-axis: thermal time from inoculation (mean value of 2 years), bottom X-axis: days after inoculation for each sampling (mean value of 2 years). Data from the 2 years and two repetitions were pooled (mean values ± SEM, n = 4). (B) Relative quantification of fungal DNA in maize kernels, expressed as a log10 F. verticillioides DNA/log10 maize DNA ratio of a susceptible variety (blue triangles, right Y-axis), and level of fumonisins accumulated in maize kernels (red squares, left Y-axis) after silk inoculation with F. verticillioides. Vertical bars show standard deviations. Top X-axis: thermal time from inoculation, bottom X-axis: days after inoculation for each sampling. Data from the two sowing date treatments were pooled. Kinetics are established with data published by Atanasova-Penichon et al. (2012) and Picot et al. (2011).

Figure 3

Kinetics of antioxidant compounds during maize grain development: (A) chlorogenic acid; (B) cell-wall-bound ferulic acid; (C) ferulic acid dehydrodimers; (D) xanthophylls; (E) carotenes and (F) tocopherols. Kinetics are established with data published by Atanasova-Penichon et al. (2012), Atanasova-Penichon and Richard-Forget (2014) and Picot et al. (2013).

Figure 4

Levels of some antioxidant metabolites in immature maize grains from three groups of varieties differing in their susceptibility to GER: highly susceptible (HS, n = 3), susceptible (S, n = 4), and moderately susceptible (MS, n = 3). (A) chlorogenic acid; (B) cell-wall-bound ferulic acid; (C) ferulic acid dehydrodimers; (D) tocopherols and (E) carotenoids. Groups with different letters are significantly different. (Duncan, α = 0.05; Atanasova-Penichon et al., ; Atanasova-Penichon and Richard-Forget, 2014).