Ana Cao

In temperate world-wide regions, maize kernels are often infected with the fumonisin-producing fungus Fusarium verticillioides which poses food and feed threats to animals and humans. As maize breeding has been revealed as one of the main tools with which to reduce kernel contamination with fumonisins, a pedigree selection program for increased resistance to Fusarium ear rot (FER), a trait highly correlated with kernel fumonisin content, was initiated in 2014 with the aim of obtaining inbred lines (named EPFUM) with resistance to kernel contamination with fumonisins and adapted to our environmental conditions. The new released EPFUM inbreds, their parental inbreds, hybrids involving crosses of one or two EPFUM inbreds, as well as commercial hybrids were evaluated in the current study. The objectives were (i) to assess if inbreds released by that breeding program were significantly more resistant than their parental inbreds and (ii) to examine if hybrids derived from EPFUM inbreds could be competitive based on grain yield and resistance to FER and fumonisin contamination. Second-cycle inbreds obtained through this pedigree selection program did not significantly improve the levels of resistance to fumonisin contamination of their parental inbreds; however, most EPFUM hybrids showed significantly better resistance to FER and fumonisin contamination than commercial hybrids did. Although European flint materials seem to be the most promising reservoirs of alleles with favorable additive and/or dominance effects for resistance to kernel contamination with fumonisins, marketable new Reid × Lancaster hybrids have been detected as they combine high resistance and yields comparable to those exhibited by commercial hybrids. Moreover, the white kernel hybrid EPFUM-4 × EP116 exploits the genetic variability within the European flint germplasm and can be an alternative to dent hybrid cultivation because white flint grain can lead to higher market prices.

Maize kernel is exposed to several fungal species, most notably Fusarium verticillioides, which can contaminate maize kernels with fumonisins. In an effort to increase genetic gains and avoid the laborious tasks of conventional breeding, the use of marker-assisted selection or genomic selection programs was proposed. To this end, in the present study a Genome Wide Association Study (GWAS) was performed on 339 RILs of a Multiparental Advanced Generation InterCross (MAGIC) population that had previously been used to locate Quantitative Trait Locus (QTL) for resistance to Fusarium Ear Rot (FER). Six QTLs for fumonisin content were detected in the bins 3.08, 4.07, 4.10, 7.03-7.04, 9.04-9.05 and 10.04-10.5. Five of the six QTLs collocate in regions where QTLs for FER were also found. However, the genetic variation for fumonisin content in kernel is conditioned by many other QTLs of small effect that could show QTL x environment interaction effects. Although a genomic selection approach to directly reduce fumonisin content in the kernel could be suitable, improving resistance to fumonisin content by genomic selection for FER would be more advisable.

Food contamination with mycotoxins is a worldwide concern, because these toxins produced by several fungal species have detrimental effects on animal and/or human health. In maize, fumonisins are among the toxins with the highest threatening potential because they are mainly produced by Fusarium verticillioides, which is distributed worldwide. Plant breeding has emerged as an effective and environmentally safe method to reduce fumonisin levels in maize kernels, but although phenotypic selection has proved effective for improving resistance to fumonisin contamination, further resources should be mobilized to meet farmers’ needs. Selection based on molecular markers linked to quantitative trait loci (QTL) for resistance to fumonisin contamination or/and genotype values obtained using prediction models with markers distributed across the whole genome could speed up breeding progress. Therefore, in the current paper, previously identified genomic regions, genes, and/or pathways implicated in resistance to fumonisin accumulation will be reviewed. Studies done until now have provide many markers to be used by breeders, but to get further insight on plant mechanisms to defend against fungal infection and to limit fumonisin contamination, the genes behind those QTLs should be identified.

Plant breeding has been proposed as one of the most effective and environmentally safe methods to control fungal infection and to reduce fumonisin accumulation. However, conventional breeding can be hampered by the complex genetic architecture of resistance to fumonisin accumulation and marker-assisted selection is proposed as an efficient alternative. In the current study, GWAS has been performed for the first time for detecting high-resolution QTL for resistance to fumonisin accumulation in maize kernels complementing published GWAS results for Fusarium ear rot. Thirty-nine SNPs significantly associated with resistance to fumonisin accumulation in maize kernels were found and clustered into 17 QTL. Novel QTLs for fumonisin content would be at bins 3.02, 5.02, 7.05 and 8.07. Genes with annotated functions probably implicated in resistance to pathogens based on previous studies have been highlighted. Breeding approaches to fix favorable functional variants for genes implicated in maize immune response signaling may be especially useful to reduce kernel contamination with fumonisins without significantly interfering in mycelia development and growth and, consequently, in the beneficial endophytic behavior of Fusarium verticillioides.

Contamination of maize with fumonisins depends on the environmental conditions; the maize resistance to contamination and the interaction between both factors. Although the effect of environmental factors is a determinant for establishing the risk of kernel contamination in a region, there is sufficient genetic variability among maize to develop resistance to fumonisin contamination and to breed varieties with contamination at safe levels. In addition, ascertaining which environmental factors are the most important in a region will allow the implementation of risk monitoring programs and suitable cultural practices to reduce the impact of such environmental variables. The current paper reviews all works done to address the influence of environmental variables on fumonisin accumulation, the genetics of maize resistance to fumonisin accumulation, and the search for the biochemical and/or structural mechanisms of the maize plant that could be involved in resistance to fumonisin contamination. We also explore the outcomes of breeding programs and risk monitoring of undertaken projects.

In the current study, the hydroxycinnamic acids in silks of diverse maize inbred lines differing in Fusarium resistance were determined at several times after inoculation with Fusarium graminearum or sterile water as control. The main objective was to determine the possible relationship between the hydroxycinnamic acid changes in silks and ear rot resistance. Several changes in the cell-wall-bound hydroxycinnamic acid concentrations were observed after inoculation with F. graminearum, although these changes were not directly correlated with genotypic resistance to this fungus. Ester-bound ferulic acid decreased, probably due to degradation of hemicellulose by hydrolytic enzymes produced by Fusarium spp., while p-coumaric acid and diferulates showed slight increases that, in conjunction, did not result in delayed F. graminearum progression through the silks. It is important to note that the decrease of ferulic acid in the F. graminearum treatment was faster in susceptible than in resistant genotypes, suggesting a differential hemicellulose degradation in silk tissues. Therefore, the ability of the maize genotypes to slow down that process through hemicellulose structural features or xylanase inhibitors needs to be addressed in future studies.