Biotic and abiotic factors associated with Fusarium ear rot of maize caused by Fusarium verticillioides
Fusarium ear rot, caused by Fusarium verticillioides, is one of the most common worldwide diseases of maize, causing yield and quality reductions as well as contamination of grain by fumonisins and other mycotoxins. Drought stress and various insects have been implicated as factors affecting disease severity. Three separate field studies were conducted during 2002 and 2003.
The first field study was conducted in Woodland, CA during 2002 and 2003, to evaluate the relative influence of 1) drought stress at different stages of crop development, and 2) ear infestation by two species of insects, upon severity of Fusarium ear rot disease and fumonisin B1 contamination of commercial maize hybrids. In each year, plots of three commercial hybrids varying in partial resistance to Fusarium ear rot were sown on three planting dates and subjected to four irrigation regimes that resulted in differing levels of drought stress in the plants. A foliar-spray insecticide treatment (sprayed vs. unsprayed) also was imposed. Populations of thrips (Frankliniella spp.) and damage by corn earworm (Helicoverpa zeae) in open-pollinated hybrid ears were assessed following pollination for all treatment combinations. Fusarium ear rot symptoms were assessed on mature grain subsamples, which were then analyzed to quantify fumonisin B1. For all hybrids, there were significant effects of planting date, insecticide treatment, and drought stress on Fusarium ear rot symptoms and fumonisin B1 contamination, and these factors also had significant interacting effects. The hybrids displayed their expected differences in susceptibility to Fusarium ear rot, and the more susceptible hybrids often had higher fumonisin B1 levels and thrips populations, depending on planting date. Later planting dates typically had higher thrips populations, more Fusarium ear rot, and higher levels of fumonisin B1. Plots treated with insecticide generally suffered lower levels of ear rot symptoms and fumonisin B1 contamination, especially in the susceptible hybrids and for the later planting dates when thrips populations were higher. Insecticide treatment successfully reduced thrips infestations in the Fusarium-susceptible hybrids, particularly for the later planting dates. Effects of drought stress were less pronounced than those of the other treatment factors, and were evident primarily in plots without insect control. An irrigation regime that promoted drought stress at anthesis sometimes resulted in higher levels of ear rot symptoms and fumonisin B1 contamination, but this effect was highly dependent on interactions with other factors. Intra-ear thrips populations and corn earworm injury were significantly correlated with disease severity and fumonisin contamination, but the correlations were weaker for corn earworm damage compared to thrips. The frequency of symptomatic kernels within a sample was strongly correlated with the concentration of fumonisin B1 in the sample. In summary, the results of this study agree with past results implicating thrips as a primary factor of Fusarium ear rot severity in California, and associate thrips with potentially high levels of fumonisin B1 in grain. Thrips appear to be a stronger influence on disease severity and fumonisin B1 contamination than earworm in this environment, and the historically higher disease severity in late plantings may be explained, at least in part, by higher thrips populations. Drought stress treatments did not influence ear rot severity in the presence of large populations of thrips and corresponding high disease severity and mycotoxin levels.
The second study was conducted in the 2002 and 2003 growing seasons in central California (Woodland), and the winter 2002 season in Hawaii (Waimea, island of Kauai). Plots were sown with a maize hybrid known to be susceptible to Fusarium ear rot. Half of the plots in each planting were treated with insecticides three times following pollination, while the remaining plots were not treated. Populations of intra-ear immature and adult thrips were subsequently evaluated at six ear developmental stages for the number of immature and adult thrips within developing ears. Grain samples from each plot were examined microscopically and the percentage of kernels with the silk-cut symptom was quantified on a weight basis. Grain subsamples from each plot were also analyzed by ELISA to quantify fumonisin B1 contamination. Maximum thrips populations for both locations and growing seasons occurred from 21 to 28 days after pollination (DAP). In both locations, the immature stages of thrips, including larvae, propupae, and pupae, predominated within maize ears at the brown-silk (21 to 28 DAP) stage. Insecticide treatment in all cases reduced numbers of adults and immatures within ears, as well as incidence of silk-cut symptom, and fumonisin B1 contamination. Numbers of immature thrips were higher than those of adults, and immature thrips populations were more strongly correlated with silk-cut symptoms (R = 0.75) and fumonisin B1 accumulation (R = 0.53), as compared to adult thrips (R = 0.48 and R = 0.36, respectively). Incidence of silk-cut kernels was highly correlated with contamination of grain by fumonisin B1 (R = 0.84). The results suggest that thrips are not simply occasional feeders on developing maize ears, but can complete a substantial portion of their life cycle on maize ears in Woodland and Waimea. The results also indicate that thrips oviposition and/or feeding may be implicated as causal factors of the silk-cut symptom that is common in many maize-growing areas, and this may be the mechanism that connects thrips activity with Fusarium ear rot and fumonisin contamination of grain.
The third study was conducted in Hawaii, California, Kansas, Iowa, Tennessee, and Georgia during the 2002 and 2003 growing seasons, to evaluate the associations of maize production regions, planting date, hybrid varieties, and ear infesting insect pests with Fusarium kernel rot symptoms, and fumonisin B1 contamination. In each season, plots of susceptible and resistant commercial maize hybrids were sown on 3 planting dates. Insects within open-pollinated hybrid ears at and following pollination were quantified for all genotype x planting date combinations at each location during each growing season. Grain subsamples were inspected to determine percentage of kernels that were either visibly molded or showed the starburst symptom of Fusarium ear rot. Grain samples were also analyzed by ELISA to quantify fumonisin B1 levels. Across locations, hybrid and planting date were both frequently significant effects ( p ≤ 0.05 ). Insect populations varied across locations, and observed kernel damage was most attributable feeding intra-ear thrips infestations. Maximum average intra-ear thrips populations were 161.8 (hybrid A, 2003), and 99.8 (hybrid B, 2002), in California and Hawaii. Across the pooled dataset, intra-ear thrips population was more strongly correlated (R = 0.78) than percentage lepidopteran kernel damage (R = 0.37), with percent visibly molded kernels. A similar trend was observed for the relationship between these two types of insects and the starburst symptom of Fusarium kernel rot. The percentage of visibly molded kernels was highly correlated (R = 0.89) with fumonisin B1 concentration (Table 4). Though significant, the correlation between starburst kernels and fumonisin B1 (R = 0.18) was substantially weaker. Intra-ear thrips populations were more strongly correlated with fumonisin B1 concentration (R = 0.89), compared to the correlation between percentage of lepidopteran kernel damage and fumonisin B1 (R = 0.34). A multiple linear regression model accounted for 84% (P < 0.001) of the variation in fumonisin B1. Given the strong association between thrips, Fusarium ear rot, and fumonisin B1, producers in the global F. occidentalis host range should consider thrips as a factor in Fusarium ear rot and fumonisin B1 management.