Diverse Components of Resistance to Fusarium verticillioides Infection and Fumonisin Contamination in Four Maize Recombinant Inbred Families

The fungus Fusarium verticillioides can infect maize ears, causing Fusarium ear rot (FER) and contaminating the grain with fumonisins (FUM), which are harmful to humans and animals. Breeding for resistance to FER and FUM and post-harvest sorting of grain are two strategies for reducing FUM in the food system. Kernel and cob tissues have been previously associated with differential FER and FUM. Four recombinant inbred line families from the maize nested associated mapping population were grown and inoculated with F. verticillioides across four environments, and we evaluated the kernels for external and internal infection severity as well as FUM contamination. We also employed publicly available phenotypes on innate ear morphology to explore genetic relationships between ear architecture and resistance to FER and FUM. The four families revealed wide variation in external symptomatology at the phenotypic level. Kernel bulk density under inoculation was an accurate indicator of FUM levels. Genotypes with lower kernel density—under both inoculated and uninoculated conditions—and larger cobs were more susceptible to infection and FUM contamination. Quantitative trait locus (QTL) intervals could be classified as putatively resistance-specific and putatively shared for ear and resistance traits. Both types of QTL mapped in this study had substantial overlap with previously reported loci for resistance to FER and FUM. Ear morphology may be a component of resistance to F. verticillioides infection and FUM accumulation.

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Relationships Among Ear Morphology, Western Flower Thrips, and Fusarium Ear Rot of Corn

Phytopathology ◽

10.1094/phyto-81-661 ◽

1991 ◽

Vol 81 (6) ◽

pp. 661 ◽

Cited By ~ 41

Author(s):

J. J. Farrar

Keyword(s):

Western Flower Thrips ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Flower Thrips ◽

Ear Morphology

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Evaluation of Food-Grade Dent Corn Hybrids for Severity of Fusarium Ear Rot and Fumonisin Accumulation in Grain

Plant Disease ◽

10.1094/pd-89-0291 ◽

2005 ◽

Vol 89 (3) ◽

pp. 291-297 ◽

Cited By ~ 22

Author(s):

C. E. Kleinschmidt ◽

M. J. Clements ◽

C. M. Maragos ◽

J. K. Pataky ◽

D. G. White

Keyword(s):

Fusarium Verticillioides ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Natural Conditions ◽

Corn Hybrids ◽

Food Grade ◽

Human Food ◽

Inoculation Technique ◽

Dent Corn ◽

High Concentrations

Fumonisins produced by Fusarium verticillioides (syn = F. moniliforme) and F. proliferatum have been associated with potentially serious toxicoses of animals and humans. Thus, hybrids with low fumonisin accumulation in grain will be valuable for the production of corn-based human food products. We evaluated 68 food-grade dent corn hybrids for severity of Fusarium ear rot and fumonisin accumulation in grain in inoculated trials in Urbana, IL in 2000 and 2001. Our inoculation technique was successful in initiating fumonisin accumulation that allowed discrimination among hybrids. We identified several hybrids that could have acceptable levels (<4 μg/g) of fumonisin accumulation in Illinois in most years. Twenty-six hybrids with low or high fumonisin accumulation in 2000 were reevaluated in noninoculated trials at three locations in Illinois in 2001. Fumonisin concentration in grain at all three locations was relatively low; thus, separation of hybrids was poor. At two locations, those hybrids with the highest fumonisin concentration in grain also had high concentrations following inoculation. However, one hybrid that had relatively low fumonisin concentration following inoculation had unacceptable levels of fumonisin (5 μg/g) in natural conditions. Therefore, hybrids need to be evaluated by inoculation and further evaluated at locations where the environment favors fumonisin accumulation.

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Fusarium verticillioides induces maize-derived ethylene to promote virulence by engaging fungal G-protein signaling

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-09-20-0250-r ◽

2021 ◽

Author(s):

Yong-Soon Park ◽

Eli J Borrego ◽

Xiquan Gao ◽

Shawn A Christensen ◽

Eric Schmelz ◽

...

Keyword(s):

G Protein ◽

Fusarium Verticillioides ◽

G Protein Signaling ◽

Protein Signaling ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Knock Out ◽

Seed Colonization ◽

Meta Analyses ◽

Exogenous Treatment

Seed maceration and contamination with mycotoxin fumonisin inflicted by Fusarium verticillioides is major disease of concern for maize producers world-wide. Meta-analyses of QTL for Fusarium ear rot resistance uncovered several ethylene (ET) biosynthesis and signaling genes within them, implicating ET in maize interactions with F. verticillioides. We tested this hypothesis using maize knock-out mutants of the 1-aminocyclopropane-1-carboxylate (ACC) synthases, ZmACS2 and ZmACS6. Infected wild-type seed emitted five-fold higher ET levels compared to controls, whereas ET was abolished in the acs2 and acs6 single and double mutants. The mutants supported reduced fungal biomass, conidia and fumonisin content. Normal susceptibility was restored in the acs6 mutant with exogenous treatment of ET precursor, ACC. Subsequently, we showed that fungal G-protein signaling is required for virulence via induction of maize-produced ET. F. verticillioides Gβ subunit and two regulators of G-protein signaling mutants displayed reduced seed colonization and decreased ET levels. These defects were rescued by exogenous application of ACC. We concluded that pathogen-induced ET facilitates F. verticillioides colonization of seed, and in turn host ET production is manipulated via G-protein signaling of F. verticillioides to facilitate pathogenesis.

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Complex Genetic System Involved in Fusarium Ear Rot Resistance in Maize as Revealed by GWAS, Bulked Sample Analysis, and Genomic Prediction

Plant Disease ◽

10.1094/pdis-07-19-1552-re ◽

2020 ◽

Vol 104 (6) ◽

pp. 1725-1735 ◽

Cited By ~ 2

Author(s):

Zifeng Guo ◽

Cheng Zou ◽

Xiaogang Liu ◽

Shanhong Wang ◽

Wen-Xue Li ◽

...

Keyword(s):

Confidence Level ◽

Genomic Prediction ◽

Complex Traits ◽

Genome Wide Association Study ◽

Fusarium Verticillioides ◽

Chromosome 1 ◽

Nucleotide Polymorphisms ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Sample Analysis

Fusarium ear rot (FER) caused by Fusarium verticillioides is one of the most prevalent maize diseases in China and worldwide. Resistance to FER is a complex trait controlled by multiple genes highly affected by environment. In this paper, genome-wide association study (GWAS), bulked sample analysis (BSA), and genomic prediction were performed for understanding FER resistance using 509 diverse inbred lines, which were genotyped by 37,801 high-quality single-nucleotide polymorphisms (SNPs). Ear rot evaluation was performed using artificial inoculation in four environments in China: Xinxiang, Henan, and Shunyi, Beijing, during 2017 and 2018. Significant phenotypic and genetic variation for FER severity was observed, and FER resistance was significantly correlated among the four environments with a generalized heritability of 0.78. GWAS identified 23 SNPs that were associated with FER resistance, 2 of which (1_226233417 on chromosome 1 and 10_14501044 on chromosome 10) were associated at threshold of 2.65 × 10−7 [−log(0.01/37,801)]. Using BSA, resistance quantitative trait loci were identified on chromosomes 3, 4, 7, 9, and 10 at the 90% confidence level and on chromosomes 3 and 10 at the 95% confidence level. A key region, bin 10.03, was detected by both GWAS and BSA. Genomic prediction for FER resistance showed that the prediction accuracy by trait-related markers was higher than that by randomly selected markers under different levels of marker density. Marker-assisted selection using genomic prediction could be an efficient strategy for genetic improvement for complex traits like FER resistance.

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Variation in pathogenicity of Fusarium verticillioides and resistance of maize genotypes to Fusarium ear rot

Archives of Phytopathology and Plant Protection ◽

10.1080/03235408.2018.1535812 ◽

2018 ◽

Vol 51 (17-18) ◽

pp. 939-950

Author(s):

Olumayowa Mary Olowe ◽

Ayodele Adegboyega Sobowale ◽

Odunayo Joseph Olawuyi ◽

Adegboyega Christopher Odebode

Keyword(s):

Fusarium Verticillioides ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Maize Genotypes

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The Effect of northern corn leaf blight severity on Fusarium ear rot incidence of maize

South African Journal of Science ◽

10.17159/sajs.2020/8508 ◽

2020 ◽

Vol 116 (11/12) ◽

Author(s):

Maryke Craven ◽

Liesl Morey ◽

Adrian Abrahams ◽

Henry A. Njom ◽

...

Keyword(s):

South Africa ◽

Agricultural Research ◽

Fusarium Verticillioides ◽

Plant Stress ◽

Leaf Blight ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Northern Corn Leaf Blight ◽

Progress Curve ◽

Corn Leaf Blight

Northern corn leaf blight (NCLB) caused by Exserohilum turcicum and Fusarium ear rot caused by Fusarium verticillioides, are economically important maize diseases in South Africa. The effect of induced plant stress by NCLB on F. verticillioides ear rot and fumonisin production is unknown. Four field trials were conducted during 2016/2017 and 2017/2018 (November and December planting dates) at the Agricultural Research Council – Grain Crops in Potchefstroom (South Africa). Three maize cultivars with varying resistance levels to NCLB were selected (IMP50-10B – susceptible, BG3292 – moderately susceptible, DKC 61-94BR – resistant). NCLB severities were created through eight treatments: TMT1 – maximum control (three fungicide applications); TMT2 – standard control (two fungicide applications) and TMT3 – natural control (not inoculated or sprayed). The remaining treatments were inoculated with a cocktail of five NCLB races (Race 3, 3N, 23, 23N and 13N): TMT4 (five weeks after planting / WAP); TMT5 (five and six WAP); TMT6 (five, six and seven WAP); TMT7 (six and seven WAP); and TMT8 (seven WAP). Maize ears were naturally infected with F. verticillioides. Fifteen random plants were labelled at dent stage and NCLB severity (%), area under the disease progress curve, ear rot diseased area, ear rot severity (%), ear rot incidence (%) and total fumonisins (FB1+FB2+FB3; ug/kg) were established. Low levels of cob rot severity and fumonisins were obtained in all four trials. NCLB severity did not affect ear rot related parameters measured. Mean fumonisin levels were below the South African tolerance levels. Fumonisin concentrations differed significantly between cultivars but was not affected by NCLB severity or the cultivar x treatment interaction.

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QTL mapping of Fusarium ear rot resistance in maize

Plant Disease ◽

10.1094/pdis-02-20-0411-re ◽

2020 ◽

Author(s):

Jing Wen ◽

Yanqi Shen ◽

Yuexian Xing ◽

Ziyu Wang ◽

Siping Han ◽

...

Keyword(s):

Qtl Mapping ◽

Phenotypic Variation ◽

Fungal Pathogen ◽

Genetic Factors ◽

Inbred Lines ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Resistant Parent ◽

Trait Locus ◽

The Individual

Ear rot is a globally prevalent class of disease in maize, of which Fusarium ear rot (FER) caused by the fungal pathogen Fusarium verticilloides, is the most commonly reported. In this study, three F2 populations, namely F2-C, F2-D and F2-J, and their corresponding F2:3 families were produced by crossing three highly FER-resistant inbred lines, Cheng351, Dan598, and JiV203 with the same susceptible line, ZW18, for quantitative trait locus (QTL) mapping of FER-resistance. The individual crop plants were inoculated by injecting spore suspension of the pathogen into the kernels of the maize ears. The broad-sense heritability (H2) for FER-resistance was estimated to be as high as 0.76, 0.81, and 0.78 in F2-C, F2-D and F2-J, respectively, indicating that genetic factors played a key role in the phenotypic variation. We detected a total of 20 FER-resistant QTLs in the three F2 populations, among which QTLs derived from the resistant parent Cheng351, Dan598 and JiV203 explained 62.89 to 82.25%, 43.19 to 61.51% and 54.70 to 75.77% of the phenotypic variation, respectively. Among all FER-resistant QTLs detected, qRfer1, qRfer10, and qRfer17 accounted for the phenotypic variation as high as 26.58 to 43.36%, 11.76 to 18.02%, and 12.02 to 21.81%, respectively. Furthermore, QTLs mapped in different F2 populations showed some extent of overlaps indicating potential resistance ‘hotspots’. The FER-resistant QTLs detected in this study can be explored as useful candidates to improve FER-resistance in maize by introducing these QTLs into susceptible maize inbred lines using molecular marker-assisted selection.

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Evaluation of Maize Inbred Lines for Resistance to Fusarium Ear Rot and Fumonisin Accumulation in Grain in Tropical Africa

Plant Disease ◽

10.1094/pdis-91-3-0279 ◽

2007 ◽

Vol 91 (3) ◽

pp. 279-286 ◽

Cited By ~ 42

Author(s):

C. G. Afolabi ◽

P. S. Ojiambo ◽

E. J. A. Ekpo ◽

A. Menkir ◽

R. Bandyopadhyay

Keyword(s):

Disease Severity ◽

Natural Infection ◽

Fusarium Verticillioides ◽

Field Trials ◽

Inbred Lines ◽

Artificial Inoculation ◽

Fusarium Ear Rot ◽

Ear Rot ◽

Maize Inbred Lines ◽

Resistant Lines

Fusarium ear rot and fumonisin contamination is a major problem facing maize growers worldwide, and host resistance is the most effective strategy to control the disease, but resistant genotypes have not been identified. In 2003, a total of 103 maize inbred lines were evaluated for Fusarium ear rot caused by Fusarium verticillioides in field trials in Ikenne and Ibadan, Nigeria. Disease was initiated from natural infection in the Ikenne trial and from artificial inoculation in the Ibadan trial. Ear rot severity ranged from 1.0 to 6.0 in both locations in 2003. Fifty-two inbred lines with disease severity ≤3 (i.e., ≤ 10% visible symptoms on ears) were selected and reevaluated in 2004 for ear rot resistance, incidence of discolored kernels, and fumonisin contamination in grain. At both locations, ear rot severity on the selected lines was significantly (P < 0.0020) higher in 2004 than in 2003. The effects of selected inbred lines on disease severity were highly significant at Ikenne (P = 0.0072) and Ibadan (P < 0.0001) in 2004. Inbred lines did not affect incidence of discolored kernels at both locations and across years except at Ikenne (P = 0.0002) in 2004. Similarly, significant effects of inbred lines on fumonisin concentration were observed only at Ikenne (P = 0.0201) in 2004. However, inbred lines 02C14585, 02C14593, 02C14603, 02C14606, 02C14624, and 02C14683 had consistently low disease severity across years and locations. Fumonisin concentration was significantly correlated with ear rot only at Ikenne (R = 0.42, P < 0.0001). Correlation between fumonisin concentration and incidence of discolored kernels was also significant at Ikenne (R = 0.39, P < 0.0001) and Ibadan (R = 0.35, P = 0.0007). At both locations, no significant inbred × year interaction was observed for fumonisin concentration. Five inbred lines, namely 02C14585, 02C14603, 02C14606, 02C14624, and 02C14683, consistently had the lowest fumonisin concentration in both trials. Two of these inbred lines, 02C14624 and 02C14585, had fumonisin levels <5.0 μg/g across years in trials where disease was initiated from both natural infection and artificial inoculation. These lines that had consistently low disease severity are useful for breeding programs to develop fumonisin resistant lines.

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Bioguided Isolation, Characterization, and Biotransformation by Fusarium verticillioides of Maize Kernel Compounds That Inhibit Fumonisin Production

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-04-14-0100-r ◽

2014 ◽

Vol 27 (10) ◽

pp. 1148-1158 ◽

Cited By ~ 15

Author(s):

Vessela Atanasova-Penichon ◽

Stéphane Bernillon ◽

Gisèle Marchegay ◽

Aurélia Lornac ◽

Laetitia Pinson-Gadais ◽

...

Keyword(s):

Chlorogenic Acid ◽

Inhibitory Activity ◽

Fusarium Verticillioides ◽

Fusarium Ear Rot ◽

Ear Rot ◽

In Planta ◽

Maize Genotypes ◽

Maize Genotype ◽

Rot Disease ◽

Susceptible Group

Fusarium verticillioides infects maize ears, causing ear rot disease and contamination of grain with fumonisin mycotoxins. This contamination can be reduced by the presence of bioactive compounds in kernels that are able to inhibit fumonisin biosynthesis. To identify such compounds, we used kernels from a maize genotype with moderate susceptibility to F. verticillioides, harvested at the milk-dough stage (i.e., when fumonisin production initiates in planta), and applied a bioguided fractionation approach. Chlorogenic acid was the most abundant compound in the purified active fraction and its contribution to fumonisin inhibitory activity was up to 70%. Moreover, using a set of maize genotypes with different levels of susceptibility, chlorogenic acid was shown to be significantly higher in immature kernels of the moderately susceptible group. Altogether, our data indicate that chlorogenic acid may considerably contribute to either maize resistance to Fusarium ear rot, fumonisin accumulation, or both. We further investigated the mechanisms involved in the inhibition of fumonisin production by chlorogenic acid and one of its hydrolyzed products, caffeic acid, by following their metabolic fate in supplemented F. verticillioides broths. Our data indicate that F. verticillioides was able to biotransform these phenolic compounds and that the resulting products can contribute to their inhibitory activity.

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